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Estuarine, Coastal and Shelf Science xxx (2012) 1e10

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Estuarine, Coastal and Shelf Science

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

Shifts in picophytoplankton community structure influenced by changingupwelling conditions

Virginie van Dongen-Vogels a,*, Justin R. Seymour b, John F. Middleton c, Jim G. Mitchell a,Laurent Seuront a,c,d

a School of Biological Sciences, Flinders University, GPO BOX 2100, Adelaide, South Australia 5001, AustraliabUniversity of Technology Sydney, PO Box 123, Broadway New South Wales 2007, Australiac South Australian Research and Development Institute (Aquatic Sciences), PO Box 120, Henley Beach, Adelaide, South Australia 5022, AustraliadCentre National de la Recherche Scientifique, Laboratoire d’Océanologie et de Géosciences, UMR LOG 8187, Université des Sciences et Technologies de Lille, Station Marine, 62930Wimereux, France

a r t i c l e i n f o

Article history:Received 30 May 2011Accepted 17 May 2012Available online xxx

Keywords:picoplanktonProchlorococcuscontinental shelvesupwellingEl Niño phenomenaSouth Australia

* Corresponding author.E-mail address: vand0267@flinders.edu.au (V. van

0272-7714/$ e see front matter � 2012 Elsevier Ltd.doi:10.1016/j.ecss.2012.05.026

Please cite this article in press as: van Donupwelling conditions, Estuarine, Coastal and

a b s t r a c t

The influence of upwelling events on the structure of picophytoplankton communities was assessed atthe annual scale from a station within the South Australian shelf region. In this region, local (wind) andglobal (La Niña/El NiñoeSouthern Oscillation) hydroclimatic conditions affect the development ofupwelling over the austral summer. Using flow cytometry, changes in picophytoplankton communitystructure were investigated in relation to the properties of the water column when the nature andstrength of upwelling event differed for the upwelling seasons of 2008, 2009, and 2010. In 2008, strongupwelling favorable southeasterlies were responsible for extensive upwelling and the dominance ofpicoeukaryotes. Alternatively, in 2009, the observed dominance of Prochlorococcus reflected the presenceof oligotrophic conditions whilst southeasterlies were replaced by downwelling favorable north-westerlies that likely prohibited the full development of upwelling. In 2010, whilst southeasterliesremained relatively weak, particularly cold and low saline upwelled waters indicated enhancedupwelling events. This weak local wind field together with the occurrence of El Niño explained theobservation of shallow upwelled waters below the warm surface layer and subsequent enhancedstratification. These conditions led to the dominance of Synechococcus in surface and fluorescencemaximum depths, but of Prochlorococcus in bottom upwelled waters. The tight association betweenupwelling and stratification, i.e. whether upwelled waters reach shallower depths and/or mix with thoseof the surface as a result of variable climatic conditions, was suggested as the process driving the verticalheterogeneity of picophytoplankton populations. This study brings valuable information for changingpicophytoplankton community structure with potential future changing hydroclimatic forcing.

� 2012 Elsevier Ltd. All rights reserved.

1. Introduction

Picophytoplankton (i.e. photoautrophic cells less than 2 mm indiameter; Sieburth et al., 1978) largely contribute to total phyto-plankton abundance, biomass, and production in the ocean(Chisholm et al., 1992; Vaquer et al., 1996; Partensky et al., 1999;Agawin et al., 2000; Marañón et al., 2001; Morán, 2007). Theyinclude three major groups that are Prochlorococcus, Synechococcus,and picoeukaryotes, which can in turn be subdivided into distinctecotypes or strains (Rocap et al., 2002; Rodríguez et al., 2005;Worden and Not, 2008). Because each of these groups are charac-terized by distinct physiological and ecological properties

Dongen-Vogels).

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gen-Vogels, V., et al., ShiftsShelf Science (2012), doi:10

(Partensky et al., 1999; Veldhuis et al., 2005), understanding thevariability in the relative importance of Prochlorococcus, Synecho-coccus, and picoeukaryotes is crucial to understand the fate ofcarbon and energy fluxes within and between ecosystems.

Current knowledge on picophytoplankton community structurein coastal upwelling systems is sparse (Hall and Vincent, 1990;Partensky et al., 1996; Sherr et al., 2005; Reul et al., 2006;Echevarría et al., 2009; Linacre et al., 2010; Daneri et al., 2012; vanDongen-Vogels et al., 2011) largely due to the fact that thesenutrient-enriched systems are typically seen as larger phyto-plankton (>20 mm) dominated systems (e.g. Herrera and Escribano,2006; Teixeira et al., 2011). Various studies have previously repor-ted changes in the relative contribution of distinct phytoplanktonsize classes in terms of both abundances and primary productionfor coastal upwelling systems (e.g. Iriarte and González, 2004;

