flow cytometry investigation of picoplankton across latitudes and along the circum antarctic ocean

Acta Oceanol. Sin., 2012, Vol. 31, No. 1, P. 134-142

DOI: 10.1007/s13131-012-0185-0

http://www.hyxb.org.cn

E-mail: [email protected]

Flow cytometry investigation of picoplankton across

latitudes and along the circum Antarctic Ocean

LIN Ling1,2, HE Jianfeng2, ZHAO Yunlong1∗, ZHANG Fang2, CAI Minghong2

1 College of Life Science, East China Normal University, Shanghai 200062, China

2 Key Laboratory for Polar Science of State Oceanic Administration, Polar Research Institute ofChina, Shanghai 200136, China

Received 8 November 2010; accepted 21 September 2011

©The Chinese Society of Oceanography and Springer-Verlag Berlin Heidelberg 2012

AbstractUsing a flow cytometer (FCM) onboard the R/V Xuelong during the 24th Chinese Antarctic cruise,picoplankton community structure and biomass in the surface water were examined along the lat-itude and around the Antarctic Ocean. Salinity and temperature were automatically recordedand total Chl a was determined. Along the cruise, the abundance of Synechococcus, Prochlorococ-cus, pico-eukaryotes and heterotrophic bacteria ranged in 0.001–1.855×108 ind./L, 0.000–2.778×108

ind./L, 0.002–1.060×108 ind./L and 0.132–27.073×108 ind./L, respectively. Major oceanic distri-bution of Synechococcus and Prochlorococcus appeared between latitudes 30◦N and 30◦S. Prochloro-coccus was mainly influenced by water temperature, water mass combination and freshwater inflow.Meanwhile, Synechococcus distribution was significantly associated with landing freshwater inflow.Pico-eukaryotes and heterotrophic bacteria were distributed all over the oceans, but with a rela-tively low abundance in the high latitudes of the Antarctic Ocean. Principal Component Analysisshowed that at same latitude of Atlantic Ocean and Indian Ocean, picoplankton distribution andconstitution were totally different, geographical location and different water masses combinationwould be main reasons.

Key words: picoplankton, distribution, Antarctic Ocean, FCM

1 Introduction

Picophytoplankton (� 2 µm), including Prochl-orococcus, Synechococcus, and pico-eukaryotes, are nu-merical and biomass dominants in the open oceans(Brown et al., 1999). These tiny primary produc-ers greatly contribute to both total phytoplanktonbiomass and production in marine ecosystems. Inoligotrophic waters, they account for up to 90% ofthe total photosynthetic biomass and carbon produc-tion (Li et al., 1983; Campbell et al., 1994). Het-erotrophic bacteria typically are considered solely asdecomposers in marine ecosystems, to which bacte-ria are also important biomass contributors (Azamet al., 1983). The technique of flow cytometry pro-vides precise quantitative assessments of the four ma-jor picoplankton groups in the open ocean (Chisholm

et al., 1988). Research on picophytoplankton in vari-ous waters of the Pacific (Binder et al., 1996; Landryet al., 1996; Kazuhiko et al., 2004), Atlantic (Yvesand Awa, 2007; Camila et al., 2008), and AntarcticOceans (Brown and Landry, 2001; Ehnert and McRoy,2007) has demonstrated the importance of picoplank-ton throughout the world’s oceans. In China, researchwork towards the Southern Ocean (Ning et al., 1996)and Prydz Bay (Antarctica) (Ning et al., 1993) by epi-fluorescence microscopy and fractionated chlorophyllmethod also demonstrated the distribution character-istic of picophytoplankton at Antarctica Ocean. How-ever, there is no comparison among continuous dis-tributions of the picoplankton at the surface water indifferent oceanic provinces. Amusedly, the CHINARE24 (24th Chinese National Antarctic Research Expe-dition) cruise provided such an opportunity, that is,

Foundation item: The National Natural Science Foundation of China under contract Nos 40576002 and 40006010; the Key In-ternational S & T Cooperation Projects under contract No. 2008DFA20420; the Youth Scientific and Technological InnovationFoundation of Polar Research Institute of China under contract No. JDQ200802; the Polar Strategic Research Foundation undercontract No. 2008209; the LMEB Open Research Foundation under contract No. LMEB200902; and the PhD Program ScholarshipFund of ECNU under contract No. 2010041.

