The Yangtze River Estuary and the Zhejiang coastal waters have a high incidence of spring phytoplankton bloom and even red tide, but there are rarely phytoplankton blooms in the open waters off the Yangtze River Estuary in the spring considering its relative oligotrophy. From 25 April to 7 May 2007, two strong phytoplankton blooms were observed in the open sea area (the east by 125° E-box C), and the chlorophyll-a concentration, whether measuring through remote sensing or in situ, consistently indicated bloom characteristics. Chlorophyll-a concentration in this area increased significantly, even up to 11 mg·m−3 at individual stations during this period. Average chlorophyll-a measured by remote sensing in region C (125–127°E, 30–32°N) was 2.07 mg·m−3, while the climatic average was only 0.97 mg·m−3 during 2000 to 2008. Analyses demonstrated that suspended sediment concentrations had almost no change, but a slight decrease occurred during the two blooms periods as well as low nitrate and phosphate and higher silicate and salinity in box C. It was suggested that the increased chlorophyll-a concentration was not caused by the intrusion of dilute water from the estuary with high suspended sediment concentrations and nutrients, but probably due to local strong winds on the night of 26 April to the morning of 27 April. A further study with profile data of chlorophyll-a, temperature, salinity and other parameters indicated that strong mixing by the local wind was the main reason for the blooms.

Introduction

A phytoplankton bloom is one of the problems of biological oceanography research, though it is a normal biological phenomenon which occurs with a sharp increase in phytoplankton biomass within a certain period (Song et al., 2011). In the spring, it is common for coastal phytoplankton blooming, even red tide, to occur due to warmer temperatures, appropriate water transparency, and adequate nutrients (Zhou et al., 2003; Shen et al., 2010). Similarly, in the Yangtze River Estuary (YRE) and Zhejiang coastal waters, with eutrophication, phytoplankton blooms and even red tide disasters happen every year in the spring. In the past 10 years, red tides happened in the YRE and Zhejiang coastal waters more often than in 60% of the national waters of China (Lei, 2011). However, it is seldom reported whether these bloom events take place in the area off YRE in the spring, and the mechanism is not clear.

The research of phytoplankton blooms started in Atlantic coastal waters. It focused on the North Sea in Europe and the Gulf of Maine in North America and records were made about the research in the North Sea in the 19th century. Bigelow (1926) carried out a scientific study concerning morphology and biomass of phytoplankton on temporal and spatial distribution and found the biomass would reach a peak in the spring and took place during blooms. Sverdrup (1953) summed up the famous “critical depth theory” about condition of blooms which stated that “spring phytoplankton blooms are triggered when the mixed layer depth becomes shallower than the critical depth.” Townsend et al. (1992) pointed out that Gulf of Maine spring blooms may happen before water stratification which may have promoted the formation of the thermocline. Edwards et al. (2004) analyzed decades of observation data and found the main factor impacting the North Sea blooms, other than water mixing, was temperature. Behrenfeld (2010) pointed out that the formation mechanism of spring blooms was contrary to the “critical depth theory” in the North Atlantic. In brief, phytoplankton spring blooms (PSB) on the ocean surface are an important issue of marine ecological dynamics, but their mechanism still remains controversial.

Concentration of chl-a is one of the most important color factors for ocean marine environments, and is closely related to research on biomass and ocean primary productivity (Tang et al., 2002, 2004; Song et al., 2011). In this article, under the support of special project 908, we found a significant increase in phytoplankton biomass in the spring in 2007 off the coast of the YRE through satellite remote sensing and in situ data. Growth of biomass with intense blooms in some areas in the open sea was even more than that in inshore waters. Further studies have shown the main causes were the entrance of high chl-a concentrations and nutrients from sub-layer to surface caused by enhanced vertical mixing from short-term and regional strong winds.

Methods and data

Study area

The research area covered 29–32°N and 122–128°E (box B), but was especially concerned with the phytoplankton bloom area in box C, which was located in the open sea area off the outside of the YRE at longitude 125°E (Figure 1).

