WANG Baoli, LIU Congqiang WANG Fushun, LI Siliang and Sivaji Patra

1) State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang 550002, P. R. China

2) Institute of Applied Radiation, School of Environmental and Chemical Engineering, Shanghai University, Shanghai 201800, P. R. China

Distributions of Picophytoplankton and Phytoplankton Pigments Along a Salinity Gradient in the Changjiang River Estuary, China

WANG Baoli1),*, LIU Congqiang1), WANG Fushun2), LI Siliang1), and Sivaji Patra1)

1) State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang 550002, P. R. China

2) Institute of Applied Radiation, School of Environmental and Chemical Engineering, Shanghai University, Shanghai 201800, P. R. China

We investigated the abundance of different picophytoplankton groups and the phytoplankton pigment ratio in relation to environmental factors such as nutrients and suspended solids along a salinity gradient in the Changjiang River Estuary. The average numbers ofSynechococcusspp. (Syn) and picoeukaryotes (Euk) were (2.7 ±5.1) ×103and (1.1±1.4) ×103cells mL-1, respectively.Prochlorococcusspp. (Pro) was only found in the high-salinity brackish water with the concentration of 3.0×103cells mL-1.Synand Euk numbers both tended to increase offshore andSynshowed a larger variation in cell abundance than Euk. The contribution of picophytoplankton to total phytoplankton biomass increased with increasing salinity and decreasing nutrient concentrations from the estuary to the open ocean. The response of different picophytoplankton groups to environmental variables was different. Water temperature was more important in its control over Euk than overSyn, while nutrients were more important in their influence overSynthan over Euk. Phytoplankton pigment ratios were different in the three different ecological zones along the salinity gradient (i.e., freshwater zone with 0-5 range, fresh and saline water mixing zone with 5-20 range, and high-salinity brackish water zone with 20-32 range), where three different phytoplankton communities were discovered, suggesting that phytoplankton pigment ratios can be considered as a complementary indicator of phytoplankton community structure in the Changjiang River Estuary.

Synechococcus; picoeukaryotes; phytoplankton pigment; salinity; Changjiang River Estuary

1 Introduction

Estuaries are coastal areas where fresh water from rivers and streams mixes with salt water from the ocean. Natural and anthropogenic materials are transported, deposited, and transformed in the estuary. Phytoplankton is sensitive to environmental variables and therefore considered as an important investigated object for environmental change (Stockner, 1988; Gao and Song, 2005). Over the last two decades, human activities have strongly enhanced nutrient loading in the Changjiang River Estuary, resulting in eutrophication and concomitant changes in species composition of phytoplankton, structure of food chain, and element biogeochemical cycle in the ecosystem (Gao and Song, 2005; Zhuet al., 2009; Jianget al., 2010).

Picophytoplankton comprises prokaryotic picocyanobacteria and eukaryotic phototrophs. They are ubiquitous in both fresh water and marine ecosystems (Stockner, 1988). Nowadays, it is well known that, with the enhancement of trophic state, picophytoplankton abundance and biomass increase and its relative importance decreases (Bell and Kalff, 2001; Callieri, 2007). Numerous studies have been conducted with respect to picophytoplankton in the East China Sea (Changet al., 2003; Jiaoet al., 2005; Panet al., 2005). However, few studies focus on picophytoplankton in the Changjiang River Estuary (Vaulot and Ning, 1988; Panet al., 2007; Shanget al., 2007).

In this study we have investigated the abundance of picophytoplanktonSynechococcusspp. (Syn),Prochlorococcusspp. (Pro), picoeukaryotes (Euk) and examined contents of chlorophylla,b,cand carotenoid index, phaeopigment index and related environmental factors along a salinity gradient in the Changjiang River Estuary. Our aim is to elucidate the distributions of different picophytoplankton groups and phytoplankton pigment ratios in relation to environmental factors, and to discern the influencing factors on their distributions in the Changjiang River Estuary.

2 Materials and Methods

2.1 Sampling

Sample collection was carried out on June 19–22, 2005. A total of 19 stations were investigated in the Changjiang River Estuary (Fig.1). Water samples for depth profiles were taken with 5 L Niskin bottles. Sampling depths were 0 and 7 m at stations 6 and 12; 0, 6 and 16 m at station 15; 0, 10, 20 and 30 m at station 17; and 0, 10, 20, 35 and 50 m at station 18. At other stations, water samples were collected from surface water (upper 0.5 m).