∗Corresponding author, E-mail: [email protected]

1

LIN Ling et al. Acta Oceanol. Sin., 2012, Vol. 31, No. 1, P. 134-142 135

conducting a large-scale investigation of picophy-toplankton and heterotrophic bacteria distributionwithin widespread oceanic provinces, including thewestern Pacific, East Indian, Antarctic Ocean, andSouthwestern Atlantic Oceans. The goal of this studywas exactly determining the distribution pattern ofpicoplankton in the above oceanic provinces along alatitudinal gradient and around the Antarctic Ocean.

2 Material and methods

The study was carried out during the CHINARE24 cruise from 12 November 2007 to 15 April 2008with R/V Xuelong. Figure 1 shows the locations ofthe sampling stations. At 6:00, 12:00, 18:00, and 24:00each day during the cruise, samples were collected bythe onboard Surface Seawater Sample System. Salin-ity and temperature were automatically recorded by aSBE21 SEACAT thermosalingraph. In addition, 500ml of seawater was collected and filtered onto What-man GF/F glass fiber filters (47 mm, pore size 0.7mm), after 24 h extraction in 90% methanol at –20◦C(Parsons et al., 1984) these samples were used to de-termine the Chl a concentration using a fluorometer

(Turner Designs 7200, Sunnyvale, California, USA).Abundance of Synechococcus, Prochlorococcus,

pico-eukaryotes, and heterotrophic bacteria were de-termined by an onboard flow cytometer (FCM, FAC-SCalibur, Becton-Dickinson Company, USA). A pre-filtered sample (50 µm mesh) was collected into a 100ml brown PEB bottle, and a 3 ml subsample of thewater was used to determine the picophytoplanktonabundance and community structure (Balfoort et al.,1992). A 10 µl dose of SYBR green I (final concentra-tion 1/10 000 v/v) was added to another 1 ml subsam-ple of water to detect the abundance of heterotrophicbacteria after 15 min of staining in the dark (Binder etal., 1996). The results were analyzed and transformedusing Cell Quest.

Carbon biomass of the four picoplankton groupswas estimated by conversion from cell abundance us-ing factors of 250, 53, 2 100, and 20 fg/cell for Syne-chococcus, Prochlorococcus, pico-eukaryotes, and het-erotrophic bacteria, respectively (Lee and Fuhrman,1987; Campbell et al., 1994; Buck et al., 1996). Pear-son correlation analysis of the picoplankton abundanceand heterotrophic bacteria abundance to salinity andtemperature was conducted.

Fig.1. Location of the sampling stations (black dots) during the CHINARE 24 cruise.

Six stations of each province including westernPacific, meeting area of Pacific and Indian, East In-dian, Southeast Indian Ocean, South Indian Ocean,South Atlantic, and Southwest Atlantic (Fig. 1) wereselected to analyze the distribution pattern of pi-coplankton by Principal Component Analysis. Alldata were analyzed using SPSS 16.0.