Remote sensing and in situ data

Concentrations of chl-a, temperature, depth and salinity were measured using a RBR water quality sensor (±2% mg m−3, ±0.002°C, ±0.1 m and 0.01 psu accuracy). The concentration of chl-a in parts of stations was also measured by “acetone extraction,” with accuracy 0.02 mg m−3 in the laboratory. Chl-a concentration (calculated in Ocean Chlorophyll 4; O’Reilly et al., 1998) and suspended sediment concentration (SCS) (calculated in Pan, 1999; He, 2004) were measured using products with 1.1 km resolution from Aqua/Terra MODIS or SeaWiFS from the Key Laboratory of Satellite Ocean Environment Dynamics of China. Sea surface temperature (SST) was obtained by NOAA/MODIS. The sliding window average fusion (SWAF) method was used for data fusion of remote sensing for several days (Fu et al., 2008). Surface wind data are based on Quick Scatterometer (QuikSCAT) satellite imaging (see http://poet.jpl.nasa.gov).

Results

Distribution of in situ chlorophyll-a concentration

Surface chl-a in some stations in box C was much higher than that in coastal waters. Of nearly 300 stations in the study area (box B), only 69 stations demonstrated a chl-a concentration obtained using both methods. Rough distribution of chl-a on surface shows “low-high-low” from west to east in the East China Sea (ECS) (Figure 2). Chl-a was in the YRE and Hangzhou Bay, with levels as low as 0.09 mg m−3. However, in the offshore area from 122 °E to 124 °E, chl-a levels were higher. In the open sea to the east of 124°E, chl-a concentrations were also lower. Maximum chl-a exceeding 11 mg m−3, obtained both through acetone extraction and the RBR sensor, was from box C, and far away from YRE area.

Chlorophyll-a concentration in the upper layer

Chl-a measured from the upper layer in situ data appeared strong in a bloom in box C. From the measured data of RBR sensor, the average chl-a concentrations in the upper layer of 10 m and 20 m from sections C15 to C17 were calculated and the results are shown in Figures 3a and b, respectively. Sections C15, C16 and C17 were shown with light grey, black and blank rectangles, respectively.

Stations from C17-1 to C17-5 were measured on 9 April 2007. After finishing the stations from C16-1 to C16-5, the sailing was forced to stop due to strong winds in the evening of 26 April 2007, and stations C16-6, C17-6, C15-8, C15-9, C16-9 were measured on 3 and 5 May. From C17-1 to C17-5, chl-a concentration showed a clear downward trend, except in C17-6 which increased significantly. The average chl-a was higher in section C15 than C17, with the maximum exceeding 8.0 mg m−3 in the upper 10 m in C16-6. In the shallow layer to 20 m, this same trend was observed. Furthermore, the mean chl-a concentration in these upper layers of C16-6 was significantly higher than that of other adjacent stations. Mean values of chl-a in C17-10, far away from the coast, measured on 5 May were also higher than that of C17-5, near to the coast, measured on 9 April.

Distribution of chlorophyll-a measured using remote sensing

Two remarkable blooms were observed through remote sensing. Chl-a concentration images with less cloud off the YRE from MODIS are shown in Figure 4: 9 April (a), 19 April (b), 28 April (c) and 7 May (d). There was no remote sensing image available on 3 May, and the image on 7 May was chosen to illustrate the change in chl-a. In early April, the distribution of chl-a in the study area presents normal distribution of “inshore-high and offshore-low,” as demonstrated in 4a and 4b. On 28 April and 7 May, as shown in 4c and 4d, respectively, a strong phytoplankton bloom occurred in the interesting area C labeled rectangle, with extremely high chl-a concentration. Results were calculated and are shown in line 2 and 3 in Table 1.

From 9–19 April, both the mean value and the maximum in box C changed little, staying relatively low; the average chl-a concentration in regional C was 0.93 mg m−3. However, during 25 April to 7 May, the chl-a concentration increased significantly and the average was 2.07 mg m−3, especially on 28 April with the average chl-a, 3.78 mg m−3, significantly exceeding the early level of this month. It is credible that the measured chl-a value exceeded 11 mg m−3 at C16-6 in box C on 26 April because the maximum chl-a was up to 32 mg m−3 on 28 April.