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Herrera and Escribano, 2006; Cermeño et al., 2006). Despites thislack of information on the dynamic of picophytoplanktoncommunities, picophytoplankton could be important for nutrientand carbon transfer to higher trophic levels in such dynamicregions (e.g. Vargas et al., 2007; Morales and Anabalón, 2012). Pastand recent studies have nevertheless recorded the dominance ofSynechococcus, or picoeukaryotes, in surface waters of coastalregions influenced by upwelling, although more typically beingreported to growth within the diluted upwelled surface watersadvected offshore (Hall and Vincent, 1990; Partensky et al., 1996;Sherr et al., 2005; Echevarría et al., 2009). Upwelling coastal watersinvolving the uplift of deep cold nutrient-rich waters toward thesurface would be hostile to Prochlorococcus, known to dominate inwarm (>20 �C) oligotrophic open oceanic waters, having limitedgrowth below 12 �C (Partensky et al., 1999). Recent studies havehowever showed that distinct ecotypes of Prochlorococcus havetheir optimal growth rates at distinct temperatures with relativelyhigher cell abundances (c.a. 104 cells mL�1) of low light adaptedecotypes in relatively cold environments (<15 �C) in contrasted tothat of high light-adapted ecotypes being more restricted to warmoligotrophic waters (e.g. South East Atlantic, Zwirglmaier et al.,2008; Jameson et al., 2010, North West Atlantic, Zinser et al.,2007). The abundances dynamic of diverse picophytoplanktonpopulations has only been recently investigated in South Australiancontinental shelf waters where their high spatial and temporalvariability in abundances reflected the complex hydrodynamic ofthe shelf region, involving localized upwelling and downwellingevents (van Dongen-Vogels et al., 2011). Taken together thesepatterns indicate that varying upwelling conditions are likely toinfluence picophytoplankton community structure.

Fig. 1. Map of the South Australian continental shelf region showing the national referencewaters of the Flinders Current are upwelled over the austral summer.

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Summer upwelling events within the South Australian conti-nental shelf waters could be important to sustain the productivity ofthe highly valuable fisheries of the region (Ward et al., 2006; vanRuth et al., 2010). During summer, southeasterly upwelling favor-able winds and Ekman transport force cold (<16 �C) and low saline(<35.7) waters of the northern boundary current, the FlindersCurrent, onto the shelf through the du Couedic Canyon, locatedsouth off Kangaroo Island (KI, Fig. 1). The physical dynamic of thesummer upwelling season has previously been reviewed byMiddleton andBye (2007a, b) and involve the occurrence of single tomultiple upwelling events by pulse, each event potentially followedby intermittent periods of relaxation, mixing, or downwellingprocesses (Middleton and Platov, 2003; Kaempf et al., 2004;Middleton and Bye, 2007a, b; van Ruth et al., 2010). Due to thewidthof the shelf, upwelledwaters typically remain below the surface andhave previously been observed to slowly (c.a. 0.1 cm s�1) advectednorthwestward along the 100 m isobath of the shelf region(Middleton and Bye, 2007a, b; van Dongen-Vogels et al., 2011). Theprevailing hydroclimatic conditions such as the alongshore windand La Niña/El Niño Southern Oscillation (ENSO) may, however,strongly affect the depth atwhich deepwaters are upwelled and thestructure of the water column (Middleton and Bye, 2007a, b;Middleton et al., 2007). The high inter-annual variability in phyto-plankton community structure and production previously observedmay hence be ultimately controlled by local and large scale changesin hydroclimatic forcing (van Ruth et al., 2010; van Dongen-Vogelset al., 2011). In this context, the present study focuses on changesin picophytoplankton community structure at a single stationlocated directly on the path of the upwelled plume for three distinctupwelling events that occurred in the summer of 2008, 2009, and

station located off Kangaroo Island (NRSKAI) and the du Couedic Canyon from which

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2010. Changingpicophytoplanktoncommunities at thefluorescencemaxima, but also above and below these depths, yet previouslyunavailable, was then analyzed in relation to changes in the watercolumn structure as a result of varying upwelling conditions. Thiswill improve the current knowledge on how picophytoplanktoncommunity structure relate to upwelling-driven processes in SouthAustralian shelf waters where the microbial food web is likely to beimportant.

2. Material and method

Every one to three months from February 2008 to July 2010, 18researchcruiseswereperformedaboard theRVNgerin at theNRSKAIstation (35�50S,136�26E, Fig.1), a national reference station locatedwest of Kangaroo Island (KI) on the path of upwelling watersadvected from its source, the du Couedic Canyon (Kaempf et al.,2004; Middleton and Bye, 2007a, b). Collected hydrographic datafrom each cruise and hydroclimatic data were first explored toquantify changes in upwelling conditions observed over theupwelling season of 2008, 2009, and 2010. To track changes inphysical, biological and chemical parameters due to upwelledwaters, we particularly focused on the surfacemixed layer (15m), atthefluorescencemaximum(SCM; identified as themaximum in vivofluorescence fromvertical profiles), and in the bottom layer (100m).To determine a potential mechanism between upwelling and pico-phytoplankton community structure we analyzed the bulk condi-tions of thewater column and picophytoplankton abundances fromthe February cruise of each upwelling season, i.e. when the pres-ence/absence and intensity of upwelling conditions differed.

