effects of coastal upwelling on picophytoplankton distribution off the coast of zhanjiang in south...

Oceanological and Hydrobiological Studies I n t e r n a t i o n a l J o u r n a l o f O c e a n o g r a p h y a n d H y d r o b i o l o g y

Volume 43, Issue 3

ISSN 1730-413X (283–291)

eISSN 1897-3191 2014

DOI: 10.2478/s13545-014-0143-x

Original research paper Received: Accepted:

May 15, 2014 June 30, 2014

Copyright© of Faculty of Oceanography and Geography, University of Gdańsk, Poland www.oandhs.ocean.ug.edu.pl

Effects of coastal upwelling on picophytoplankton distribution off the coast of Zhanjiang in South China Sea Mei-Lin Wu1,3, You-Shao Wang1, Dong-Xiao Wang1,3, Jun-De Dong1,2,*

1State Key Laboratory of Tropical Oceanography, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China 2Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China 3Xisha Deep Sea Marine Environment Observation Station, Chinese Academy of Sciences, Sansha 573199, China Key words: Northern South China Sea, coastal upwelling, picophytoplankton, canonical correspondence analysis, Synechococcus, Prochlorococcus

Abstract

Coastal upwelling occurred along the west coast of Guangdong in the northern South China Sea during the summer of 2006. The effects of upwelling on the vertical and horizontal distributions of Prochlorococcus and Synechococcus were investigated. A distinct vertical temperature difference between the surface water and water at a depth of 30 m was observed in the coastal upwelling region. There was a clear spatial variability of temperature, and an increasingly obvious horizontal gradient was created from the coast to offshore waters. Picophytoplankton communities observed from the coast to offshore waters were significantly different. In the coastal upwelling waters, the picophytoplankton community was dominated by Synechococcus within the euphotic zone. Prochlorococcus dominated the

* Corresponding author: [email protected]

picophytoplankton community in the euphotic zone in the non-upwelling region. This difference in the picophytoplankton community structure was due to different hydrodynamics. The results of canonical correspondence analysis demonstrate that temperature, salinity, and phosphate concentration may be important factors affecting the distribution of Prochlorococcus and Synechococcus. INTRODUCTION

Picophytoplankton (photoautotrophic cells <2 μm in diameter) comprise heterotrophic bacteria and photosynthetic picoplankton, which include three major groups: Prochlorococcus, Synechococcus, and picoeukaryotes. These organisms are ubiquitous in the planktonic marine food web, and their activity has a large impact on ecosystem metabolism and function (Silovic et al. 2011). Picophytoplankton primarily contribute to the total biomass and production in the tropical and sub-tropical oligotrophic oceans (Agawin et al. 2000, Grob et al. 2007). Synechococcus is typically ubiquitous in marine environments and abundant in mesotrophic conditions. Its distribution is generally restricted to the upper well-mixed layer (Partensky et al. 1999a). By contrast, Prochlorococcus is generally absent in well-mixed waters, but the vertical distribution of Prochlorococcus often goes beyond the boundaries of the euphotic layer under oligotrophic conditions (Partensky et al. 1999b, Campbell et al. 1994, Goericke and Welschmeyer 1993). The distribution of Prochlorococcus is controlled by various factors, including physical forces (temperature, salinity, and light) caused by upwelling, a mesoscale eddy, and fronts, which are frequent in the open ocean, as well as chemical factors, such as nutrient concentrations. Despite the lack of information on the mechanisms underlying the dynamics of picophytoplankton communities in the continental shelf waters (Mackey et al. 2009, Calvo-Diaz and Moran 2006, Calvo-Diaz et al. 2008), the variability of hydrodynamics may

284 | Mei-Lin Wu, You-Shao Wang, Dong-Xiao Wang, Jun-De Dong


identify the variability and relative importance of the environmental factors affecting the picophytoplankton distribution in these ecosystems (Jiao et al. 2002).

The northern South China Sea (SCS) is a region where coastal summer upwelling occurs to a large extent along the northern shelf region (Wang et al. 2012, Jing et al. 2009). SCS can be considered a natural laboratory to analyze the interactions between upwelling and picophytoplankton populations. The upwelling of deep nutrient-rich waters in the euphotic zone can trigger not only an increase in primary production, but also a shift in the microbial community structure. Coastal upwelling ecosystems are usually dominated by large phytoplankton groups (Wilkerson et al. 2000), such as diatoms (Hutchings et al. 1995), but they may vary. Limited information is available on the effects of coastal upwelling on the dynamics of picoplankton, such as Prochlorococcus and Synechococcus, in the northern SCS.

