Seasonal Changes in Phytoplankton Biomass and Dominant Species in the Changjiang River Estuary and Adjacent Seas: General Trends Based on Field Survey Data 1959 - 2009

YANG Shu, HAN Xiurong, ZHANG Chuansong, SUN Baiye, WANG Xiulin, and SHI Xiaoyong,

1) Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Ocean University of China, Qingdao 266100, P. R. China

2) Yellow Sea Fisheries Research Institute, Chinese Fisheries Science Academy, Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Qingdao 266071, P. R. China

3) National Marine Hazard Mitigation Service, SOA, Beijing 100194, P. R. China

4) Agricultural Engineering College, Weifang Vocational College, Weifang 261061, P. R. China

Seasonal Changes in Phytoplankton Biomass and Dominant Species in the Changjiang River Estuary and Adjacent Seas: General Trends Based on Field Survey Data 1959 - 2009

YANG Shu1,2), HAN Xiurong1), ZHANG Chuansong1), SUN Baiye4), WANG Xiulin1), and SHI Xiaoyong1),3),*

1) Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Ocean University of China, Qingdao 266100, P. R. China

2) Yellow Sea Fisheries Research Institute, Chinese Fisheries Science Academy, Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Qingdao 266071, P. R. China

3) National Marine Hazard Mitigation Service, SOA, Beijing 100194, P. R. China

4) Agricultural Engineering College, Weifang Vocational College, Weifang 261061, P. R. China

The characteristics of seasonal variation in phytoplankton biomass and dominant species in the Changjiang River Estuary and adjacent seas were discussed based on field investigation data from 1959 to 2009. The field data from 1981 to 2004 showed that the Chlorophyll-a concentration in surface seawater was between 0.4 and 8.5 μg dm-3. The seasonal changes generally presented a bimodal trend, with the biomass peaks occurring in May and August, and Chlorophyll-a concentration was the lowest in winter. Seasonal biomass changes were mainly controlled by temperature and nutrient levels. From the end of autumn to the next early spring, phytoplankton biomass was mainly influenced by temperature, and in other seasons, nutrient level (including the nutrient supply from the terrestrial runoffs) was the major influence factor. Field investigation data from 1959 to 2009 demonstrated that diatoms were the main phytoplankton in this area, and Skeletonema costatum, Pseudo-nitzschia pungens, Coscinodiscus oculus-iridis, Thalassinoema nitzschioides, Paralia sulcata, Chaetoceros lorenzianus, Chaetoceros curvisetus, and Prorocentrum donghaiense Lu were common dominant species. The seasonal variations in major dominant phytoplankton species presented the following trends: 1) Skeletonema (mainly S. costatum) was dominant throughout the year; and 2) seasonal succession trends were Coscinodiscus (spring)→Chaetoceros (summer and autumn) → Coscinodiscus (winter). The annual dominance of S. costatum was attributed to its environmental eurytopicity and long standing time in surface waters. The seasonal succession of Coscinodiscus and Chaetoceros was associated with the seasonal variation in water stability and nutrient level in this area. On the other hand, long-term field data also indicated obvious interannual variation of phytoplankton biomass and community structure in the Changjiang River Estuary and adjacent seas: average annual phytoplankton biomass and dinoflagellate proportion both presented increased trends during the 1950s - 2000s.

the Changjiang River Estuary and adjacent seas; phytoplankton; biomass; dominant species; seasonal variation

1 Introduction

The ecological environment of the Changjiang River Estuary and adjacent seas, which are contiguous to the Changjiang River Delta, is significantly affected by human activities. The eutrophication status of seawater in this area has increased with economic development since the 1980s, resulting in frequent red tides and considerable economic losses (Zhou et al., 2001). The situation has worsened with the advent of the 21stcentury (Zhu et al., 2009). To solve the red tide problem, the ecological environment conditions of this area should be thoroughly understood.