2.1. Hydroclimatic parameters

El Niño and La Niña conditions were evaluated using theSouthern Oscillation Index (SOI) given by the Australian Bureau ofMeteorology. The method used by the Australian Bureau of Mete-orology is the Troup SOI, which refers to the standardized anomalyof the Mean Sea Level Pressure difference between Tahiti andDarwin (http://www.bom.gov.au/climate/glossary/soi.shtml).

Changes in upwelling and downwelling favorable wind condi-tions were evaluated from changes in alongshore wind stressaccording to Middleton et al. (2007) and van Ruth et al. (2010).Wind data were automatically recorded at the Neptune Island

Fig. 2. Exemple of a cytogram showing the distinct analyzed picophytoplankton populations(SCC).

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weather station and were provided by the Australian Bureau ofMeterology. Monthly averages were considered here to be consis-tent with the SOI data.

2.2. Biological and chemical parameters

Seawater was collected in the surface mixed layer (15 m), at thechlorophyll fluorescence maximum, and in the bottom layer using5 L-Niskin bottles from which, three subsamples of (i) 50 mL ofseawater were filtered through bonnet syringe filters (Micro Ana-lytix Pty Ltd) and stored at �20 �C for nutrient analysis, (ii) 300 mLof seawater were filtered through fiber glass filters (Whatman GF/C) and stored at �20 �C for chlorophyll a analysis, and, (iii) 1 mL ofseawater were fixed with paraformaldehyde (2% final concentra-tion), frozen in liquid nitrogen, and stored at �80 �C for picophy-toplankton analysis.

Nutrient analysis was performed according to the LachatQuickchem methods for phosphate (PO4, detection limit; 0.03 mM),nitrate þ nitrite (NOx, detection limit; 0.07 mM), and ammonium(NH4, detection limit; 0.07 mM) on a QuickChem QC8500 Auto-mated Ion Analyser. Chlorophyll a was extracted by placing eachfilter in 5 ml of methanol for 24 h in the dark at 4 �C (Welschmeyer,1994) and chlorophyll a (Chl a) concentration was determinedusing a Turner 450 fluorometer previously calibrated with chloro-phyll a extracted from Anacystis nidulans (Sigma Chemicals, StLouis). The chlorophyll concentrations determined fromGF/C filterswere used here as a standard for environmental parameter formicrophytoplankton pigment concentration, allowing comparisonwith previous investigations in the region (e.g. McClatchie et al.,2006; van Ruth et al., 2010; van Dongen-Vogels et al., 2011).Abundances and fluorescence properties of distinct picophyto-plankton populations were analyzed by running each sample for5 min on a FacsCanto flow cytometer from Becton Dickinson (Marieet al., 1999; van Dongen-Vogels et al., 2011). Synechococcus, Pro-chlorococcus, and picoeukaryotes were identified based on theirautofluorescence and light scatter properties using the softwareFlowJo (TreeStar). Although distinct populations of picoeukaryotes,Prochlorococcus and Synechococcus were recently reported withinthe South Australian shelf waters (van Dongen-Vogels et al., 2011),only two distinct Prochlorococcus e like populations (Proc1, Proc2)could be consistently characterized by distinct SSC and Fl3 signalsalong the present study (Fig. 2). Mean red fluorescence per cell was

characterized by their pigment cell content (red autofluorescence, FL3) and side scatter

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reported as an indication of the amount or conditions of chlorophyllpigment per picophytoplankton cell (e.g. Moore et al., 1995;Blanchot et al., 2001).

2.3. Physical parameters

For each cruise, vertical profiles were performed with a SeabirdSBE 19plus CTD system mounted with a biospherical PAR sensorand a Wet Star fluorometer probe (WetLabs). Pressure, conduc-tivity, temperature, light irradiance, fluorescence concentrations,and derived salinity, depth, and density of the water column werethen processed using Seabird SBE data processing win32 software.Pressure, temperature, salinity and density data were then used tocalculate a stratification index based on the potential energyanomaly PEAz (J m�3; Simpson, 1981; Mann and Lazier, 1996)defined as:

PEAz ¼ 1=HZ

gz ðr� rÞdz (1)

where r is the water density, r the depth-averaged density

(r ¼ 1H

Z 0

�Hrdz), H the water column depth, g the gravitational

acceleration, and z is a given depth. High PEAz values representstrong and stable density stratification of the water column,whereas low PEAz values represent unstable water column due tomixing and downwelling process (Mann and Lazier, 1996). Giventhe dependence of the stability of the water column upon thedistribution of heat and salt in the ocean, the vertical variation ofthe potential density, r, was further considered as a function of