In this study, we aimed to identify the relationships between picophytoplankton communities and environmental factors. We investigated the dynamics of Prochlorococcus and Synechococcus in the coastal upwelling off Zhanjiang in mid-July when the Southeast Asian monsoons entering in a southwesterly direction from May to September predominate in the SCS and non-upwelling waters off eastern Hainan. Our results will improve the current knowledge on how a picophytoplankton community structure responds to upwelling-driven processes in the northern South China shelf waters. MATERIALS AND METHODS Study area

The SCS is the largest marginal sea in the western tropical Pacific Ocean, with a total area of 3.5 million km2 and average depth of over 2000 m. The main feature of SCS is a broad continental shelf with a depth shallower than 200 m and isobath that is parallel to the continental coastline. The northern SCS is surrounded by China, Vietnam, Taiwan Island, Luzon Island, and Hainan Island. Hainan Island is the largest island, and most of the other islands are much smaller. Monsoons prevail in the SCS, with a strong northeast wind during winter and a weak southwest wind during summer.

Regarding the current pattern off the eastern Hainan Island and the Zhanjiang Bay (ZB),

oceanographers have documented the existence of two main current systems, i.e. the Guangdong coastal current (GCC) and the SCS Warm Current (SCSWC); GCC flows southward along the west coast of Guangdong (Yuexi coast), whereas SCSWC, which originates from the offshore area east of Hainan Island, crosses the shelf-slope region of the northern SCS and finally enters the southwestern part of the East China Sea via the Taiwan Strait (Guan and Fang 2006, Wang et al. 2010). Therefore, the coastal upwelling along the eastern Leizhou Peninsula (ELP) and Zhanjiang is formed in the summer. However, whether and how these processes can affect the picoplankton dynamics in this region remains unclear. Sampling and analysis

The open cruise was conducted from 19 July 2006 to 6 August 2006 aboard R/V Shiyan 3. Three transects (D13, D14, and D15) off Zhanjiang and Hainan were established from 19 July 2006 to 23 July 2006 (Fig. 1). Temperature and salinity profiles were obtained using a Sea-Bird 911 plus CTD. Water samples for nutrients, pH, and picophytoplankton were obtained from two sets of four water depths,

Fig.1. Map of the investigated areas in the northern SCS and locations of sampling sites analyzed in this study, which was conducted from 19 July 2006 to 23 July 2006. GCC and SCSWC (dotted arrow) represent the Guangdong Coastal Current and the South China Sea Warm Current, respectively. The red square represents the coastal upwelling region off the ELP and Zhanjiang. The green square represents the non-upwelling region off eastern Hainan.

Coastal upwelling having effects on picophytoplankton distribution| 285

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i.e. 0, 5, 10, and <30 m (bottom layer), and 0, 10, 30, and >30 m (bottom layer). Samples of inorganic nutrients, i.e. nitrate (NO3-N (μmol l–1)), nitrite (NO2-N (μmol l–1)), and dissolved phosphorus (DIP (μmol l–1)) were filtered through 0.45 μm cellulose acetate filters and analyzed using a visible spectrophotometer according to the standard colorimetric techniques (Kirkwood et al. 1996). The samples were pre-filtered through a 200 mm mesh to remove large abiotic particles or zooplankton, which was followed by further filtering onto Whatman GF/F filters for Chl a determination. Residents in the filters were then extracted with acetone (90% v/v) in the dark for 24h at 4°C (Parsons et al. 1984) for fluorescence measurements using a Turner Design 10 fluorometer. Flow cytometric analysis of picophytoplankton composition

Samples were pre-filtered through 20 μm mesh netting, fixed with formaldehyde (2% final concentration) in 2 ml cryotubes, and quickly frozen in liquid nitrogen until analysis in the laboratory with a FACSCalibur flow cytometer (Becton–Dickinson) equipped with a laser emitting at 488 nm. To estimate the abundance of different groups,

calibration of the cytometer flow rate was performed daily, and a solution of 1 μm yellow-green (YG) latex beads (Polysciences Co., USA) was added to 0.5 ml sub-samples as an internal standard. Quantities were calculated by the ratio metric method from the determined amount of added beads, and calibrated daily against YG beads (Polysciences). Satellite data

The sea level anomaly (SLA) data, gathered from TOPEX/Poseidon and JASON altimeters (http://www.aviso.oceanobs.com), were used to highlight the oceanic features, such as upwelling. Statistical analysis

Data were analyzed by multivariate methods. A logarithmic transformation [log (x+1)] was used to obtain the normal distribution of the picophytoplankton abundance. Canonical correspondence analysis (CCA) was used to display the relationships between the environment and picophytoplankton.