3 Results and discussion

3.1 Latitude distribution of picoplankton

3.1.1 ProchlorococcusThe results of the current study revealed a signif-

icant pattern of picoplankton distribution along latit-

136 LIN Ling et al. Acta Oceanol. Sin., 2012, Vol. 31, No. 1, P. 134-142

ude, with higher abundance and carbon biomass atlow and mid latitudes. In those oceans, such as thewestern Pacific, East Indian, and Southwest Atlanticoceans, Prochlorococcus and Synechococcus were themost important parts of the picoplankton communityand their actual distribution changed with the oceanicprovinces. The major oceanic provinces of Prochloro-coccus were found between latitudes 30◦N and 30◦S(Fig. 2a) and it was the major picoplankton in theEast Indian Ocean with the cell abundance rangedfrom 0.000 to 2.778×108 ind./L (Fig. 2a), whichwas 0%–90% of total picophytoplankton abundanceand 15% of total picoplankton carbon biomass (Fig.3). Water temperature influenced the distribution ofProchlorococcus, with high positive correlation coef-ficient (cc) of 0.611 (P=0.000 1) (Table 1). John-son et al. (2006) reported that the optimal growthtemperature of Prochlorococcus was 25◦C. And therelative high Prochlorococcus abundance between lat-itudes 30◦N and 30◦S was also caused by the suit-able temperatures ranging between 24.5 and 29.8◦C.Prochlorococcus could grow at high latitude of 45◦Nin the subarctic Pacific Ocean (Boyd and Harrison,1999; Obayashi et al., 2001). Besides, Jiao et al.(2002) suggest that instead of temperature, the com-bination of water masses determined the distributionscope of Prochlorococcus in marginal seas. They re-ported: when the Taiwan Warm Current and KuroshioCurrent reached, Prochlorococcus was present. Doolit-tle et al. (2008) found Prochlorococcus were not ob-served in water cooler than 10.65◦C or south of 42◦S.Our investigation also shows that Prochlorococcus waspresent at 26.8◦N south and disappeared at 26.8◦Nnorth (Fig. 2a). At 26.8◦N south, Taiwan WarmCurrent and Kuroshio Current brought warm andsalty water which also brought the Prochlorococcus.However at 26.8◦N north, Changjiang River (YangtzeRiver) diluted water and the Huanghai Sea (YellowSea) Coastal Current meet the Taiwan Warm Current,which could constitute complicated water situationand did not suit for the survival of Prochlorococcus.The penetration of freshwater from north conductedthe decrease of water salinity and temperature andlimited the growth of Prochlorococcus. Besides, Wa-ter from Changjiang River and Huanghe River (Yel-low River) decreased the diaphaneity which also lim-ited the growth of Prochlorococcus because irradiancewas another factor that determine the distribution ofProchlorococcus (Bouman et al., 2006). Meanwhile,

Fig. 2a also shows that Prochlorococcus disappeared atthe Java Sea where water temperature was higher than25◦C, during the wet season of the Equatorial Region.Freshwater from the land flowed into Java Sea (Gingeleet al., 2002) and limited the growth of Prochlorococcus.All of these suggest that water masses and currentsinstead of water temperature played more importantpart in the latitude distribution of Prochlorococcus, es-pecially at marginal seas.3.1.2 Synechococcus

The major distribution ocean province of Syne-chococcus could reach a latitude range between 33◦Nand 50◦S. Its cell abundance ranged from 0.070 to1.855×108 ind./L (Fig. 2b), contributed 10%–86%of the total picophytoplankton abundance and 35%of total picoplankton carbon biomass (Fig. 3). TheMakassar Strait area and southwest Atlantic area gothigher Synechococcus abundance. The Makassar Straitlocated at the Equatorial Region, warmer water (28.3–29.8◦C) and nutrients from the landing inflows accel-erate the growth of Synechococcus. And southwest At-lantic area was a shelf area, also got relative higher wa-ter temperature (17.13–22.10◦C), nutrients from thelanding inflows and Falkland Cold Current [an off-shoot formed when Antarctica Circumpolar Current(ACC) flows to the east, brings the nutrient rich At-lantic deep water into the Argentina Sea] (Peterson,1992) conducted the higher Synechococcus abundance.Besides the water temperature limitation, Synechococ-cus preferred eutrophic conditions (Jiao et al., 2005).