Water temperature (T), dissolved oxygen (DO), pH, and salinity were measuredin situusing a portable multi-parameter instrument (pIONneer 65). Water samples for determination of nitrate (NO3-) and dissolved silicon (DSi) were filtered through 0.45 μm acid-cleaned acetate cellulose filters. The filtrates were poisoned by HgCl2and stored in the dark at 0–4℃ before analysis. NO3-was measured with the cadmium reduction method (Parsonet al., 1984) and DSi silicomolybdenum blue method (Strickland and Parsons, 1968) with precision of <5%. Duplicate samples were taken to determine the amount of total suspended solids (TSS, mgL-1), for which the salts trapped on the cellulose filters were removed by distilled water. TSS was calculated by the dry-weight method. Water samples for determining the abundance of different picophytoplankton groups were filtered by 53 μm nylon fabric in order to remove impurities and then were put aside in darkness for 15 min with paraformaldehyde (final concentration: 1%) and stored in liquid nitrogen till analysis in one month (Panet al., 2005).

Fig.1 Map showing sampling locations and sample numbers. The dashed lines are isobaths and depth is given in meters.

2.2 Analysis of Phytoplankton Pigments

One liter of seawater was filtered by 0.45 μm acetate cellulose membrane. Phytoplankton on the membrane was soaked in 90% acetone at 4℃ in the dark for 20 h in order to adequately extract the pigments. The extract was analyzed at 410, 430, 480, 630, 647, 663, and 750 nm wavelengths, respectively, against a 90% acetone blank. The concentrations of chlorophylla,b,c(μg L-1, Jeffrey and Humphrey, 1975), Carotenoid index (CI; Strickland and Parsons, 1968), and Phaeopigment index (PI; Moss, 1967) were calculated according to the following equations:

whereAxis absorbance atxnm;Vais extraction volume in milliliter;Vwis filter volume in liter.

2.3 Analysis of Picophytoplankton

Picophytoplankton samples were analyzed on a FACScan flow cytometer (Becton Dickinson, San Jose, CA, USA) equipped with an air-cooled argon laser (488 nm, 15 mW). Cell fluorescence emissions and light scatter signals were calibrated by adding yellowish green fluorescent beads (1.002 μm) (Polysciences Inc., catalogue # 18660). For each particle in the sample, forward light scatter, side light scatter, orange fluorescence (585 nm± 21 nm), and red fluorescence (>650 nm) were recorded and the data obtained were processed with CELLQuestTMsoftware (Becton Dickinson, San Jose, CA, USA). According to their specific autofluorescence properties and light scatter differences, the different picophytoplankton groups could be discriminated and enumerated (Collier, 2000).

The software SPSS (version 11.5; SPSS Inc.) was used to carry out statistical analysis of the data and Pearson’s correlation coefficient analysis was conducted.

3 Result

Fig.2 Distributions of temperature, pH, dissolved oxygen, salinity, dissolved Si, NO3-, total suspended solids, picoeukaryotes, Synechococcus, chlorophyll a, b, c in the investigated area.

Fig.2 shows the spatial and temporal distributions of water temperature, salinity, DO, pH, TSS, DSi, and NO3-in the studied area. The average values were 23.9±2.3℃ (from 20.2 to 28.7℃) for water temperature, 15.5±12.5 (from 0 to 32.3) for salinity, 7.2±1.0 mg L-1(from 5.4 to 9.6 mg L-1) for DO, 8.0±0.4 (from 7.0 to 8.7) for pH, 77.8±111.3 mg L-1(from 0.3 to 518.2 mg L-1) for TSS, 48.9±33.6 μmol L-1(from 13.5 to 99.9μmol L-1) for DSi, and 57.3±39.2μmol L-1(from 2.2 to 105.5μmol L-1) for NO3-. pH and DO leaned to the increase of salinity. Water temperature decreased with depth and increasing salinity and therefore it showed significant correlations withdepth and salinity (Table 1). At station 15, an upwelling of cold and saline water existed (Fig.2). Low DO appeared with this upwelling and this low DO did not come directly from the Changjiang River Diluted Water in the upper layer, instead it might come from the modified high saline Taiwan Warm Current Water in the deep and bottom layers (Zhaoet al., 2001). TSS showed high values at stations 9-12 (Fig.2), which is located in the Turbidity Maximum Zone that is originated from sediment resuspension caused by salt and fresh water mixing (Panet al., 1999). Since there was an inverse correlation between NO3-and the salinity and between DSi and the salinity, respectively (Table 1), both NO3-and DSi tended to decrease rapidly with the increase of the salinity (Fig.2).