All mathematical and statistical computations were performed using MATLAB 2010 (Mathworks Inc., USA).

a

b

c

d

e

Fig. 2. Daily Sea Level anomaly from AVISO (a) Before the sampling time: 14/7/2006; (b) and (c) the sampling time: 19 and 23/7/2006; (d) After the sampling time: 27/7/2006; (e) the sampling month: July, 2006



RESULTS Coastal upwelling episode in the west coast of Guangdong

The sea surface height anomaly (SSHA) showed favorable upwelling conditions in the western coast of Guangdong, China, during the second half of July 2006. The upwelling event off the ELP was observed with low values of SSHA ranging from –30 cm to –20 cm during the sampling periods (Fig. 2). The contour line showed how the low SSHA moved eastward and southward after 19 July 2006.

The horizontal distribution of temperature and salinity in the upper layers is shown in Fig. 3. Cold surface water off the eastern Leizhou Peninsula EPL was observed during the study period (17 July 2006 to 29 July 2006), and the water temperature ranged from 20.20°C to 27.62°C. The sea surface temperature off the ELP was approximately 2°C to 3°C lower than in the offshore waters. Meanwhile, at depths of 10 and 30 m, the sea temperature increased from off the ELP to offshore.

The distinct vertical temperature difference between the surface and 30 m depth was observed off Zhanjiang. There were clear spatial differences in the temperature along the increasing horizontal gradient from the coast to offshore waters. Salinity was lower in the nearshore surface water than in the offshore surface water, and distinguishable zones of low salinity waters (<33.5 PSU) were situated along the ELP coast and off Zhanjiang. However, salinity was generally higher (>34.0) in the nearshore waters at depths of 10 and 30 m than in the offshore water, and decreased rapidly from nearshore to offshore. Generally, upwelling transported cold water from the deep basin to the near-surface layer off Zhanjiang during the survey period. Biogeochemical conditions off ELP

The concentrations of nitrate and DIP were nearly depleted in the surface layer (Fig. 4). Nutrient concentration increased with depth. The distinct vertical nitrate difference between the surface water and water at a depth of 30 m off Zhanjiang indicates that upwelling transported cold water from the deep basin to the near-surface layer. At a depth of 10 and 30 m, horizontal distribution of nitrate showed a decreasing gradient from the coast to offshore waters. The horizontal and vertical variability of DIP was very similar to those of nitrate. Chl-a

concentration was relatively higher at the near-shore regions (>0.2 μg l-1) below the surface water compared to offshore regions (Fig. 4C).

The second distinctive feature along the three transects (D13 to D15) was the high concentration of Synechococcus cells at a depth of 0 and 30 m off the EPL (Fig. 5). The Synechococcus population was dense near the surface at coastal sites (D13-1, D13-2, D14-1, and D15-3), and this population density was associated with the strong upwelling, which increased the delivery of nutrients from the bottom to the surface of the ocean (Fig. 5). Synechococcus cells existed in most of the surveyed areas, but the population density was abundant in the nearshore water (D13). Prochlorococcus was scarce in the deep water column and abundant in the upper water column (Fig. 5), which was possibly due to the light inhibition of Prochlorococcus clades in this region.

The counts of picoeukaryote cells were high off the EPL with a clear maximum at a depth of 40 m in the transect D13 (Fig. 5). The number of eukaryote cells decreased at the same depth of 30 m (D13 to D10) when the upwelling intensity off the ELP slowly decreased after 14 July 2006. CCA

According to the right-tail significance level for the chi-square test, the p-values of the first three canonical axes were 0.00, 0.00, and 0.04, respectively. These results reveal that the environmental variables were of major importance to the observed spatial variations in the picophytoplankton community composition (Fig. 6). Among all the environmental factors, temperature, salinity, phosphate and nitrite concentrations were most strongly correlated with axis 1. Temperature was most strongly correlated with axis CCA1 (–1.5193), and was followed by salinity (–0.8562). Therefore, temperature and salinity were the primary determinants of picophytoplankton, as shown by the positions of picophytoplankton groups along axis CCA1. Prochlorococcus and Synechococcus showed negative and positive scores along axis 1, respectively.