By using epi-fluorescence microscopy, Ning et al.(1996) found that the cyanobacteria abundance atthe Southern Ocean ranged from 0.600 to 20.400×108

cells/L. And this was different with our results. How-ever at Atlantic section of the Southern Ocean, an in-vestigation including 41 stations with water tempera-ture less than 1◦C also cannot detect the Synechococcuby Flow Cytometry (Doolittle et al., 2008). Doolittlethought there was too few of cells were counted toconstitute a recogsisably distinct cytometric cluster.Meanwhile, Cyanobacteria were also detected in theEast Antarctic marginal ice zone (Wright and van denEnden, 2000) and meltwater ponds of an Antarcticaice shelf (Jungblut et al., 2009) using other methodssuch as autofluorescence spectrum, high performanceliquid chromatogram (HPLC) and Denatured Gradi-ent Gel Electrophoresis (DGGE) analysis. By limitat-ing the protein synthesise (Ning et al., 1996), watertemperature became the primary controlling factors


to the growth of Synechococcu at the Southern Ocean.Our research also found the obvious correlation be-tween Synechococcu abundance and water temperature

(P <0.01) (Table 1). Besides the water temperature(cc=0.436; P=0.002), Chl a concentration became an-other positive factor, with correlation coefficient of

Fig.2. Surface distribution of picoplankton along the cruise. a. Prochlorococcus, b. Synechococcus,c. Pico-eukaryotes, and d. Heterotrophic bacteria.


Fig.3. Picoplankton carbon biomass contribution to total carbon biomass and variation along latitude. a.33◦N–35◦S, b. 35◦–68◦S and c. picoplankton carbon biomass contribution to total carbon biomass andvariation around Antarctic Ocean.

Table 1. Correlations among picoplankton carbon biomass, total picoplankton carbon biomass (Total), Chl a concen-

tration, salinity, and temperature

Factors Bac Euk Pro Syn Total Chl a

Temperature/◦C Pearson correlation 0.323∗∗ 0.129 0.611∗∗ 0.436∗∗ 0.272∗∗ –0.116

Sig. (2-tailed) 0.000 0.131 0.000 0.000 0.001 0.173

Salinity (PSU) Pearson correlation –0.043 –0.021 0.004 0.007 –0.025 –0.008

Sig. (2-tailed) 0.613 0.805 0.964 0.937 0.769 0.924

Chl a/µg·L−1 Pearson correlation 0.408∗∗ 0.641∗∗ –0.155 0.227∗∗ 0.624∗∗ 1

Sig. (2-tailed) 0.000 0.000 0.068 0.007 0.000

Notes: Bac, Euk, Pro and Syn stands for heterotrophic bacteria, picoeukaryotes, Prochlorococcus, and Synechococcus, respec-

tively. ∗∗ Correlation is significant at the 0.01 level (2-tailed). N=139.

0.227 (P=0.007) (Table 1). This is accordant withthat Synechococcus prefers eutrophic conditions whichare propitious to form high Chl a concentrations; com-paratively, Prochlorococcus prefer oligotrophic waterconditions (Jiao et al., 2005). Doolittle also found theSynechococcus did not appear consistently in samples

until the water temperature exceeded 1.26◦C, and wa-ter temperature of the area of our Southern Oceaninvestigation was almost less than 0◦C, prolongingthe detecting time and increasing the sample volumnwhich might improve the results. Besides the detectinginstrument limitation, freshwater inflow could be the


more important factors of Synechococcus distribution.During the investigation, Synechococcus rich areas asshown in Fig. 2b were significantly associated withfreshwater inflow. Zone A was influenced by HuangheRiver runoff, Zone B by freshwater plumes and runoffand Zone C by La Plata Parana River runoff.