Phytoplankton is the major producer in the marine ecosystem. Studies have shown that the horizontal distribution of phytoplankton biomass in the Changjiang River Estuary and adjacent seas is generally higher in nearshore areas than that off the coast (Zhou et al., 2003). High biomass values generally occur in spring and summer, whereas biomass is generally lower in winter (Zhou et al., 2003). Diatoms are the most important members of the phytoplankton community in this sea area, and Skeletonema costatum, Chaetoceros curvisetus, Paralia sulcata, and others are common dominant species (Gao et al., 2003; Zhang, 2009). However, most of the existing studies on the seasonal variation in phytoplankton in this area,especially those regarding seasonal changes in phytoplankton community structure, were based only on survey data from a single year. The survey times were also limited (Lin et al., 2008; Zhao et al., 2009). The findings in these studies retained the contingency of ecological environment changes in short time scales, which were inadequate in clarifying the general trends of seasonal phytoplankton variation.

In this study, the relatively general seasonal variation characteristics of phytoplankton biomass and dominant species in the Changjiang River Estuary and adjacent seas were analyzed based on field investigations from 1959 to 2009. This study can improve the understanding of the ecological environment in this area, and address the challenging red tide problem.

2 Data Source and Processing

In this study, the target areas are the Changjiang River Estuary and its adjacent area (Fig.1). We collected information on phytoplankton biomass (based on Chlorophylla concentration) and the dominant species in the surface water in recent years. The phytoplankton biomass data were acquired from field investigations (Table 1) of 51 surveys from 1981 to 2004. Information on dominant phytoplankton species originated from field investigations (Table 2) of 96 surveys from 1959, and the period 1990 to 2009.

Fig.1 Study areas. a: seas in the solid line box are the target areas in this study; b: seas in the broken line box are the study areas in previous studies.

Table 1 Data sources of phytoplankton biomass

Table 2 Data sources of dominant phytoplankton species

To investigate the seasonal variation trends in phytoplankton biomass, the results of each field investigation were used to estimate the monthly average Chlorophyll-aconcentration in the target sea area in the survey month. The monthly average biomasses of all surveys were examined to study the seasonal variation trends in phytoplankton biomass. Notably, the study areas in the historical field investigations were incompletely overlapped with the target area in the current study. Thus, the accurate average biomass in our study areas was difficult to confirm. In this study, we assumed that the interannual variation in the horizontal distribution of phytoplankton biomass in the target area was not distinct from 1981 to 2004. With ‘the methods for calibrating average concentration in the domains being partially or totally different from target domains’ (Wang et al., 2010), the average biomass of our target area in the corresponding month was estimated using historical field investigation data (detailed in Sun, 2008).

The compositions and seasonal changes in the phytoplankton community were estimated using dominant species information obtained from field investigations in the target sea area from 1959 to 2009. An accurate understanding of the compositions of the phytoplankton community in this sea is difficult to obtain because of the considerable regional difference in the distribution of the phytoplankton community and the incomplete overlapping of the study areas in this study with the study areas of previous field investigations. Due to these limited conditions, we can only roughly examine the seasonal variation characteristics of the phytoplankton dominant species using existing data. Data in Table 2 from 96 field investigations in the Changjiang River Estuary and adjacent seas were used for this study. 30 of these investigations were conducted in spring, 32 in summer, 23 in autumn, and 11 in winter. In each investigation, algae with Y (priority degree) > 0.005 were considered as dominant algae, Y being calculated by

where niis the total amount of algae i obtained during a survey; fiis the frequency at which this type of algae is present in all samples; and N is the total amount of algae obtained during a survey.

3 Results

3.1 Seasonal Variation Features of Phytoplankton Biomass

Based on the field investigation data for the Changjiang River Estuary and adjacent seas from 1981 to 2004, the annual variation scope of the monthly average Chlorophyll-a concentration in the surface water ranged from 0.4 μg dm-3to 8.5 μg dm-3(Fig.2). The Chlorophyll-a concentration was highest in summer, followed by spring and autumn. The biomass was significantly lower in winter, and the lowest value occurred in February. The seasonal biomass variation generally displayed a bimodal distribution trend, with the peak occurring in August and the sub-peak occurring in May. This trend is typical of phytoplankton biomass in temperate seas.