The parameter lines were obtained from the factor loadings of the original variables. These lines represent the contribution (significance) of the parameters to the samples. The two-parameter lines are placed close to each other, and the proximity increased with their increasing mutual correlation. Temperature, salinity, and phosphate were positively correlated with Prochlorococcus (Fig. 6). Temperature


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and salinity were mostly negatively correlated with Synechococcus. Vertical and horizontal diversification in the samples was observed. A cluster of samples in the coastal upwelling region was characterized by the occurrence of Synechococcus, whereas another cluster of samples in the non-upwelling region and in the deep region − by Prochlorococcus (Fig. 7). DISCUSSION

The ecological effect of upwelling has become an attractive topic of research in the previous decades. Upwelling can transport bottom/subsurface water to the surface, and rich deep sea water can stimulate phytoplankton growth. Several studies have focused on changes in the phytoplankton community induced by upwelling (Rodriguez et al. 2003, Linacre et al. 2010, van Dongen-Vogels et al. 2012). These studies showed that the vertical location, magnitude, and composition of the maximum chlorophyll content can be highly affected by changes in the vertical nutrient transport and pycnocline oscillations, which are associated with coastal upwelling. In the study

area, the permanent feature of the cold eddy with its center located at 111°E, 20.30°N has been identified off Zhanjiang in the summer (Guan and Fang 2006, Guan and Yuan 2006). The general feature of the coastal upwelling event observed off the EPL was the transportation of cold water from the deep basin to the near-surface layer along the ELP, where the landward rise of subsurface seawater occurred inside Zhanjiang. Upwelling may be caused by wind and bathymetric changes across the extended shelf region where the bottom depth gradually increases seaward. These factors may facilitate the upwelling of deep water along the bottom slope of the ZB, and cause more nutrient loading.

Our results show a similar pattern of nutrient profiles along the three transects, with higher concentrations near the subsurface layer of coastal waters and lower concentrations at the surface of offshore waters. In the coastal upwelling region, both nitrate and phosphate concentrations were depleted within the euphotic zone. Upwelling was generally intense in the upper layers, Chl-a concentrations at the same depth were relatively higher in the near-

Fig. 3. Horizontal distributions of temperature (A) and salinity (B) at different depths: 0 m, 10 m and 30 m, respectively.



shore region than in the offshore region (Fig. 4C). A higher Chl-a concentration can be supported by a higher nutrient supply from the deep waters induced by upwelling. The coastal upwelling region was characterized by different population densities of Prochlorococcus and Synechococcus in different transects (D13, D14, and D15). These differences in picophytoplankton characteristics in the coastal upwelling region resulted from upwelling intensity. Coastal upwelling was observed in the summer of 2006 (Fig. 2). The biological responses were affected by a combination of timing, magnitude, and duration

of nutrient inputs, which varied with upwelling intensity.

CCA results demonstrate that the population densities of Prochlorococcus and Synechococcus in different water masses (coastal and offshore waters and euphotic layer) were associated with temperature, salinity, and nutrients. Nutrient concentrations were high near the subsurface layer of coastal waters but low at the surface of offshore waters. Population density of Synechococcus was higher in the coastal upwelling region compared to the non-upwelling region (Fig. 5), which may indicate that nutrient

Fig. 4. Horizontal distributions of A) nitrate, B) DIP and C) Chl-a at different depths: 0 m, 10 m and 30 m, respectively.


