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Cruise observation of Ulva prolifera bloom in the southern Yellow Sea, China
Estuarine, Coastal and Shelf Science 163 (2015) 17e22
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Cruise observation of Ulva prolifera bloom in the southern Yellow Sea, China Xiangqing Liu a, b, Yan Li a, b, *, Zongling Wang a, b, Qingchun Zhang c, Xiaoqing Cai a a
The First Institute of Oceanography, State Oceanic Administration, 266061 Qingdao, Shandong, PR China Key Lab of Science and Engineering for Marine Ecological Environment, State Oceanic Administration, 266061 Qingdao, Shandong, PR China c Institute of Oceanology, Chinese Academy of Sciences, 266100 Qingdao, Shandong, PR China b
a r t i c l e i n f o
a b s t r a c t
Article history: Accepted 4 September 2014 Available online 28 September 2014
Four cruises were carried out in the southern Yellow Sea from May to June of 2012 with the aim of observing the development of green tides. Free-floating patches of green algae dominated by Ulva prolifera occurred in early May in coastal waters of the southern Yellow Sea with an average biomass of 0.05 g m2. The average biomass of free-floating green algae developed rapidly and reached 3.20 gm2 in mid-May, and the affected area reached 8.7 103 km2 with a total biomass of 1.37 105 tons. In late May, the average biomass reached 5.81 gm2, and the affected area reached 3.2 104 km2 with a total biomass of 2.5 105 tons. In early June, the average biomass reached 8.47 gm2, the affected area covered 3.6 104 km2, and the total biomass of floating green algae was 3.64 105 tons. The affected areas of green tide in our observed data were higher than those estimated from remote sensing images in the early two cruises, and basically matched the remote sensing data in the last two cruises. With the increased biomass and the expansion of the affected area, the free-floating algal patches moved progressively northward. They first appeared in coastal water of middle Jiangsu province, gradually reached 35 N in early May, and finally drifted to the southern coast of the Shandong Peninsula (36 N) after one month. This work can offer help for the early prediction and warning of a green algal bloom and provide decision-making bases for governmental departments. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Ulva prolifera green tides distribution southern Yellow Sea
1. Introduction Since 2007, green tides have occurred in the southern Yellow Sea from May to July each year and caused serious damage to local tourism, aquaculture and the environment (Liu et al., 2009, 2010; Fan et al., 2012). Previous investigations have indicated that the free-floating green tides in the southern Yellow Sea were from the coastal waters of the Jiangsu province and drifted to the southern coast of the Shandong Peninsula under wind-current action (Zhang et al., 2009; Liu et al., 2009, 2010; Yi et al., 2010; Qiao et al., 2011). The above information, however, mainly came from the satellite observation and numerical modeling. Observations in situ are very limited. Due to the resolution limitation of remote sensing (RS) images, small patches less than 250 m2 cannot be detected using RS
* Corresponding author. The First Institute of Oceanography, State Oceanic Administration, 266061 Qingdao, Shandong, PR China. E-mail addresses: liyan@fio.org.cn, abclxqfi[email protected] (Y. Li). http://dx.doi.org/10.1016/j.ecss.2014.09.014 0272-7714/© 2014 Elsevier Ltd. All rights reserved.
techniques. Thus, RS images might underestimate the movement of algal patches and cannot reflect the actual process of Ulva prolifera bloom development. Thus, cruise observations in situ can compensate for the weaknesses of RS and help to illustrate the entire blooming process. Furthermore, the RS techniques cannot be applied to precisely predict and calculate the green algae biomass because the thickness of floating algal mats varied during the bloom. The varied biomass of green tide every summer made the local government difficult to prepare sufficient salvaging facilities and hire enough workers to clean up, and thus an accurate prediction on green tide biomass is important for management. Observations in situ could provide biomass data for algal mats and help administrators make decisions. Therefore, we conducted four cruises in 2012 to investigate the biomass development and spatial movement of green algal patches in the southern Yellow Sea, China. These studies will help to reveal the blooming process of Ulva prolifera and help governors manage the risks of green tides and take precautions against them.
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X. Liu et al. / Estuarine, Coastal and Shelf Science 163 (2015) 17e22
The total biomass is calculated as follows:
2. Materials and methods 2.1. Study area and sampling methods
Wt ¼ 120 000 E
2.2. Species identification and biomass measurement Both morphological characteristics (Ding and Luan, 2009) and fluorescence in situ hybridization (Zhang et al., 2015) were used for on-site species identification. Green algal samples were washed with filtered seawater to remove impurities. The biomass Wi (tons) at station i is calculated as follows:
Wi ¼
Gi Si dL
where Gi is the fresh weight of floating green algae (g); d is the inner opening diameter of the WP2 zooplankton net (m); L is the trawling distance (m); and Si is the quadrat area of station i. Si is calculated as a rectangle, with the length and width determined as described in Fig. 1.