Fig. 3. Temporal changes in hydroclimatic forcing (a) from February 2008 to July 2010 are sconditions and negative values for El Niño conditions, and the alongshore wind stress beingin the physical structure of the water column (b) and sampled layer depths (c, d). Potential ean index of stratification. The combined temperature and salinity gradients between the sactivity occurring in the austral summer of each year that led to differences in stratificatio

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temperature ðqÞ and salinity (S). Given Eq. (1), the effect of thevariations in temperature and salinity separately to the stabiliza-tion of the water column was thus defined as follow:

PEAzðTÞ ¼ 1=HZ

gz ðrðq; SÞ � rÞdz (2)

PEAzðSÞ ¼ 1=HZ

gzðrðS; qÞ � rÞdz (3)

where q and S are the average temperature and salinity of the watercolumn, respectively. Finally, the difference between equations (2)and (3), PEAz(T)ePEAz(S), allowed for a distinction between strati-fication due to (i) cold and low saline upwelled waters, and (ii)temperature gradients alone which is typical for the summer oftemperate systems. This latter consideration was based on theearlier works of Budeus (1989) and Czitrom, 1982 who used theratio between density and salinity gradients to differentiate thecontribution of salinity gradients alone from that of temperature tototal density gradients.

3. Results and discussion

3.1. Hydroclimatic conditions and upwelling strength

As indicated by the Southern Oscillation Index (SOI) and along-shore wind stress, the nature, intensity and duration of upwellingfavorable conditions varied markedly between the three yearsstudied (Fig. 3a). In the long-term, themonthlyaveraged alongshorewind stress showed stronger upwelling favorable winds (positive

hown by the Southern Oscillation Index (SOI) with positive values indicative of La Niñaupwelling favorable when negative and downwelling when positive. Temporal changesnergy anomalies of the water column (PEAz and PEAz(T) � PEAz(S)) were considered asurface and bottom layer depths showed the intensity and duration in the upwellingn intensity and duration. Selected sampling cruises for this study are hashed in grey.

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alongshorewind stress values) over the 2008 upwelling season thanover that of the year 2009 or 2010 (Fig. 3a). Fluctuation in SOI indi-cated the alternance of La Niña (positive SOI) and El Niño (negativeSOI) events over the study period (Fig. 3a). Although a seeminglypositive link between SOI and wind data is noticed during El Niño(Fig. 3a), this relationship is clearly uncertain at such short timescales. Nevertheless, the present observed long-term trend agreedwith past investigations showing the absence of long-term rela-tionship between ENSO and localwindfieldfluctuations (Middletonet al., 2007). The physical effect of El Niño on the upwelling season ofthe South Australian continental shelf region hence differ from thatobserved in the Eastern Pacific upwelling coastal regions, whereshorter and less intense windedriven upwelling events are relatedto El Niño (e.g. Montecinos and Gomez, 2010).

Differences observed between upwelling seasons in the hydro-climatic conditions were reflected in the potential energy anoma-lies of the water column which showed, for instance, morepersistent stable stratification (Fig. 3b) over the 2010 upwellingseason but relatively unstable stratified water column over the2008 and 2009 ones (Fig. 3b). This variation in the intensity ofstratification over the upwelling season is perceptible from thedifferences between the potential energy anomalies expressed asa function of temperature and salinity (Fig. 3b). The presence ofupwelled waters influenced both salinity and temperature gradi-ents, but temperature gradients also result from the summerwarming of surface waters. Upwelled waters were characterized bytemperature and salinities below 15 �C and 35.5 (Fig. 3c, d,McClatchie et al., 2006; Middleton and Bye, 2007a, b). Dependingon the frequency of upwelling pulses, a greater difference intemperature and salinity between the sampled depths suggeststhat multiple upwelling events successively occurred as deeperwaters may have accumulated on the continental shelf slope(Kaempf et al., 2004; McClatchie et al., 2006; Middleton and Bye,2007a, b). In contrast, a smaller difference would reflecta discrete upwelling event. The observed fluctuations in stratifica-tion intensities and in the differences between temperature andsalinity recorded at the distinct depths (Fig. 3bed) hence suggestthe occurrence of single (e.g. February 2009) or multiple (e.g.February toMarch 2008, November 2009 toMarch 2010) upwellingevents that may have been intermitted by mixing or downwellingperiods (i.e. drop in temperature and/or salinity differencesbetween sampled depths, e.g. December 2009; Fig. 3ced).