Fig.2 Seasonal Chla changes in the Changjiang River Estuary and adjacent seas.

3.2 Seasonal Variation Characteristics of the Phytoplankton Dominant Species

According to the field investigation data from 1959 to 2009, approximately 67 species of dominant phytoplankton were found in the Changjiang River Estuary and adjacent sea. Diatoms were the major phytoplankton in this area, with 53 species belonging to 23 genera. Diatoms accounted for approximately 80% of the dominant species. In addition, 13 species of dinoflagellates and two types of Cyanobacteria were discovered. S. costatum, Pseudonitzschia pungens, Coscinodiscus oculus-iridis, Thalassinoema nitzschioides, P. sulcata, Chaetoceros lorenzianus, C. curvisetus, and Prorocentrum donghaiense Lu were the common dominant species in this area.

S. costatum was the most dominant species throughout the year. In addition, 15 genera and 32 species of dominant algae (e.g., C. oculus-iridis and P. donghaiense Lu), comprised of dinoflagellates (5 genera and 8 species) and diatoms (10 genera and 24 species), were discovered in spring; 17 genera and 35 species of dominant algae (e.g., P. pungens and C. lorenzianus) comprised of Cyanobacteria (1 genera and 1 species), dinoflagellates (7 genera and 11 species), and diatoms (9 genera and 23 species), were discovered in summer; 16 genera and 25 species of dominant algae (e.g., T. nitzschioides and P. sulcata), comprised of Cyanobacteria (1 genera and 1 species), dinoflagellates (1 genera and 1 species), and diatoms (14 genera and 23 species), were discovered in autumn; and 14 genera and 22 species of dominant algae (e.g., P. sulcata and Biddulphia sinensis), being all diatoms, were discovered in winter.

According to the distribution of major dominant phytoplankton species in each season, the phytoplankton community structure of the Changjiang River Estuary and adjacent seas shows that Skeletonema and Coscinodiscus were the most dominant in winter and spring, whereas Skeletonema and Chaetoceros dominated in summer and autumn (Table 3).

Table 3 Major dominant phytoplankton species in the Changjiang River Estuary and adjacent seas†

4 Discussions

4.1 Influential Factors of the Seasonal Variation in Phytoplankton Biomass

Phytoplankton growth is affected by temperature, salinity, illumination, nutrient levels, trace elements, and other factors. Previous studies showed that temperature, illumination, and dissolved inorganic nutrients in the Changjiang River Estuary and its adjacent sea have relatively significant impacts, and temperature and nutrient levels are the major factors influencing seasonal variation in phytoplankton biomass (Han, 2009). According to the statistical results in this study, phytoplankton biomass was relatively low in winter when the amount of nutrients (DIN, PO4-P, and SiO3-Si) was generally high (Fig.3). Phytoplankton growth is not prone to the constraints of nutrient levels. Thus, low biomass may be correlated with low water temperature and illumination (Fig.4). Studies showed that the optimum growth temperature for common phytoplankton, such as S. costatum and P. donghaiense, in this area is above 20℃ (Yu, 2005), and below this, with the decreasing of temperature, the limitation of algae growth is enhanced. Besides, throughout the year, solar radiation intensity can meet the requirements for phytoplankton growth (Maucha, 1940). Thus, temperature may be the major factor that controls the phytoplankton biomass in winter. The water temperature in our study area was lowest in February, and could drop to below 10℃. The Chlorophyll-a concentration in this period was also the lowest for the entire year at approximately 0.4 μg dm-3.

Fig.3 Seasonal changes in phytoplankton biomass (Chla), nutrients (DIN, PO4-P, and SiO3-Si), and Changjiang River dischargea. DIN, PO4-P and Changjiang River discharge data were obtained from Tang, 2009; SiO3-Si data were obtained from Zhang, 2008.