Measurements from only 11 stations could be obtained both in situ and by remote sensing on the same day or adjacent day in box C (shown in Table 2). The results show a high correlation between satellite and in situ data. The relation between in situ measured chl-a and revised chl-a by MODIS was best in the open sea area off YRE (R2 = 0.93).

Chl-a in box C in the spring of 2007 was much higher than the average climate level. The average of chl-a concentration (2000–2005 from SeaWiFS and 2006–2008 from MODIS) in box C in the same period (from 26 April to 5 May) from 2000 to 2008 had an obvious fluctuation from about 0.5 mg m−3 (2006) to 2.07 mg m−3 (2007) (Figure 5), and the mean value over this 8 years in the same period was only 0.97 mg m−3, so the concentration of chl-a in the spring of 2007 was 2.13 times higher than that of the perennial climate condition.

The months average chl-a concentration was calculated in time and space from 3 to 6 months in 2000–2005 in the open sea area of the ECS (OSECS:124–128° E, 26–32° N). The result was as shown in Figure 6. On the one hand, the chl-a distribution revealed a phenomenon with “north high and south low” in this region from March to June. On the other hand, chl-a decreased consistently from March to June, especially during April and May. The change of chl-a concentration from that of the annual climate shows that the chl-a measured on 9 April in section C17 should be much higher than that taken on 27 April and 3 May in section C16 and C15, regardless of the time and spatial. However, the result from our measurement was completely contrary. In short, it can be deducted that there were two strong water blooms in this sea area from April to May in 2007 compared to the annual state climate level.

Discussion

Change of suspended sediment concentration in the study

Because Changjiang diluted water brings a vast quantity of sediment into the ECS, this study area usually has high SSC (Cheng et al., 1984). Many scholars think, for the coastal waters, high SSC will greatly enhance the remote sensing reflection signals, heightening remote sensing data which invert the elements of water color especially chl-a concentration and making large errors (Wren et al., 2005; Hu et al., 2007; Fang et al., 2006). High chl-a from remote sensing in box C was probably caused by the high SSC. The calculation revealed that the SSC in the whole study area B (121-129°E, 28–34°N) had little change from April to May, and the mean value was 8.27 mg l−1 from 14–25 April and 8.58 mg l−1 from 26 April to 8 May. The average and maximum SSC in the C box were calculated and shown in lines 4 and 5 in Table 1. From April to May in the C box, both average and maximum SSC had a downward trend. The average SSC in first three volumes in the line 4 was 0.87 mg l−1 and in the last three, 0.61 mg l−1 with lower level. Therefore, the high chl-a concentrations on 28 April and 7 May in box C were not due to the high inversion error caused by high SSC; meanwhile, high correlation between remote sensing and in situ data indicated the chl-a concentration from remote sensing was reliable.

Is this bloom then caused by the diluted water from the YRE which brings high nutrients into the open sea area under the wind and current? The spring distribution of salinity and nutrients in the study area were further analyzed to determine the answer.

The distribution of salinity and nutrients

Waters with low salinity were almost limited to the west by 124°E. The salinity distribution in the spring of 2007 had typical features of spring salinity distribution in the YRE (Figure 7), namely, there were two freshwater tongues outward with low salinity from the mouth of the Yangtze River, one with inconspicuous shape stretched northeastward shown as line segment X1 and the other with a narrow-band stretching obvious tendency, southeastward extended to the outer of the longitude 124°E as line segment X2, while there was almost high salinity in the special interested box C. Therefore, the diluted water from the YRE in the spring of 2007 mainly limited approximately to the west of longitude 124°E. It is clear that the water bloom in the open sea area was not caused by the nutrients from diluted water of the YRE.

There were lower nitrate and phosphate and higher silicate in the box C in the spring in 2007. The distribution of nutrients concentration is “coastal-high and outer-low” in the spring in the ECS. The concentrations of nitrate and silicate in some area in the coastal waters were up to 100 umol l−1 (Tang et al., 1990). In the outer of YRE, they were much lower and even not detected in some stations. In the spring of 2007, the distribution of nutrients in the box C was shown in Figure 8. Except for C18-3 with high nutrients, the nitrate and phosphate were very low in the box C, especially in the bottom right corner from section 13 to 16, and the concentrations of nitrate and phosophate in most stations were less than 2.0 umol l−1 and 0.1 umol l−1, respectively. And the concentration of nitrate and phosophate on the surface in the early of May was lower than that in the late of April in the box C. Low SSC, nitrate and phosophate and high salinity in the box C consistently pointed to that the diluted water from YRE in the spring in 2007 was not entered into this area. However, the silicate concentration was much higher in the box C, especially from section 15 to 16 where bloom happened. So, the strong phytoplankton blooms may come from high silicate concentration and high chl-a from subsurface or deeper layer due to strong vertical mixed by the wind.