3.2 Circum Polar distribution of picoplankton

Heterotrophic bacteria and pico-eukaryotes weredistributed along the whole investigation areas, andconstituted major portions of picoplankton commu-nity in the Antarctic Ocean. Here, the abundance ofheterotrophic bacteria ranged from 0.041 to 0.740×108

ind./L (Fig. 2d). There were also significant correla-tion between heterotrophic bacteria biomass and wa-ter temperature (P <0.01) (Table 1). Pico-eukaryoteabundance in the Antarctic Ocean fluctuated slightly,varying from 0.002 to 0.182×108 ind./L, with an av-erage of 0.032×108 ind./L (Fig. 2c). Meanwhile, thecarbon biomass of pico-eukaryotes ranged from 0.03to 38.2 µg/L. Neither water temperature nor salin-ity had visible correlation with picoeukaryote biomass(P >0.05) (Table 1). In contrast with the low andmid latitude ocean provinces, pico-eukaryotes and het-erotrophic bacteria contributed an average of 57% and41% of the total picoplankton carbon biomass, respec-tively (Fig. 3), and contributed major part of pico-phytoplankon abundance and carbon biomass in theAntarctic Ocean. The high pico-eukaryote abundanceappeared at open sea area of southwest Atlantic andobviously different from offshore area. The offshorearea was highly influenced by Falkland Cold Current,with higher water temperature and richer nutrients,which accelerated the growth of big size phytoplank-ton and thus limit the small size phytoplankton. Onthe contrary, the open sea area was located at the Sub-antarctica Front, with decreased influence of FalklandCold Current and increased influence of the AtlanticSea water (Orsi et al., 1995). The decrease of nutrientcaused the high abundance of pico-eukaryotes.

High abundance of heterotrophic bacteria was dis-tributed at low and mid latitude area, and higherabundance at southwest Atlantic and east Weddell Sea(0◦–15◦W). The highest value appeared at estuary ofLa Plata Parana River, southwest Atlantic. The nutri-ent rich water from landing inflow and Falkland ColdCurrent formed a high Chl a and primary productivityarea. Excepting the nutrients of ammonia and nitrate,the high DOC concentration from the phytoplanktondegradation was also a main reason for the high het-

erotrophic bacteria abundance. When coming to theeast Weddell Sea, it belongs to the exit of ACC flowthrough the Weddell Sea, the melting water from theinner fjord Larsen and Ronne Ice Shelf brought the nu-trient rich water into the east exit (Krell et al., 2005),bloomed a high phytoplankton abundance and concen-tration, thus conducting the high DOC concentration.This might be a main reason for the high HB abun-dance of this area. Besides, Krell et al. (2005) founda high Chl a concentration at there and thought itwas caused by the cyclonic eddy type current, whichmay be another reason for it. Our research also in-dicated a sub high HB abundance appearing at 70◦Eof Antarctica Ocean, front of Amery Ice Shelf, andmelting water inflow may be the main reason.

3.3 Picoplankton composition and distribution

differences at same latitude of Atlantic

Ocean and Indian Ocean

The picoplankton distribution characteristicswere typical in different ocean provinces as revealedby Principal Component Analysis (Fig. 4), in whichprincipal component 1 (PC1) and 2 (PC2) cumu-lated explained 78.1% of total picoplankton distri-bution characteristics and can be used as the proxyto the total community. Heterotrophic bacteria andpico-eukaryotes contributed the major picoplanktoncommunity of Southeast Antarctic Oceans, whereasProchlorococcus and Synechococcus contributed themajor picoplankton community of the meeting area ofthe Pacific and Indian Oceans, East Indian Ocean andWest Pacific Ocean. At the same latitude of AtlanticOcean (SWA) and Indian Ocean (SA) (between 36◦–44◦S), picoplankton was distributed entirely different(Fig. 4). SWA distributed high abundance of pico-eukaryotes and heterotrophic bacteria, however whenat SA, picoplankton abundance were at low level. Thelocation of SWA and SA determined the difference ofpicoplankton distribution and constitution. Firstly,SWA was coastal area and SA was basin area, be-cause of the landing freshwater inflow and existence ofcontinental shelf. It was believed that nutrient con-centration at SWA would be much higher than at SA.Besides, different water masses combination broughtdifferent picoplankton. SWA and SA all influenced bySubantarctic Front and Subtropical Front (Doolittle etal., 2008; Sultan et al., 2007), however at SWA, Falk-land Cold Current (Peterson, 1992) conducted thedecrease of water temperature and salinity, which


Fig.4. Scatter plot of 42 picked-up stations by using the factor scores: WP represents West Pacific, PI

meeting area of Pacific and Indian, EI East Indian Ocean, SEI Southeast Indian Ocean, SI South Indian

Ocean, SA South Atlantic, SWA Southwest Atlantic, Bac bacteria, Euk picoeukaryotics, Pro Prochlorococcus,

and Syn Synechococcus.

could also conduct the difference of picoplankton dis-tribution and abundance.

