PHOTOSYNTHETIC PICOPLANKTON COMMUNITY STRUCTURE

IN THE PEAR RIVER ESTUARY AND ADJACENT SHELF WATERS∗

AIJIA ZHU
South China Sea Environmental Monitoring Center (SCSEMC), State Oceanic Administration
(SOA), No.155 West Xingang Road, Guangzhou, 510300, China
South China Sea Institute of Oceanology, Chinese Academy of Science, No.164 West Xingang
Road Guangzhou, 510300, China

HAITAO LI, YANG GAO, DUAN LIN, HONGDA FANG, YANHONG DONG
South China Sea Environmental Monitoring Center (SCSEMC), SOA, No.155 West Xingang Road,
Guangzhou, 510300, China

Dynamics of Prochlorococcus (Pro), Synechococcus (Syn) and picoeukaryotes (Euk) was studied in
the Pearl River Estuary and adjacent shelf waters in the summer. The average cell abundance of
photosynthetic picoplankon (Pico) was 104 cells/mL. Synechococcus was the dominant group in the
inner estuary and coastal waters. Prochlorococcus was dominant in shelf waters. The proportion of
Euk was less variable in the studied area. The abundances of Syn and Euk were positively correlated
with nitrogen and silicon concentrations, whereas they were negatively correlated with temperature.
However, %Pro had significant negative correlations with nitrogen, phosphorus and silicon, and
positive correlations with temperature. There were differences in the niches between Pro and the
other 2 groups of Pico in the wet season (summer), which was quite different from the observation
in the dry season (winter).

1 Introduction

Photosynthetic picoplankton (Pico) defined as the cells with a diameter less than 2 μm
[1] has been found to widespread in a variety of marine ecosystems [2－6]. Flow
cytometry clearly demonstrated that 3 groups of Pico can be categorized as
Prochlorococcus (Pro), Synechococcus (Syn), and picoeukaryotes (Euk) [7].
Prochlorococcus is the smallest oxygenic photoautotroph with abundance of 105 cells/mL
in the oceanic waters [2,8－11]. Synechococcus, slightly larger than the Pro, is reported
to be more important in mesotrophic or coastal regions [4,12－18]. Picoeukaryotes is the
most competitive among Pico in near-shore waters [6,9,11,16－18].
The Pearl River Estuary (PRE) is located midway along the northern boundary of
the South China Sea [19]. It is a subtropical estuary and the second largest in China
based on discharge volume [19]. The PRE is a complex estuary with seasonal dynamic
variations in freshwater discharge, monsoon winds and coastal circulation and the
processes in the estuary vary spatially and temporally (wet season vs dry season, [19,20].
During the summer wet season with southwest monsoon winds, the high river discharge

∗
This work is supported by the National Project of Coastal Environment Investigation and
Assessment (908-01-ST07, 908-ZC-I-02, 908-02-02-02).

1
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dilutes the nutrient and organic loads [19]. Phytoplankton in the PRE is potential
P-limited in the estuary, P and Si co-limited at the edge of the coastal plume, and
N-limited in the oceanic side in summer [21]. During the dry season with northeast
monsoon winds, the eutrophication impacts on the upper estuary are serious due to the
low river discharge during the dry season [19].
In spite of the recognized importance of Pico in oceanic ecosystems [2－6,9,17]
there are few studies from the PRE. Previous study has analyzed the dynamics of Pico in
the PRE and adjacent shelf waters in the dry season, and related those to the
hydrochemical change from the inner estuary to the open waters [22]. Here, the
relationship between the community structure of Pico and the environment factors are
explore to determine which factors controlling the spatial distribution of Pico in the PRE
in the wet season and weather the dynamics of Pico vary temporally (wet season vs dry
season) as the physical processes in the estuary do.

2 Material and Methods

The cruise including 92 Pico sampling stations was conducted in the PRE and adjacent
shelf waters from July to August, 2006 (Figure 1).Water samples were collected using
van Dorn samplers triggered at depths of 0.5m, 10m, 30m, and bottom layer (2m off the
bottom). Triplicate sea waters samples for Pico analysis were pre-treated and analyzed
using the flow cytometer (FACSCalibur, Becton-Dickinson) following the procedures
described by Marie et al. [7]. Prochlorococcus, Syn and Euk were discriminated by flow
cytometric signals of scatter and fluorescence [7,11,23]. The measurements of
temperature, salinity and dissolved oxygen (DO) were made using a SBE 911plus CTD
(Sea-Bird). The pH was analyzed immediately on board with a PHS-3C pH instrument
(LeiCi, Shanghai). Nutrients —— including total nitrogen (TN), total dissolved nitrogen
(TDN), nitrate (NO3－), nitrite (NO2－), ammonium (NH4＋), total phosphorous (TP), total

Figure 1. Distribution of the investigation stations in the Pearl River Estuary.