Theweakmonthly averaged upwelling favorablewinds over boththe 2009 and 2010 upwelling seasons could not, however, explainalone the differences in temperature and salinity and stratificationobserved between these two seasons. Peaks of strong downwellingfavorable winds recorded over the 2009 upwelling season (notshown) most likely reduced the potential full development ofupwelling. On the other hand, enhanced stratification and upwellingevents have been shown to result from an input of a distinct coldwater source to the Flinders Current during El Niño event (Middletonet al., 2007). Specifically, El Niño promotes the poleward propagationof a cold coastal trapped waveguide along the western side ofAustralia which is then further directed along the southern side ofAustralia. The encountering of the coastal trapped waveguide to theFlinders Current at the shelf break off South Australia may have hel-ped the accumulation and uplift of colder waters (Middleton et al.,2007). These upwelled waters do not, however, reach the surfacebecause of the relatively wide shelf in this region and its specifictopography. As such, when (i) upwelled waters reach shallowerdepths, (ii) are colderor less salineor (iii) sea surface temperatures arehigher, stratification intensifies. The observed changes in upwellingconditions and stratification intensities (Fig. 3bed) could have beenhence ultimately driven by the combined local wind field, theoccurrence of El Niño, and shelf topography.

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3.2. Upwelling strength and changes in the water columnproperties

Upwelled waters of temperatures and densities respectivelybelow 15.5 �C and above 26 laid below 70m in February 2008, wereabsent in February 2009, and reached a depth of 40 m in February2010 (Fig. 4). In February 2008, the surface mixed layer was rela-tively cold for the summer. The long lasting southeasterlies favoredvertical mixing between the cold upwelled waters and the warmupper mixed layer, with subsequent cooling and nutrient enrich-ment, and, the development of a thick and strong subsurfacefluorescence maximum (SCM, Fig. 4). In contrast, enhanced strati-fication due to El Niño conditions in February 2010 led to relativelylow nutrient concentrations the upper depths and strong shallowthermocline and pycnocline. The thin and weak subsurface SCMobserved in February 2010 contrasted with that observed in 2008.Such differences likely reflected a greater C/Chl a ratio due to thepresence of larger phytoplankton cells in 2008 in contrasted to thatobserved in 2010. Although the location of the SCM relative to thethermocline and nutrient concentrations differed betweenupwelling events of 2008 and 2010, chl a concentrations greaterthan 1 mg l�1 were recorded for both years (Table 1). Similar chla concentrations were previously recorded for the region duringthe 2004 wind-driven upwelling season (van Ruth et al., 2010), butwere about four times lower than that of themajor upwelling eventrecorded in March 1998 (Kaempf et al., 2004), an El Niño upwellingseason. Although Kaempf et al. (2004) were not aware of thepotential influence of El Niño to upwelling activity, the strongerupwelling favorable winds that occurred during their study mayhave explained the differences observed between the presentresults and those of Kaempf et al. (2004). On the other hand, thevertical structure of the water column in February 2009 presenteda weak fluorescence maximum below a deep thermocline (Fig. 4)with chl a concentrations not exceeding 0.1 mg l�1 and nutrientconcentrations increasing below the thermocline (Table 1),reflecting oligotrophic conditions (e.g. Marañon et al., 2001).

3.3. Changes in picophytoplankton community structure withupwelling strength

Picophytoplankton abundances (Table 1) were between thosepreviously observed in eutrophic and oligotrophic waters (e.g.Campbell et al., 1997; Partensky et al., 1999; Durand et al., 2001;Sherr et al., 2005; Zwirglmaier et al., 2008; Echevarría et al., 2009)and agreed with those recently reported for the present region (vanDongen-Vogels et al., 2011). Each picophytoplankton group showeda maximum abundance value specific to each observed upwellingcondition (i.e. fluorescence maximum (SCM) in February 2010 forSynechococcus, surface in February 2009 for Prochlorococcus, andSCM in February 2008 for picoeukaryotes) while lowest cellabundances were reported for all three groups in bottom coldnutrient rich upwelled waters recorded in February 2010 (Table 1).

In surface waters, Synechococcus mainly dominated bulk pico-phytoplankton abundances, although differences between Syn-echococcus and Prochlorococcus absolute abundance values weretwo times lower in February 2009 than in 2010, Prochlorococcusabundances being lower in 2010 (Fig. 5, Table 1). In contrast,picoeukaryotes absolute and relative abundances were higher inFebruary 2010. These observed differences in the abundances ofeach picophytoplankton group between years (Fig. 5, Table 1) mightbe explained by their difference in surface to volume ratio (e.g.Raven, 1998; Veldhuis et al., 2005) together with (i) a potentialload of nutrients from upwelled waters through small shearprocesses prior to sampling in February 2010, and, (ii) the shallowerupwelled waters observed in February 2010 (Fig. 4). Shifts in

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Fig. 4. Vertical structure of temperature, density (sigma-t), and chlorophyll fluorescence of the NRSKAI station in February 2008, 2009, and 2010. As indicated by temperatures anddensities below 15 �C and above 26.5, the signature of upwelled waters was observed in February 2008 and 2010, but not in 2009. Note the difference in the scale of the fluorescenceand in the relative position of the subsurface fluorescence maximum depth to the mixed layer depth between years.