In surface waters of the world’s oceans, at anyparticular temperature, the abundance of phytoplank-ton is variable and spans a range of one to two or-ders of magnitude (Li, 2008). And the logarithmof phytoplankton abundance was significantly corre-lated with water temperature. Our research also con-cluded an equation between picophytoplankton abun-dance (N) and temperature (T ) of all stations: lgN =3.543+0.048 4T (R2=0.669 3), which also proved thecorrelation between them. However, water tempera-ture was not the only factor controlling the picophy-toplankton community structure. In other words, thecommunity is structured in such a way that the sumof its components gives rise to a striking pattern thatis closely alighed with temperature, but which is notreflected in the individual functional groups. Instead,community structure appears to be determined by aninterplay between water mass coherence (Doolittle etal., 2008). The picoplankton distribution characteris-tic of southwest Atlantic, specific distribution of Syne-chococcus at Makassar Strait, higher HB abundance

at east Weddell Sea and front of Amery Ice Shelf per-fectly proved the conclusion. In other words, researchwork toward picoplankton community structure at theSouthern Ocean could help us to understand the watermass constitution of the Southern Ocean at the otherhand.

Picoplankton conducted different ecotypes toadapt different enviroment. Using direct PCR am-plification of RNA polymerase genes, genetic and eco-logical diversity of picoplankton was easily detected.Bouman et al. (2006) found the main ecotypes ofProchlorococcus were totally different at the South Pa-cific and Indian Ocean. At South Pacific, Low light(LL) adapted ecotypes dominated the Prochlorococ-cus, however at Indian Ocean, it was SS120 type (an-other LL type). Ma et al. (2004) found that the mainProchlorococcus of South China Sea could be high light(HL) adapted II genotype. Thus, the geographical fac-tors may be important in determining the distributionof Prochlorococcus genotypes (Ma et al., 2004). Dur-ing the cruise at tropic and sub-tropic oceans, abun-dance Prochlorococcus varied rarely, progress diver-sity analysis should help us to know the detail nat-


ural environment farther. Meanwhile, Vincent (2000)thought Synechococcus came from freshwater, and westill did not find any typical oceanic type of Syne-chococcus (Waleron, 2007). Our research also agreedwith the conclusion. The main Synechococcus distri-bution zones were significantly associated with landingfreshwater inflow (Fig. 2b).

4 Conclusions

In this paper, using flow cytometer onboard, wereported the picoplankton abundance and structurecomposition across latitudes and along the circumAntarctic Ocean. We found that Synechococcus (Syn)and Prochlorococcus (Pro) were mainly distributed atlow and middle latitude ocean provinces, and pico-eukaryotes (Euk) and heterotrophic bacteria (HB)were distributed at oceans all over the world. Tem-perature was proved to be an important factor to Proabundance but could not be the only one, accordingto the Pro distribution pattern during the cruise, wa-ter mass combination could be more important one.Meanwhile, the main Syn distribution areas were sig-nificantly associated with freshwater inflows, thereforewe guess that Syn may be freshwater types. The high-est Euk abundance appeared at offshore area of thesouthwest Atlantic Ocean, besides the water temper-ature, river runoff and water current may also deeplyinfluenced the Euk abundance. HB abundance mayalso deeply influenced by river runoff and melt wa-ter inflows (Fig. 2d). Thus we suggest that at theocean surface, removing the influence of water tem-perature, external water sources such as river runoff,landing freshwater inflow, melting water inflows andso on brought the difference of picoplankton distribu-tion and composition, besides, water mass combina-tion could also be important to picoplankton abun-dance and composition.Acknowledgements

The authors would like to thank the captain andcrew of the R/V Xuelong and many other colleaguesof CHINARE 24 for their assistance in collecting thesamples.