 3

dissolved phosphorus (TDP), phosphate (PO43－) and silicic acid (SiO32－) were analyzed
with QuikChem 8500 automatic flow injection analyzer (Lachat, USA) in the laboratory.
Suspended sediment concentration (SSC) was analyzed by a gravimetric method using
BS110S analytical balance (Sartorius, Germany) in the laboratory. The data were
analyzed using the SPSS 11.0 software (SPSS Inc.). Pearson correlations between cell
abundances of 3 groups of Pico and environmental factors were calculated.

3 Results

3.1. Hydrological Conditions

Surface water temperature were 24.2－31.2 ℃ in the study area, with lower values
found in the inner estuary (the Lingdingyang Bay, Fig. 1) and higher values recorded in
the southeast part of the shelf waters (>50 m). Surface salinity increased from 0.83 at the
head of the estuary to 34.2 in the shelf waters. SSC decreased significantly from the inner
estuary (>30 mg/L) to the coastal waters (<50 m, 2 mg/L), and it was low in the shelf
waters. The average concentrations of surface dissolved inorganic nitrogen (DIN, NO3－
＋NO2－＋NH4＋), PO43－ and SiO32－ were respectively 30.6, 0.54 and 30.7 μmol/L. All
nutrient concentrations decreased offshore. In the shelf waters, there was a strong spatial
gradient in DIN concentrations from the northeast area (5－10 μmol/L) to the southwest
(<3 μmol/L), which might due to the intrusion of the oceanic waters in the southwest area
during the wet season with southwest monsoon winds [19]. Consequently, low N/P ratio
(<50) in the surface occurred in the southwest outer shelf. The N/P ratios in the PRE and
the adjacent shelf waters in summer were rather high that the average value was 118.5.
SiO32－ had a strong spatial gradient in the coastal waters, from >100 μmol/L decreased
to 5 μmol/L, and was less variable in the shelf waters.
Water temperature increase offshore in the upper waters (0－30 m) but decreased
outwards in the bottom waters in the outer shelf waters (>100 m). Salinity increased with
depth and a strong vertical gradient (27－33) was found in the coastal waters. The
vertical variation of DIN and PO43－ concentrations in the upper layer (0－30 m) were
not significant. But in the shelf waters, they increased in the bottom layer. At the same
time, N/P ration in the shelf waters decreased from 107 in the surface layer to 22 in the
bottom layer. SiO32－ showed similar vertical distribution and the increase could be seen
in the 30m-layer.

3.2. Photosynthetic Picoplankton Abundance

The abundance of Pico in the surface waters decreased from the inner estuary [average
(2.76±0.92)×105 cells/mL] to the open waters [average (4.29±2.80)×104 cells/mL].The
abundance of Pico tended to decrease with depth in the inner estuary and coastal waters.
While in the shelf waters, the maximum values occurred at the 30 m layer and the
abundance of Pico decreased in the bottom waters.
4

The distribution of Pro, Syn and Euk showed spatial heterogeneity. The abundances
of Pro at the surface increased offshore, while the abundance of Syn and Euk were
higher in the inner estuary and coastal waters than those in the shelf waters. In the inner
estuary, %Syn (as of total Pico) was the highest among the 3 groups of Pico. The average
%Syn at the surface reached to (95.4±4.6) % in the inner estuary, while Pro disappeared
at some stations. Synechococcus was also the dominant group in the coastal waters, and
the average %Syn was higher than 85% at the surface. The average %Pro was the
highest in the shelf waters [(61.2±22.0) %], and was about (12.9±16.7)% in the coastal
waters. The abundances of Euk in the inner estuary and coastal waters were comparable
[average (2.81±1.79)×103 cells/mL and (2.91±0.67)×103 cells/mL respectively], and
were one order of magnitude higher than that in the shelf waters.
Pearson correlations between the environmental factors and cell abundance of Pico,
Pro, Syn and Euk, %Pro, %Syn, %Euk, and the Pro: Syn ratio were calculated (Table 1).
The correlations between Pro abundance, %Euk and environmental factors were not as
significant as %Pro and Euk (Table 1). The relationships between cell abundances of Syn
and Euk, %Syn and environmental factors were opposite to those between %Pro, the Pro:
Syn ratio and environmental factors (Table 1). In the studied area, no significant
relationship was found between temperature, SSC and cell abundance of Pico, Pro, Syn
and Euk, %Pro, %Syn, %Euk, and the Pro: Syn ratio in summer (Table 1).

Table 1. Pearson correlations1 between the surface environmental factors and surface cell abundance of Pico,
Pro, Syn, Euk, %Pro, %Syn, %Euk2, and the surface Pro: Syn ratio.
Environmental
Pico Pro Syn Euk %Pro %Syn %Euk Pro:Syn
factors
Temperature － － － － － － － －
Salinity 0.443 － -0.447 -0.385 0.492 -0.492 － 0.376
SSC － － － － － － － －
－
NO3 0.353 － 0.371 0.327 -0.414 0.414 － -0.311
－
NO2 0.262* － 0.294 -0.341 0.344 － -0.233
＋
NH4 0.267 － 0.305 0.257* -0.316 0.316 － －
DIN 0.355 － 0.375 0.324 -0.419 0.418 － －
－
PO43 － － － － -0.315 0.319 － －
2－
SiO3 0.412 － 0.424 0.353 -0.409 0.409 － －
N: P 0.313 － － 0.297 － － － －
1
P<0.01, N＝92.
2
cell abundance－103 cells/mL, %Pro, %Syn, %Euk－%, temperature－℃, SSC－mg /L, nutrients－μmol /L.
* indicated P<0.05.
－indicated the correlation was not significant (P>0.05).