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picophytoplankton community structure between years wereparticularly marked at the fluorescence maxima (SCM, Fig. 5).There, picoeukaryotes dominated bulk picophytoplankton abun-dances in 2008, Prochlorococcus in 2009, and Synechococcus in2010. Changes in picophytoplankton community structure reflectedthe inter-annual variability in stratification intensity associatedwith upwelling conditions and in the location of the SCM depthsrelative to those of the thermocline and pycnocline (Table 1, Fig. 4).

In February 2009 and 2010, the vertical variability in picophy-toplankton communities was marked by the inverse relativecontribution of two distinct populations of Prochlorococcus (Proc1,Proc2) with depths (Fig. 5). This vertical segregation between Proc2and Proc1 suggests that Proc1 may represent one high-light andProc2 one low-light adapted ecotypes of the Prochlocococus genera(West and Scanlan, 1999; Johnson et al., 2006). Because of the lowvertical resolution of our sampling strategy, their niche partitioningwas not apparent. However, Proc2 was absent in the surface depthsand accounted for less than 30% of the total Prochlorococcusabundances at the SCM. In contrast, at the bottom, Proc2 accountedfor 77 and 92% of the total Prochlorococcus and for 41 and 56% of thetotal picophytoplankton in 2009 and 2010, respectively.

Synechococcus contributed the most to bulk picophytoplanktonchlorophyll in surface waters and only in SCM waters in February2010, whereas picoeukaryotes made the most of picophyto-plankton chlorophyll at the SCM and bottom depths (Table 1).These dominances, both in terms of chlorophyll content andabundance, of picoeukaryotes and Synechococcus in the presence ofupwelled waters conformed to those previously reported in thesurface waters of other coastal regions affected by upwelling (Halland Vincent, 1990; Sherr et al., 2005; Echevarría et al., 2009). Therelationship between the amount of chlorophyll content per celland abundances also differed between picophytoplankton groups(Fig. 6), likely reflecting their differential capacity of physiological

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adaptation to changing light levels (e.g. Veldhuis and Kraay, 1990;Moore et al., 1995; Dusenberry et al., 2000). For instance, thesignificant inverse relationship between cell abundances and redfluorescence for Synechococcus showed important photo-acclimation processes. This was also shown by its increasing chlo-rophyll content per cell but decreasing cell abundances with depth(Fig. 6). In contrast, the absence of significant relationship betweencell abundances and red fluorescence for picoeukaryotes suggeststhe presence of diverse picoeukaryotes with distinct potential ofphotoacclimation (Fig. 6). Further insights into the nature of thedistinct populations identified here through flow cytometry couldbe provided by molecular approaches. The molecular character-ization of the picoeukaryotic populations remains too rudimentaryto currently provide a complete characterization of the community,only recently being achieved (Massana et al., 2004, 2011).

Besides changing light levels, the low temperatures of upwelledwaters might limit the growth of picophytoplankton, and especiallyProchlorococcus. Low temperatures have previously explained theirreduced cells abundance or absence in polar or coastal regionsaffected by seasonal changes in the ocean hydrodynamic, includingcoastal upwelling systems. The relatively high abundance of Pro-chlorococcus observed here (up to 104 cells ml�1) however fallwithin the upper ranges of past recorded Prochlorococcus abun-dances found elsewhere at temperatures below 15 �C (Table 2). Insummer, surface temperatures above 15 �C may however be criticalfor the growth of Synechococcus and Prochlorococus at the upperdepths of the sampled station, both groups being able to thrive innutrients depleted waters (Durand et al., 2001; Tai and Palenik,2009). At the bottom, abundances of all picophytoplanktongroups were largely reduced in cold (c.a. 12 �C) and high nitrateupwelled waters (i.e. February 2010, Table 1, Fig. 5) when comparedwith warmer and lower NOx conditions (i.e. February 2009, Table 1,Fig. 5). Nevertheless, the present finding that Prochlorococcus

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Table 1Nutrients (mM) and chlorophyll a (mg L�1) concentrations, picophytoplankton abundances (�103 mL�1), and the relative contribution of red fluorescence (%) of each populationobserved at the surface, subsurface chlorophyll maximum (SCM), and bottom sampled depth (m) for each February of the 2008, 2009, and 2010 upwelling season. Note:‘<’:lower than limit of detection, ‘e’:absent.