References

Azam F, Fenchel T, Field J G. 1983. The ecological role

of water column microbes in the sea. Mar Ecol Prog

Ser, 10: 257–263

Balfoort H W, Berman Th, Maestrini S Y, et al. 1992.

Flow cytometry: instrumentation and application in

phytoplankton research. Hydrobiologia, 238: 89–97

Binder B J, Chisholm S W, Olson R J, et al. 1996. Dy-

namics of pico-phytoplankton, ultra-phytoplankton,

and bacteria in the Central Equatorial Pacific. Deep-

Sea Res II, 43: 907–931

Bouman H A, Ulloa O, Scanlan D J, et al. 2006. Oceano-

graphic basis of the global surface distribution of

Prochlorococcus ecotypes. Science, 312: 918–921

Boyd P W, Harrison P J. 1999. Phytoplankton dynamics

in the NE subarctic Pacific. Deep-Sea Res II, 46(11-

12): 2405–2432

Brown S L, Landry M R. 2001. Microbial community

structure and biomass in surface waters during a

Polar Front summer bloom along 170◦W. Deep-Sea

Res II, 48(19–20): 4039–4058

Brown S L, Landry M R, Barber R T, et al. 1999. Pi-

cophytoplankton dynamics and production in the

Arabian Sea during the 1995 Southwest Monsoon.

Deep-Sea Res II, 46: 1745–1768

Buck K R, Chavez F P, Campbell L. 1996. Basin-wide

distribution of living carbon compponents and the

inverted trophic pyramid of the centrall gyre of the

North Atlantic Ocean, Summer 1993. Aquatic Mi-

crobial Ecology, 10: 283–298

Camila F, Melilotus T, Michel D. 2008. Microbial com-

munity structure along 18◦W (39◦N–44.5◦N) in the

NE Atlantic in late summer 2001 (POMME pro-

gramme). Journal of Marine Systems, 71: 46–62

Campbell L, Nolla H A, Vaulot D. 1994. The impor-

tance of Prochlorococcus to community structrue

in the central North Pacific Ocean. Limnology and

Oceanography, 39(4): 954–961

Chisholm S W, Olson R J, Zettler E R, et al. 1988. A

novel free-living prochlorophyte abundanct in the

oceanic euphotic zone. Nature, 334: 340–343

Doolittle D F, Li W K W, et al. 2008. Wintertime

abundance of picoplankton in the Atlantic sector of

the Southern Ocean. Nova Hedwigia, Beiheft, 133:

147–160

Ehnert W, McRoy C P. 2007. Phytoplankton biomass

and size fractions in surface waters of the Australian

sector of the Southern Ocean. Journal of Oceanog-

raphy, 63: 179–187

Gingele F X, Deckker P D, Girault A, et al. 2002. His-

tory of the South Java Current over the past 80 Ka.

Palaeogeography, Palaeoclimatology, Palaeoecology,

183: 247–260

Jiao Nianzhi, Yang Yanhui, Hong Ning, et al. 2005.

Dynamics of autotrophic picoplankton and het-

erotrophic bacteria in the East China Sea. Con-

tinental Shelf Research, 25(10): 1265–1279

Jiao Nianzhi, Yang Yanhui, Koshikawa H, et al. 2002. In-

fluence of hydrographic conditions on picoplankton

distribution in the East China Sea. Aquatic micro-

bial ecology, 30: 37–48


Johnson Z I, Zinser E R, Coe A, et al. 2006. Niche

partitioning among Prochlorococcus ecotypes along

ocean-scale environmental gradients. Science, 311:

1737–1740

Jungblut A D, Allen M A, Burns B P, et al. 2009. Lipid

biomarker analysis of cyanobacteria-dominated mi-

crobial mats in meltwater ponds on the McMurdo

Ice Shelf, Antarctica. Organic Geochemistry, 40(2):

258–269

Kazuhiko M, Ken F, Takeshi K. 2004. Association of

picophytoplanktonn distribution with ENSO events

in the equatorial Pacific between 145◦E and 160◦W.