Change of sea in box C with time

Daily average SST in box C from 24 April to 7 May was calculated with 4 images of MODIS (Table 3). SST-aver and SST-max in the Table 2 is average and maximum SST, respectively. The SSTs on 26–28 April were obviously lower than other days’. One of the reasons was surface sea water evaporation to release the massive latent heats and the other was vertical mixing between surface water with high temperature and deep layer with lower temperature caused by local strong wind from the evening on the 26 April to morning on 27 April.

Chl-a, temperature, salinity and turbidity in profile

The chl-a, water temperature, salinity and turbidity of latitudinal sections C16, C17 and C15 have been measured (Figures 9–11). Sections C16, C16-2∼C16-5 were measured on 26 April and C16-6 on 3 May. Surface chl-a on C16-6 reached its maximum value, exceeding 12 mg m−3 (Figure 9a). This value gradually decreased with at greater depths and the spring layer of chl-a was about 20 m. At the other stations, the general characteristics of low chl-a level on surface and high on sub-surface (about 10 to 20 m) were consistent with this finding. At the same time, chl-a on subsurface in C16-3 was higher than the others and its thermohaline profile revealed high salinity and low temperature shown in Figures 9b and c. So this high chl-a in C16-3 may be from the local mixing. In addition, There was a very low turbidity on the surface in the whole section C16 from Figure 9d and further indicated a lower SSC in this area at that time.

To the section C17 (Figure 10), we measured from C17-1 to C17-5 on 9 April and C17-6 on 3 May. In Figure 10a, the chl-a concentration maximum layer was at 10∼20 m. To the C17-6, the profile distribution in chl-a with maximum in the subsurface layer was different to the adjacent C16-6, furthermore, the unstable value of chl-a up to 8 mg m−3 seating about 10 m was much higher than that of the other stations near to the coast in this section. The salinity of the section was very high almost above 33 psu as Figure 10c. There was a remarkable spring layer of turbidity in 25 m under the waters, but very low turbidity less than 5FTU covered the whole surface on this section (10d). Therefore, it was high clean waters in the upper layer in this section.

Although there were only 4 chl-a samples in section C15 (from C15-4 to C15-1 in the order of the measurement time), they were all rare samples measured in wild wind in the early morning of 27 April. The distribution of chl-a on the upper layer (Figure 11a) was opposite to that of section C17. On section C15, chl-a concentration was higher on the surface than on the subsurface, and gradually reduced with the depth. At the same time, from east to west (near to the coast), the surface chl-a increased significantly. Depth of mixing layer was more than 20 m on C15-1 and almost up to the bottom from C15-2 to C15-4 from Figure 11b. This result indicated high chl-a from remote sensing on 28 April is from the subsurface by mixing under the action of a strong local wind.

Distributions and changes about chl-a and seawater temperature in profile of this area could be clearly observed from sequence diagrams from 26 April to 3 May near to C16-6 (Figure 12). On the one hand, chl-a concentration at C16-4 measured before strong wind was a typical characteristic distribution with a high signal peak in subsurface about 10–20 m, and the thing was approximately same at C17-6 measured on 3rd May after a week of the wind, But unstable chl-a concentration at C15-4 and C15-3 under strong wind was much higher on the surface and then gradually decreased with the depth. Chl-a on the surface layer at C16-6 was significantly higher than others. On the other hand, the temperature at C16-4 before strong wind was very similar to those of C16-6 and C17-6 after a week of wind in general. There was an obvious thermocline about in depths of 20 m at C16-4, 25-30 m at C17-6 and C16-6, respectively, and the change of average water temperature above thermocline was more than 3°C to these three stations; however, the water temperature vertical distributions are similar both on the C15-4 and C15-3 during strong wind, whose thermoclines almost disappeared. The water temperature difference between surface and bottom on station C15-4 and C15-3 was less than 0.5°C and 1°C, respectively. The temperature on upper layer of station C15-3 fluctuated obviously, which indicated that the water vertical mixing was strong and fully. Meanwhile, it could be found from the change of water temperature and Chl-a of time sequence that physical processes like water temperature and mixing caused by strong wind responded and disappeared quickly. It may be said “easy come easy go;” however, corresponding biochemical effect such as change of chl-a concentration was relatively slow, which could lasted for more than 1 week.