Surface FM Bottom

Feb-09 Feb-10 Feb-08 Feb-09 Feb-10 Feb-09 Feb-10

Depth 15 15 28 62 30 92 103NH4 < < 0.1 < < 0.1 <

NOx < 0.4 1.3 0.2 0.0 2.0 8.8PO4 < < 0.1 0.1 < 0.2 0.5Chl a 0 to 0.1 0.5 to 0.8 1.3 0.1 1 to 1.1 0.1 0.4 to 0.8AbundanceSyn 35.1 to 53.4 35.4 to 113.4 7.9 to 9.5 1.8 to 2.2 57.8 to 137.5 2.6 to 4.2 1.0 to 1.4Proc1 44.4 to 59.7 15.1 to 45.8 6.4 to 6.8 4.7 to 5.2 27.4 to 56.5 1.1 to 1.5 0.4 to 0.5Proc2 e e 0.1 to 0.6 1.9 to 2.3 e 7.6 to 11.2 1.3 to 1.6Euk 0.9 to 1.8 1.7 to 5.3 21.3 to 32.9 0.9 to 2.1 2.7 to 3.3 3.4 to 4.7 0.5 to 0.6Relative mean red fluorescenceSyn 47.6 to 60.4 63.3 to 63.6 3.3 to 7.4 18.4 to 22.8 77.0 to 84.2 13.4 to 14.3 33.1 to 36.2Proc1 14.8 to 22.5 8.0 to 9.1 0.2 to 0.5 4.6 to 8.7 6.9 to 7.3 0.3 to 0.4 0.5Proc2 e e 0 to 0.1 5.6 to 8.8 e 10.8 to 12.7 7.6 to 8.7Euk 17.1 to 37.6 27.0 to 28.7 92.1 to 96.4 59.6 to 71.5 8.8 to 15.7 73.5 to 74.6 55.8 to 57.7

Fig. 5. Vertical and annual changes in the relative contribution of Prochlorococcus,Synechococcus and picoeukaryotes (bars) to total picophytoplankton abundances(dashed line) at the surface, fluorescence maximum (SCM), and bottom layer depthsfor February 2008, 2009, and 2010.

Fig. 6. Mean red fluorescence as a function of abundances for eukaryotes (Euk), Syn-echococcus (Syn) and Prochlorococcus (Proc1, Proc2) at the surface (black diamond),fluorescence maximum (grey squares), and bottom (open circles) depths.

V. van Dongen-Vogels et al. / Estuarine, Coastal and Shelf Science xxx (2012) 1e10 7

Please cite this article in press as: van Dongen-Vogels, V., et al., Shifts in picophytoplankton community structure influenced by changingupwelling conditions, Estuarine, Coastal and Shelf Science (2012), doi:10.1016/j.ecss.2012.05.026

Table 2Prochlorococcus abundances (Abs) recorded in diverse cold (c.a. < 15 �C) environments. LL: Low-Ligth.

Region T (�C) Abs (�103 ml�1) References Notes

Meditteranean SeaNW Mediterranean Sea <14 40 Vaulot et al., 1990 Winter surface watersAtlanticNorth Atlantic Ocean <15 <10 Buck et al., 1996

10.2 8<15 6.8 þ/� 12.8

SE to NE Atlantic 7 to 19 Few to >0.1 Johnson et al., 2006 LL with higher abs at T ¼ 13 �C passed 40�S than passed 40�NSE Atlantic 12 to 13 15 to 51 Zwirglmaier et al., 2007 LL genotypes found throughout the mixed water columnPacificSouthern California Bight 32.53�N, 117.15�W 13 to 15 Absent to 40 Worden et al., 2004 Proc dominated bulk picophytoplankton when T ¼ 15 �CEast China Sea (transitional waters) 6 to 17.1 Absent to 6 Jiao et al., 2005 Winter waters

15.6 0.3 Lowest winter T for Proc to be present14.3 4 summer stratified cold waters

South East Pacific <20 <0.1 Zwirglmaier et al., 2008 LL ecotype observed deep down in mixed watersonly detectable south of 60�N

Southern Ocean34. 8 to 55.0�S at about <10.64 Absent Doolittle et al., 2008 Only detectable north of 38�S10�W to 10�E 14.3 to 15.7 10 to >100 Proc dominated bulk picophytoplankton when T > 14 �C

V. van Dongen-Vogels et al. / Estuarine, Coastal and Shelf Science xxx (2012) 1e108

(potentially a LL-adapted ecotype) can also dominate bulk pico-phytoplankton abundances in relatively deep coastal nutrient-richupwelled waters as cold as 12 �C (Figs. 4e6, Table 1) was in linewith previous studies showing relatively abundant LL-adaptedecotypes in cold waters (Table 2) and the great potential micro-diversity of various Prochlorococcus ecotypes being to grow indiverse ecological niches (e.g. Johnson et al., 2006; Zinser et al.,2007; Zwirglmaier et al., 2007; Martiny et al., 2009; Boumanet al., 2011).