Deep-Sea Res I, 51: 1851–1871

Krell A, Schnack-Schiel S B, Thomas D V, et al. 2005.

Phytoplankton dynamics in relation to hydrogra-

phy, nutrients and zooplankton at the onset of sea

ice formation in the eastern Weddell Sea (Antarc-

tica). Polar Biology, 28: 700–713

Landry M R, Kirshtein J, Constantinou J. 1996. Abun-

dances and distributions of picoplankton popula-

tions in the central equatorial Pacific from 12◦N to

12◦S, 140◦W. Deep-Sea Res II, 43(4-6): 871–890

Lee S H, Fuhrman J A. 1987. Relationships between Bio-

volume and Biomass of Naturally Derived Marine

Bacterioplankton. Appl Environ Microbiol, 53(6):

1298–1303

Li W K W. 2008. Plankton Population and Comunities.

Chicago: University of Chicago Press

Li W K W, Subba Rao D V, Harrison W G, et al. 1983.

Autotrophic picoplankton in the trophical ocean.

Science, 219: 292–295

Ma Ya, Jiao Nianzhi, Zeng Yonghui. 2004. Natural

community structure of cyanobacreria in the South

China Sea as revealed by rpoC1 gene sequence anal-

ysis. Letters in Applied Microbiology, 39: 353–358

Ning Xiuren, Liu Zilin, Shi Junxian, et al. 1993. Standing

crop and productivity of phytoplankton and POC

in Prydz bay and the adjacent waters. Antarctic

Research (in Chinese), 5(4): 50–62

Ning Xiuren, Shi Junxian, Liu Zilin, et al. 1996. The

abundance and distribution of Cyanobacterium and

picophytoeukaryotes at the Southern Ocean. Sci-

ence in China (Series C), 26(2): 164–171

Obayashi Y, Tanoue E, Suzuki K, et al. 2001. Spatial

and temporal variabilities of phytoplankton com-

munity structure in the northern North Pacific as

determined by photyplankton pigments. Deep-Sea

Res I, 48(2): 439–469

Orsi A H, Whitworth T, Nowlin W D. 1995. On the

meridional extent and fronts of the Antarctic Cir-

cumpolar Current. Deep-Sea Res I, 42: 641–673

Parsons T R, Maita Y, Lalli C M. 1984. A manual of

chemical and biological methods for seawater analy-

sis. Toronto: Pergamon Press

Peterson R G. 1992. The boundary currents in the west-

ern Argentine Basin. Deep-Sea Res I, 39: 623–644

Sultan E, Mercier H, Pollard R T. 2007. An inverse

model of the large scale circulation in the South

Indian Ocean. Progress in Oceanography, 74: 71–94

Vincent W F, Gibson J A E, Pienitz R, et al. 2000. Ice

shelf microbial ecosystems in the high Arctic and

implications for life on snowball earth. Naturwis-

senschaften, 87(3): 137–141

Waleron M, Waleron K, Vincent W, et al. 2007. Al-

lochthonous inputs of riverine picocyanobacteria to

coastal waters in the Arctic Ocean. FEMS Microbiol

Ecol, 59: 356–369

Wright S W, van den Enden R L. 2000. Phytoplankton

community structure and stocks in the East Antarc-

tic marginal ice zone (BROKE survey, January-

March 1996) determined by CHEMTAX analysis

of HPLC pigment signatures. Deep Sea Research

Part II: Topical Studies in Oceanography, 47(12-

13): 2363–2400

Yves D, Awa N. 2007. Assemblages of phytoplankton

pigments along a shipping line through the North

Atlantic and tropical Pacific. Progress in Oceanog-

raphy, 73: 127–144

flow cytometry investigation of picoplankton across latitudes and along the circum antarctic ocean

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