4 Discussion

4.1. Environmental factors controlling Pico community structure

The cell abundances of Pro and Syn in the adjacent shelf waters of the PRE were very
close to those in the adjacent shelf waters of the Changjiang Estuary (a temperate estuary
 5

in the East China Sea) [6]. Temperature, which was one of the major factors influencing
the Pico abundance in the two estuaries in winter [6,22], no longer seems to be the
limited factor in the PRE in summer. Pico seems to be potential nitrogen limited in the
PRE in summer although the average concentration of DIN was higher in summer than
that in winter [(15.8±20.6) μmol/L, 22]. On the other hand, the average TDP in the study
area in summer [(1.0±1.1) μmol/L] was also much higher than that in winter [(0.5±0.3)
μmol/L]. The potential nitrogen limited may cause by the rich TDP in summer since
numerous organic phosphorus can be utilize as phosphorus sources by Syn [24,25], which
need further test.
Prochlorococcus was absent at some stations in the inner estuary and become the
dominant group in the shelf waters, which is similar to the previous findings
[3,6,14,15,17,18,26,27]. Temperature is reported to be crucial to Pro [2,6,14,22,28]. But
in the present study, no significant relationship was found between Pro and temperature
at the surface due to the high sea surface temperature in summer. Pro replaced Syn,
which dominated in the shelf waters in winter [22], to be the dominant group in the shelf
waters. Prochlorococcus maybe absent in the low-salinity waters [4,6,17,18,30,], which
was also occur in this study. Nutrients have been suggested to be playing a role in the
distribution of Pro [9,14,18,31]. In this study, the negative relationship between %Pro
and nutrient concentrations (Table 1) suggested that no nutrient limitation to Pro
occurred in summer as same as in winter [22].
Compared with Pro, Syn is reported to be more nutrient-dependent [2,4,6,9,31－34].
Similar result was found in the study that Syn dominated in the inner estuary and coastal
waters and its abundance were positively correlated with nutrients (Table 1). The
temperature could be a limiting factor on Syn growth during the cold season in the PRE
and Changjiang River Estuary [4,6,22,34]. However, the relationship between surface
Syn and sea surface temperature in the PRE in summer was no as significant as that in
winter [22].
Picoeukaryotes was reported to be the most competitive among Pico in near-shore
waters with abundant river-borne nutrients [17,18]. In the present study, Euk abundance
and %Euk was less variable among the inner estuary, coastal waters and shelf waters.
Picoeukaryotes was more adaptable in low temperature in the PRE and Changjiang
River Estuary in winter [6,22,35]. But in summer, the %Euk was low and Euk cannot
become the dominant group in the PRE. Cell numbers of Euk had significant positive
correlation with nitrogen and SiO32－ concentration, which indicated that Euk might
potentially limited by nitrogen and SiO32－ in the PRE in summer.

4.2. Comparison of dynamics of Pico in different season

The community structure of Pico in the PRE and its adjacent waters in simmer was quite
different from that in winter [22]. In summer, Euk was no longer the dominant group in
the inner estuary and Pro, instead of Syn, became the dominant group in the shelf waters.
This suggests that the seasonal change in water temperature play a key role in the
6

variation of Pico community structure. However, the role of temperature was less
important in controlling the spatial heterogeneity of Pico in simmer than in winter.
Salinity was still one of the controlling factors in spatial heterogeneity of Pico in summer,
but the limitation of salinity to Syn and Euk was less serious in summer than in winter,
which may partly resulted from the low temperature in winter. However, the nutrients
became the limited factors to the abundance of Syn and Euk in summer with higher
nutrient concentrations than in winter, which might associate with the seasonal change of
the nutrient structure.
In winter, the observations strongly suggested that the niches of Pro and Syn are
very similar but the niches of Euk is quite different from that of the prokaryotic cells
(Pro and Syn) [22]. However, in summer, the correlations between the cell numbers of
Syn and the environmental factors became consistent with those between the cell
numbers of Euk and the environmental factors. But the correlations between %Pro and
the environmental factors were opposite to those between the abundance of Syn and Euk
and the environmental factors. Such results revealed that the niches of the 3 groups of
Pico varied significantly with the season. The relationship between these 3 groups
appeared to be closely associated with the seasonal change of environmental
characteristics in the PRE and its adjacent waters, which deserves further study.

Acknowledgments
This study was supported by the National Project of Coastal Environment Investigation
and Assessment (908-01-ST07, 908-ZC-I-02, 908-02-02-02). We thank the Chemical
Analysis Lab of SCSEMC, SOA and the South China Sea Marine Engineering Surveying
Center, SOA for the chemical and hydrological data.

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