Fig.4 Seasonal changes in temperature and solar radiation fluxa. Temperature data were obtained from Han, 2011; solar radiation flux data were obtained from Sun, 2008.

As the water temperature increases in spring, the constraint of temperature on algae growth gradually weakens. The Chlorophyll-a concentration continued to increase and peaked in May. Zhang (2008) suggested that diatoms in this area could grow substantially at water temperatures higher than 11.5℃, which further triggers red tide. In addition to adequate temperature and illumination, the Changjiang River runoffs, which can supply nutrients, also cause the generally high level of phytoplankton biomass in April and May.

In May and June, the decline in Chlorophyll-a concentration was mainly due to the lowered nutrient levels. The Changjiang River runoffs declined during this period, and the nutrient supply gradually decreased. In addition, the substantial growth of phytoplankton further decreased the nutrient level in seawater. And then the nutrient level became a major limiting factor in phytoplankton growth. By June, the nutrient level and Chlorophyll-a concentration dropped to their minimum values. At this time, temperature and illumination were adequate for phytoplankton growth, so they were not the major limiting factors in algae growth.

Between June and August, the Changjiang River runoffs increased, and a good supply of nutrients was provided to the Changjiang River Estuary and adjacent seas. Thus, the phytoplankton biomass increased and peaked at around August. Although the phytoplankton biomass level decreased after this period, it remained at a relatively high level. Until October, the Chlorophyll-a concentration still remained above approximately 2.1 μg dm-3. During this period, water temperature and illumination intensity were at their highest levels for the year at 28.7℃ (August) and 262 W m-2(July), respectively. Although phytoplankton growth was believed to be limited in high temperature or high illumination conditions, the variation tendency of phytoplankton biomass did not demonstrate evident temperature or illumination constraints during this period. Thus, temperature and illumination were not the major restrictive factors, whereas the nutrient levels (including the nutrient supply from the Changjiang River runoffs) were the major influential factor in phytoplankton growth in the Changjiang River Estuary and adjacent seas in summer and autumn.

After November, with the drop of water temperature, DIN and illumination, the Chlorophyll-a concentration continued to decrease. And in winter, low temperature and illumination, especially the low temperatures, were the main limiting factors in phytoplankton growth again.

In summary, the low water temperature in the Changjiang River Estuary and adjacent seas was the major influencing factor in low phytoplankton biomass from late autumn to early spring. In other seasons, the variation in phytoplankton biomass was mainly subject to the influence of nutrients (including the nutrient supply from the Changjiang River runoffs). The illumination intensity had a less significant impact on the seasonal variation in phytoplankton biomass. Not only in the Changjiang River Estuary and adjacent seas, but also in the East China Sea, the northern Yellow Sea, and the North Atlantic Ocean are the seasonal changes of phytoplankton biomass mainly controlled by temperature and nutrients (Dutkiewicz et al., 2001; Gong et al., 2003; Teira et al., 2005; Gao, 2009). In addition to the aforementioned influencing factors, hydrodynamic condition, predator-prey relationship, and other factors can equally influence phytoplankton biomass levels. For example, Dutkiewicz examined the relationship between phytoplankton biomass seasonal changes and hydrodynamic condition in the Atlantic Ocean (Dutkiewicz et al., 2001) and Wei insisted that phytoplankton biomass distributions related well to the vertical turbulent mixing of the waters (Wei et al., 2001). However, these other factors are not discussed in this study because of limitations in data.

4.2 Influential Factors for Seasonal Variation in Phytoplankton Dominant Species

The major features of seasonal variation in phytoplankton dominant species in the Changjiang River Estuary and adjacent seas were: 1) Skeletonema (mainly S. costatum), which was the major phytoplankton in this area, dominated throughout the entire year; 2) other major dominant phytoplankton species followed the seasonal succession trends of Coscinodiscus (spring)→ Chaetoceros (summer and autumn)→ Coscinodiscus (winter).