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availability determines the Synechococcus growth (Chen et al. 2007). Upwelling led to the dominance of Synechococcus in the surface and fluorescence maximum depths, but Prochlorococcus was dominant in upwelled bottom waters (van Dongen-Vogels et al. 2012). Similarly to upwelling, cold eddies transport cold and nutrient-rich water to the surface layer. The population density of Synechococcus significantly increases in the recently occurring cold eddy, whereas Prochlorococcus dominates in the cold eddy and

surrounding oligotrophic waters along the Vietnam coast in the SCS (Jing and Liu 2011). The number of Synechococcus was higher than the number of Trichodesmium in the surface water, and higher inside than outside the eddy in the Luzon Strait bordering the SCS (Chen et al. 2007). Synechococcus was more abundant in the plume-affected and coastal waters compared with Prochlorococcus, which dominated in the oligotrophic water in the Mississippi River plume and adjacent waters (Liu et al. 2004). Compared with the

Fig. 5. Typical vertical profiles of picophytoplankton (cell concentration 104 ml-1) in three transects: D13 transect, D14 transect and D15 transect of Zhangjiang and Hainan. Samples were collected on 17-23 July, 2006.

Fig. 6. Canonical correspondence analysis (CCA) biplot showing the relationship between phytoplankton groups (Eukaryotes, Synechococcus and Prochlorococcus) and environmental factors. The length of each line is correlated with the degree of relationship between the response variables.



population of Synechococcus, the population of Prochlorococcus did not increase with the increasing nutrient concentration in the eddy. As evidenced by the previous studies, Prochlorococcus dominates in subtropical oligotrophic oceans (Campbell et al. 1994, Goericke and Welschmeyer 1993), whereas Synechococcus is usually more abundant in intermediate nutrient conditions (Liu et al. 1997). Prochlorococcus can outcompete Synechococcus only in highly oligotrophic oceans. The sea surface temperature and salinity along the coast of Zhanjiang were lower compared to offshore waters (Fig. 3). Prochlorococcus was absent in coastal waters, whereas Synechococcus was absent in offshore waters (Fig. 5). The population density of Synechococcus was associated with low temperature and salinity in coastal waters, whereas that of Prochlorococcus − with high temperature and salinity. The population density of Synechococcus has also been reported at fairly high amounts in environments with low salinity and/or temperature. By contrast, Prochlorococcus is less ubiquitous and by far the most abundant group in the central oligotrophic part of oceans.

In this study, Synechococcus was absent at depths below 30 m, whereas Prochlorococcus was present at depths below 50 m (Fig. 5). The effect of light explains the vertical distribution of Synechococcus and Prochlorococcus. The euphotic depth was approximately 30 m in the nearshore waters and even below 80 m in the offshore waters (Song et al. 2012). Synechococcus may thrive in either green or blue water, whereas Prochlorococcus adapts to blue waters from the surface down to the water depths receiving 0.1% of the

irradiance incident at the surface. Prochlorococcus may grow under low light intensities compared with Synechococcus in the field (Moore et al. 1995). CONCLUSIONS

Temperature, salinity, nutrient concentrations, and picophytoplankton communities in coastal upwelling and non-upwelling regions off Zhanjiang and east Hainan in the northern SCS were significantly different. In the coastal upwelling region, Prochlorococcus was absent and the population density of Synechococcus was significantly high. By contrast, Synechococcus was absent in the offshore water. Multivariate analysis demonstrated that the population density of Synechococcus was associated with low temperature and salinity in coastal waters, whereas that of Prochlorococcus − with high temperature and salinity. In addition, both Prochlorococcus and Synechococcus populations within the euphotic zone showed significant vertical differences in coastal upwelling and non-upwelling regions. Synechococcus was absent at depths below 30 m, whereas Prochlorococcus was found below 50 m. Light may also be an important factor affecting the vertical distribution of both Synechococcus and Prochlorococcus. Thus, coastal upwelling affected the physical-chemical environment, and resulted in subsequent changes in the picophytoplankton community. ACKNOWLEDGEMENTS

We thank the Captain and the crew of RV Shiyan 3 for their help at sea. This research was supported by the National Natural Science Foundation of China (No. 31270528 and No. 41206082), the project of the knowledge innovation program of the Chinese Academy of Sciences (No.SQ200913), the Key Laboratory for Ecological Environment in Coastal Areas, State Oceanic Administration (No. 201211), and Chinese Offshore Investigation and Assessment (908-01-ST08 and GD908-02-05), Strategic Priority Research Program of the Chinese Academy of Sciences (XDA11020202),National High Technology Research and Development Program of China (863 Program, 2012AA092104, 2013AA092901). REFERENCES Agawin, N. S. R., Duarte, C. M. & Agusti, S. (2000). Response of

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Fig. 7. Canonical correspondence analysis (CCA) biplot showing the distribution pattern of different sampling sites.


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