Table 1 Relationships between the investigated factors in terms of Pearson’s correlation coefficient analysis

The average cell abundance was (2.7 ±5.1) ×103cells mL-1forSynwith the range from 0.03 to 17.8 ×103cells mL-1, (1.1 ± 1.4) ×103cells mL-1for Euk with the range from 0.1 to 7.7 ×103cells mL-1, respectively.Prowas only found at station 19 with the concentration of 3.0 ×103cells mL-1.Synand Euk numbers both tended to increase offshore andSynshowed a larger variation in cell abundance than Euk (Fig.2). Euk tended to decrease with depth; however, this phenomenon was not observed forSynand the high cell abundance ofSynappeared in the 10 m layer of seawater at station 18 (Fig.2).Synshowed significant correlations with NO3-and DSi concentrations, while this was not found for Euk (Table 1).

The average concentration was 9.3±13.4 μg L-1for Chlawith the range from 0.4 to 46.1 μg L-1, 0.7±0.7μg L-1for Chlbwith the range from 0.1 to 3.6 μg L-1, and 0.6 ± 0.7 μg L-1for Chlcwith the range from 0.03 to 4.2 μg L-1, respectively. On both sides of the upwelling area (i.e., station 15), one area with high Chlaconcentration appeared. In the freshwater area (stations 1-8), Chla,b, andcshowed a similar variation trend (Fig.2). High Chlaoccurred in upper low salinity area due to the dominance of Changjiang River Diluted Water with ample nutrients in this zone (Songet al., 2009).

4 Discussion

4.1 Distribution of the Different Picophytoplankton Groups in Relation to Environmental Factors Along the Salinity Gradient

The environmental factors in the Changjiang River Estuary are mainly influenced by the extremely high nutrient loads from the Changjiang River and the mixing between the fresh and saline water. Both water temperature and pH show significant correlations with salinity (Table 1), suggesting that they were controlled by the mixing between the fresh and saline water. In surface waters, nutrient concentrations decrease from eutrophic coastal to oligotrophic open shelf waters (Zhanget al., 2007; Chaiet al., 2009; Chenet al., 2010) though patchy character of nutrient distribution can be produced by biological uptake and regeneration in the surface waters (Zhanget al., 2007). In this study, both NO3-and DSi showed significant negative correlations with salinity (Table 1). With the increase of surface salinity from 0 to 23.8, NO3-decreased from 104.3 to 7.7 μmol L-1and DSi decreased from 99.9 to 14.6 μmol L-1; meanwhile, chlorophylladecreased from 46.1 to 1.9 μg L-1, indicating a rapid change of trophic state along the salinity gradient. Phosphate was found to show similar distribution pattern to that of nitrate in the Changjiang River Estuary (Chenet al., 2010). Potential phosphorus limitation mainly took place where the salinity was less than 30 after 2003, while potential silicon limitation occurred in an area of salinity more than 30 (Chaiet al., 2009).

Euk were the most competitive among the picophytoplankton in freshwater zone (0-5 salinity range, named Zone I) with high temperature and abundant nutrients (Figs.2 and 3a); they showed significant correlation with temperature and this phenomenon was not found forSyn, suggesting that water temperature was a more important factor controlling Euk thanSyn. In fresh and saline water mixing zone (5-20 salinity range, named Zone II), picophytoplankton numbers decreased due to the limitations forced by high turbidity (the radiation effect). In highsalinity brackish water (20-32 salinity range, named Zone III),Synnumbers increased rapidly with low nutrients and clear water while Euk did not, andProwas also discovered (Figs.2 and 3a), suggesting the change of composition of different picophytoplankton groups in this zone.

Fig.3 Picoeukaryotes (Euk) and Synechococcus (Syn) vs the salinity (a), and contributions of Euk and Syn to chlorophyll a (Chl a) vs the salinity (b).

Our previous study showed thatsynhad the significant negative correlation with PO43-(Wanget al., 2008). As phosphate presented similar distribution pattern to that of nitrate (Chenet al., 2010), it can be inferred thatSyncould had close relationship with PO43-in the Changjiang River Estuary and nutrients could be more important factors influencingSynthan Euk (Table 1).Prowas only found at station 19 with a salinity of 23.8 due to its favorable marine environment (Partenskyet al., 1999). These results demonstrated that the responses of different picophytoplankton groups to environment variables such as temperature, light, and nutrients are genus-specific. The picophytoplankton numbers in this study are comparable to these in previous studies conducted in the Changjiang River Estuary (Vaulot and Ning 1988; Shanget al., 2007; Panet al., 2007). The ratios ofSynand Euk numbers to that of chlorophyllaincreased with the increase of salinity (Fig.3b), suggesting the increasing importance of photosynthetic picoplankton from estuaries to the open ocean with the decreasing nutrient concentrations. This result is consistent with the studies of picophytoplankton in Southampton Water (south coast of England; Iriarte and Purdie, 1994) and in San Francisco Bay (Ninget al., 2000).