S. costatum is a typical eurythermal and euryhaline alga, which is found globally in the Arctic, equator, heavy salt water of open seas, and low saline coastal water (Jin et al., 1965). Compared with other phytoplankton species, the impact of environmental factors, such as temperature, illumination, and nutrients, on the growth of S. costatum was relatively small because of its environmental eurytopicity. Besides, the small particle size of S. costatum (approximately 6 μm to 7 μm) (Jin et al., 1965) enables it to remain in the euphotic layer for a long period, which is conducive to its growth. Thus, Skeletonema remained dominant throughout the year.

According to results of Sun, the optimum illumination intensities for Coscinodiscus and Chaetoceros are relatively close to each other at 49.9 ± 4.9 W m-2and 54.4 W m-2, respectively (Sun, 2008). Thus, illumination may not be the major influential factor in the seasonal successionof Coscinodiscus and Chaetoceros. Similarly, temperature was not a key factor that directly influenced the seasonal succession of Coscinodiscus and Chaetoceros. Studies have showed that the optimum growth temperature of Coscinodiscus jonesianus is approximately 27℃ (Huang et al., 1998), whereas those of Chaetoceros. curvisetus and Chaetoceros socialis are 25℃ and 26℃ to 30℃, respectively (Yu, 2005; Wang et al., 1990), the differences being not significant. Besides, in the Changjiang River Estuary and adjacent seas, the major species of these two genera, such as Coscinodiscus radiatus, Coscinodiscus oculus-iridis, Coscinodiscus asteromphalus, Chaetoceros curvisetus, Chaetoceros socialis, and Chaetoceros affinis, are all eurythermic (Jin et al., 1965). Therefore, the influence of temperature on the growth of Coscinodiscus and Chaetoceros may not be distinct obviously. However, the vertical mixing of water, which can be influenced by the seasonal variation of sea surface temperature, may further influence the seasonal succession of Coscinodiscus and Chaetoceros. It is believed that a high rate of upwelling tends to favor large-cell phytoplankton production for the reasons that in mixed water columns, the large-cell phytoplankton could remain in the euphotic layer for a longer time (Parsons and Takahashi, 1973). In the Pacific Ocean, velocity of vertical water movement has been considered as one of the three major factors governing the production of small and large algae (Semina, 1972). In the Changjiang River Estuary and adjacent seas, the surface temperature is relatively low in winter and spring, thus the vertical mixing of water is relatively intense, and thermocline is not formed. Larger Coscinodiscus (with a particle size generally larger than 100 μm) (Jin et al., 1965) can remain in the surface water for a long period, which is conducive to their growth. Thus, Coscinodiscus became the major dominant species during this period. In summer, a significant thermocline forms in this area, so the vertical mixing of water is hindered, and the water is more stable. At this point, larger Coscinodiscus generally tends to sink. Because of the shortened retention time of the larger Coscinodiscus, they are replaced by smaller Chaetoceros (with particles smaller than 50 μm) (Jin et al., 1965), which can remain in the surface water for a longer time. Except for water stability, nutrient in water bodies is also an important factor controlling succession of phytoplankton. Compared with large-cell phytoplankton, small-cell phytoplankton has larger specific surface areas and can grow better in low-nutrient environment for their stronger ability to absorb nutrients (Friebele et al., 1978). In the Changjiang River Estuary and adjacent seas, the nutrient level is relatively low during summer, and supplement of upper water nutrients is limited by stratification of water bodies. In contrast with Coscinodiscus, smaller Chaetoceros which have more specific surface areas can grow in these low nutrient levels better. While in whiter, water nutrients levels are relatively high, which fits the growth of largecell Coscinodiscus.

In summary, the impacts of temperature and illumination on the seasonal succession of major dominant species are relatively small in the Changjiang River Estuary and adjacent seas. The seasonal variation in water stability and nutrient levels are possibly the major factors influencing the seasonal succession of major algae in this area.