Overall, the observed inter-annual change in picophytoplanktoncommunity structure was associated to changes in the physicalproperties of the water column reflecting the importance of strat-ification and upwelling processes. Under relativelyweak or absenceof upwelling event (i.e. easterly upwelling favorable winds, El Niñocondition, temperature of <15.5 �C, salinity >35.5, February 2009),Prochlorococcus is likely to dominate the picophytoplanktonstanding stock because of the development of deep stratificationleading to oligotrophic conditions which may have reduced thedevelopment of picoeukaryotes and Synechococcus. The presence oftwo distinct Prochlorococcus-like ecotypes showing distinct nichepartitioning and physiological adaptation (e.g. Figs. 2, 5 and 6;Zinser et al., 2007) also likely allowed for the extended dominanceof this group on the vertical. Under relatively strong upwellingevent, the dominance of picoeukaryotes and Synechococcus topicophytoplankton standing stocks are both likely to take place atthe SCM, but the former could be dependent on the occurrence ofmixing processes between the nutrient-rich upwelled andnutrient-depleted uppermixedwaters (i.e. February 2008 vs. 2010).This is consistent with the faster growth rates of larger phyto-plankton cells under mixing conditions (e.g. Raven,1998; Partenskyet al., 1999) and the increasing absolute and relative abundances ofpicoeukaryotes below the thermocline in the presence of highernutrients concentrations in the bottom layer (Fig. 5, Table 1). Incontrast, upwelling activity and enhanced stratification likelyallowed the dominance of Synechococcus during El Niño. Althoughthe physical processes involved in the effect of El Niño on upwellingevents observed here might differ from that of the Eastern Pacific(e.g. Chavez et al., 2002; Masotti et al., 2011) and Western TropicalPacific regions (e.g. Blanchot and Rodier, 1996), the high Synecho-coccus abundances (>104 cells ml�1) observed at the surface andSCM depths were similar to those reported in these above regionsof the Pacific, being in all cases the result of an increase in abun-dances between the early to later stages of El Niño (van Dongen-Vogels, unpublished data; Blanchot and Rodier, 1996; Chavez

Please cite this article in press as: van Dongen-Vogels, V., et al., Shiftsupwelling conditions, Estuarine, Coastal and Shelf Science (2012), doi:10

et al., 2002; Masotti et al., 2011). Such coincidence betweendistinct geographical environments calls for further work to enableto depict the potential mechanistic linkages between Synecho-coccus and El Niño events, but yet question its ecological meaning.

Finally, the succession of distinct dominant picophytoplanktonpopulations possibly also occurred following upwelling due tointermittent mixing and downwelling in between upwelling pulsesand the subsequent redistribution of nutrients in the water column(Fig. 2, Table 1, McClatchie et al., 2006; Middleton and Bye, 2007a,b). The better adapted population to changing local water condi-tions will have then rapidly increased in abundances. The differ-ential dependence of temperatures, light availabilities, and nitrateconcentrations to the growth and abundances of distinct picophy-toplankton groups, ecotypes, or strains together with changes instratification intensity associated to varying upwelling conditionslikely explained the depth heterogeneity in picophytoplanktoncommunity structure observed here.

4. Conclusions

Changing wind conditions were recently suggested to affectthe productivity and community structure of the Concepciónupwelling area (Daneri et al., 2012). Here, variable upwellingconditions associated to climatic forcing (wind field and El Niño)was suggested as the process influencing vertical and annualchanges in picophytoplankton community structure, abundances,and fluorescence properties within the continental shelf of SouthAustralia. Wind-driven upwelling event could be expected toresult in rather homogeneous distribution of phytoplankton pop-ulations through mixing. However, depending on the strength ofupwelling favorable winds and the occurrence of El Niño, thedepth reach by upwelled waters might differ, resulting in varyingmixing and stratification intensity. The local topography charac-terized by a relatively wide continental shelf and the presence ofislands might also have affected mixing between upwelled andsurface waters around the sampled station (i.e. Figs. 3 and 4). Thestrong patterns observed here indicate that the hydroclimaticvariability observed in this location may exert a strong influenceon the microbial ecology of this region. Further studies investi-gating the influence of these processes on other groups of theprokaryotic and eukaryotic plankton will be useful for betterintegrating microbial food-web processes into temporal hydro-climatic variability.

in picophytoplankton community structure influenced by changing.1016/j.ecss.2012.05.026

V. van Dongen-Vogels et al. / Estuarine, Coastal and Shelf Science xxx (2012) 1e10 9

Acknowledgment

We thank the crew of the RV Ngerin for their valuable help withdata collection at sea. Data was sourced as part of the IntegratedMarine Observing System (IMOS) e IMOS is supported by theAustralian Government through the National CollaborativeResearch Infrastructure Strategy and the Super Science Initiative.This research was also supported under Australian ResearchCouncil’s Discovery Projects funding scheme (projects numberDP0664681 and DP0988554) and the Government of SouthAustralia through the Marine Innovation South Australia (MISA)initiative. Professor L. Seuront is the recipient of an AustralianProfessorial Fellowship (project number DP0988554). V. vanDongeneVogels is the recipient of an Endeavour InternationalPostgraduate Research Scholarship (EIPRS) funded by the Austra-lian Government through the Department of Innovation, Industry,Science and Research.

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