4.2 Distribution of Phytoplankton Pigment Composition Along the Salinity Gradient

Phytoplankton pigments absorb light over different wavelength ranges. Chlorophyll absorbs it in the 430-450 nm and 600-690 nm ranges, and carotenoid in the 400-500 nm range. Phytoplankton pigment composition can be considered as a taxonomic signature (Stonet al., 2002) because there are highly specific quantities and relative proportions of pigments in particular species. Adaptive divergence in pigment composition promotes phytoplankton biodiversity (Falkowski and LaRoche, 1991; Stompet al., 2004).

Chlorophyta contains Chlaandb, while Bacillariophyta and Pyrrophyta have Chlaandc, diadinoxanthin and β-carotene. Phytoplankton showed lower values of Chla/b,a/c, andb/cin Zone III and higher values of Chla/banda/cin Zone II (Fig.4), indicating that Chlorophyta decreased and Bacillariophyta increased with the salinity. They also showed different CI and PI in Zone II from those in Zones I and III. These results indicate that there were three different phytoplankton communities along the salinity gradient. An earlier study has distinguished these three different phytoplankton communities in accord with salinity gradient in Changjiang River Estuary according to the analyses of phytoplankton species (Table 2; Wang, 2002). Another study found thatMelosira granulataand most of the Chlorophyta species that belong to the freshwater community predominated in Zone I, Euryhaline species such asSkeletonema costatumpredominated in Zone II, and another euryhaline species,Prorocentrum dentatum, predominated in Zone III (Gao and Song, 2005). Different phytoplankton groups have different responses to the environmental variables along the salinity gradient. The optimal range of salinity forP.dentatumgrowth is 25-31 and that forS.costatumis 18-35.7(Chenet al., 2005).S.costatumshowes a much higher phosphatase activity and thus can assimilate phosphorus from the environment much faster thanP.donghaienseunder the same nutrient conditions (Zhaoet al., 2009).

Table 2 Basic ecological parameters for the three different phytoplankton communities

Our study demonstrated that phytoplankton pigment compositions were different in the three different ecological zones (Table 2; Fig.4), where three different phytoplankton communities had been earlier discovered (Wang, 2002; Gao and Song, 2005). Therefore, phytoplankton pigment ratios can be used as the indicator of phytoplankton community structure. Chlaandbcan possibly be overestimated because a small part of them may originate from vascular plant detritus in turbid estuary (Lionardet al., 2008, Zhuet al., 2009); therefore, phytoplankton pigment ratios should be considered a complementary to, but not exclusive replacement for, microscopic observation for understanding the dynamics of phytoplankton.

Fig.4 Phytoplankton pigment ratios vs the salinity. Ca, chlorophyll a; Cb, chlorophyll b; Cc, chlorophyll c, CI, Carotenoid index; PI, Phaeopigment index.

5 Conclusion

The responses of different picophytoplankton groups to environmental variables in the Changjiang River Estuary were genus-specific. Pro was only found in the high-salinity brackish water. Water temperature was more important in its regulation of Euk than of Syn, while nutrients were more important in their influence over Syn than over Euk. The contribution of picophytoplankton to total phytoplankton biomass increased with increasing salinity and decreasing nutrient concentrations from estuaries to the open ocean. Phytoplankton pigment ratios were different in the three different ecological zones along the salinity gradient, indicating that they can be an indicator of phytoplankton community structure in the Changjiang River Estuary.

Acknowledgements

We are grateful to Drs. LI Jun and WU Pan for their assistance in sample collection in the field and to Dr. ZHANG Lihua for her assistance in picophytoplankton determination. It is supported by the Foundation of Chinese Academy of Sciences (Grant No: kzcx2-ew-102) and the National Natural Science Foundation of China (Grant No. 41021062).

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(Edited by Ji Dechun)

(Received April 9, 2013; revised May 21, 2013; accepted July 4, 2013)

? Ocean University of China, Science Press and Springer-Verlag Berlin Heidelberg 2014

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E-mail: baoliwang@163.com