4.3 Interannual Variation of Phytoplankton Biomass and Component

When seasonal changes of phytoplankton biomass and dominant species were studied based on field investigations data in recent years, interannual variations of phytoplankton biomass and component were also observed in the Changjiang River Estuary and adjacent seas. Since 1981, average annual phytoplankton biomass has increased obviously (Fig.5a), which is consistent with the results of Wang and Cao (Wang, 2006; Wang and Cao, 2012) well. It has been believed that water body eutrophication caused by development of human society mainly results in the increasing biomass. Sun insisted that enhancement of solar radiation in recent years could also promote the growth of phytoplankton in the Changjiang River Estuary and adjacent seas (Sun, 2008). Meanwhile, phytoplankton community structure also changes obviously. Although diatoms were always predominant among all phytoplankton in certain years, the amounts of dinoflagellates increased obviously and their proportion among all phytoplankton had increased from less than 5% in the 1980s to about 20% in the 2010s (Fig.5b). On the other hand, the frequent occurrences of dinoflagellate bloom in the Changjiang River Estuary and adjacent seasafter 2000 also imply their importance in the present phytoplankton system. And water eutrophication and increased N/P ratios are generally considered able to promote the growth of dinoflagellate (Hodgkiss et al., 1997; Anderson et al., 2002).

Fig.5 Interannual variation of average annual phytoplankton biomass (a) and community structure (b) over the past 30 years. Data processing and other detailed information are to be published.

As mentioned above, when the long-term field investigation data were used to study seasonal changes of phytoplankton biomass and component, we assumed that the phytoplankton system in the Changjiang River Estuary and adjacent seas has been relatively consistent during the last 30 years. However, according to previous studies and our results, phytoplankton biomass and component changed obviously during 1981-2009. So the accuracy of our results, including seasonal variation patterns of phytoplankton biomass and dominant species, would be weakened or questioned. But, when compared with the long-term phytoplankton system changes such as those in tectonic scale, orbital or sub-orbital time scale, these 30-year phytoplankton changes in the Changjiang River Estuary and adjacent seas are relatively small. So we insist that the assumption mentioned above is reasonable and acceptable, and the final results in this paper are believable. On the other hand, in previous studies, discussions of phytoplankton seasonal changes were usually based on limited data of several field investigations, and contingency variations of ecological environment are inevitable. Compared with these contingencies, our results could better represent the general characters of phytoplankton seasonal changes on the macro level.

5 Conclusions

According to several years of field investigations in the Changjiang River Estuary and adjacent seas, the monthly average concentration of surface Chlorophyll-a is between 0.4 and 8.5 μg dm-3. A ‘bimodal’ seasonal distribution has generally been observed, with the peaks occurring in May and August. Temperature is the major control factor in low phytoplankton biomass from the end of autumn to early spring. In other seasons, the nutrient level (including the nutrient supply from the Changjiang River runoffs) is the major influential factor in phytoplankton biomass variation. The phytoplankton in this sea are mainly composed of diatoms, and the seasonal variations in major dominant species are as follows: 1) annual dominance of Skeletonema (mainly S. costatum); 2) seasonal succession trends of Coscinodiscus (spring) →Chaetoceros (summer and autumn) → Coscinodiscus (winter). The environmental eurytopicity of S. costatum and its long standing time in surface waters may be the major reasons for its annual dominant status. The seasonal succession of Coscinodiscus and Chaetoceros is correlated with the seasonal variation in water stability and nutrient level. During the 1950s -2000s, the average annual phytoplankton biomass and dinoflagellate proportion among all phytoplankton are proven to be increased, so more attention on these ecological changes should be paid.

Acknowledgements

The authors wish to appreciate the supports from the National Basic Research Program of China (Nos. 2001 CB409703 and 2010CB428701) and the National Natural Science Foundation of China (Nos. 41140037 and 41276 069).

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(Edited by Ji Dechun)

(Received October 17, 2013; revised April 15, 2014; accepted May 11, 2014)

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

* Corresponding author. Tel: 0086-532-82032479

E-mail: shixy@ouc.edu.cn