Upwelling by strong wind

Many studies show that strong winds, and tropical storms may cause upwelling which results in high nutrients in seawater from the deep layers of cold water to pump up to surface layer so that phytoplankton grow exuberantly and chl-a concentration increases significantly (Wei et al., 2007; Fu et al., 2008). The calculation shows that the Ekman upwelling velocity on the 25, 26 and 28 April are all relatively weak with only about 10−6 ∼ 10−5 m s−1. Wind power with speed 20 m s−1 on 27 April was comparatively strong and made the corresponding upwelling speed about 2 ∼ 8×10−5 m s−1. In general, the upwelling caused by the wind with small scope and short time was comparatively weak, so this contribution to the bloom was weaker than that of vertical mixing.

In short, the entrance to the surface of high chl-a concentration and nutrients from subsurface caused by local wind was the main cause of blooms in the outer of YRE in the spring in 2007. On the one hand, the disappeared thermoclines and chlorophyll concentration maximum layer in the subsurface indicated that the vertical mixing was strong and rapid under the local wind, and that high chl-a was brought directly to the surface. On the other hand, picophytoplanktons in the ECS could reach its growth peak in 1d on the condition of enough nutrients (Fang et al., 2006). It was the root cause that intense phytoplankton blooms could be observed on 27 and 28 April after wind. Meanwhile, growth of phytoplankton was promoted by high nutrients such as silicate, and lower concentration of nitrate and phosophate in early May than that in late April on the surface in the box C indicated a lot of nutrients were consumed with the growth of phytoplanktons, and the vigorous growth period of phytoplanktons such as prorocentrum donhaiense and skeletonema costatum which are the dominant species during blooms in the ECS is usually between 5d and 10d under the natural lighting (Wang et al., 2008), therefore high chl-a concentration could be observed again on 3 and 7 May. So, local strong mixing of upper layer seawater caused by local strong wind was the primary cause of the two observations to phytoplankton bloom in the outer of YRE.

Conclusions

During the period from 27 April 2007 to 7 May, high chl-a concentrations and phytoplankton blooms were observed twice in the offshore area to the YRE, measured either with remote sensing or by means of in situ measurement, while low SSC, nitrate and phosophate and high salinity were found in this area. This indicated that the increase of chl-a in the offshore area was neither due to high inversion errors from high SSC, nor to high nutrients from the intrusion of diluted water of the YRE. The real reason for the phytoplankton blooms in the offshore area to the YRE at this time was the regional strong wind from 26 to 27 April. Under the fierce wind, strong water mixing and comparatively weak upwelling were evident in this sea area. On the one hand, higher chl-a concentration on subsurface was taken into the surface layer directly through mixing action. On the other hand, high nutrients such as nitrate, phosophate and silicate were taken into the euphotic layer by the vertical mixing, and enhanced photosynthesis of phytoplankton consumed a lot of nitrate and phosophate and promoted exuberant biomass on upper layer. Twice strong phytoplankton blooms were observed in the outer area of YRE. More studies are needed in this important area.

Acknowledgements

Thanks to all my colleagues for their help and to reviewers for their valuable comments and suggestions.

Funding

This study was supported by the National Marine Important Charity Special Foundation of China under contract No. 201305019 and by NSFC (Grant No. 41340049); by Second Institute of Oceanography, State Oceanic Administration Post-Doctoral Starting Fund: JG1208 and JG1319, by the Post-Doctoral Fund of Zhejiang: BSH1301015 and by Guangdong Ocean University Doctor-Starting Fund: E11332.

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