Wi
i¼1
122 300 E
The study area covers offshore water from to and from 33 300 N to 35 220 N range in the southern Yellow Sea (Fig. 1), where the largest macroalgal bloom in the world was observed in 2008 (Liu et al., 2009). Four cruises were conducted with 27 stations along five transections A, B, C, D and E from 2nd of May to 6th of June 2012 as listed in Table 1. The first two cruises were carried out during the clean-up of the Porphyra aquaculture raft, and the last two cruises were carried out after clean-up of the raft. We used a horizontal trawl to obtain the biomass of the macroalgal mats. WP2 zooplankton nets (mesh size 0.5 mm, inner opening diameter 0.8 m) were mounted vertical to the vessel, trawling at 3 knots for 10 min. The trawling distance was measured by global position system (GPS) for further calculation of the biomass.
n X
where Wt is the total biomass of the survey area (tons); Wi is the biomass of station i (tons). The total area of affected area is calculated as follows:
St ¼
n X
Si ;
i¼1
where St is the total quadrat area of affected stations; and Si is the quadrat area in station i. The average biomass of free-floating green algae in the survey area (g m2) is calculated as follows:
B¼
Wt ; St
where B is the average biomass of free-floating green algae in the survey area (g m2); Wt is the total biomass of survey area (tons); and St is the total area of affected stations. 2.3. Acquisitions of RS data The formation of the patches of green algae was tracked using 250 m2 resolution ‘‘MODIS” satellite images (http://oceancolor.gsfc. nasa.gov). The affected area of floating green algae is calculated using the Normalized Difference Vegetation Index (NDVI) method, which generates a strong contrast between the floating patches of algae and the turbid waters of the Yellow Sea. The pixels with floating algae had NDVI values between 0.2 and 0.75, while the areas of water around them had NDVI values between 0 and 0.1. A conservative approach by summing the area of the pixels with an NDVI value of greater than 0.24 was taken to calculate the area of the floating patches. The daily sea surface temperature (SST) was
Fig. 1. The sampling sites in the southern Yellow Sea (120 000 E ~ 122 300 E, 33 300 N ~ 35 220 N, a e rectangles with solid line represent the quadrat area of one station, b e the study area).
X. Liu et al. / Estuarine, Coastal and Shelf Science 163 (2015) 17e22
19
Table 1 The biomass, affected area, species composition and proportion of free-floating green algae during four cruises. Cruises
1 2 3 4
Date
2e6 May 14e22 May 25e29 May 31 Maye6 June
Average biomass (g m2)
0.05 3.20 5.81 8.47
Total biomass (tons)
2.20 1.37 2.50 3.64
3
10 105 105 105
Affected area (km2)
5.7 1.4 2.2 2.7
3
10 104 104 104
Species composition and proportion U. prolifera
U. linza
Blidingia sp.
Others
98.3% 98.9% 99.3% 99.4%
1.1% 0.3% e e
0.2% 0.3% 0.1% e
0.4% 0.5% 0.6% 0.6%
(“e” indicates the species was not found). The average biomass is the average biomass of free-floating green algae in survey area (g m2); the total biomass is the total biomass of survey area (tons); the affected area is the total quadrat area of affected stations in situ investigation (km2).
obtained from the towed conductivity-temperature-depth system data. 3. Results
in three days (Figs. 3c, d). The northern border of the green tides moved to 36 N (Fig. 3d). The area affected by remote sensing was consistent with our observations in these two cruises (Table 1, Fig. 2c, d).
3.1. Species composition of free-floating patches
4. Discussion
Floating green algae were composed mainly of Ulva prolifera (>98%), with a few other green algae (e.g., U. linza and Blidingia sp.).
The important finding of our investigation was that we revealed the whole developmental process of the world's largest macroalgal bloom from two aspects. The biomass of green algal patches dominated by Ulva prolifera increased dramatically in just over one month. Meanwhile, the affected area expanded sharply to nearly 36,000 km2 and spread across two provinces in China.
3.2. Temporal variations of green algal biomass The biomass of floating green algae increased rapidly over time during MayeJune 2012 in the southern Yellow Sea as shown in Table 1. In early May, the average biomass of free-floating green algae was 0.05 gm2, and the total biomass was 2.2 103 tons in the studied area. In mid-May, we found that the biomass of freefloating green algae dramatically increased, and the percentage of Ulva prolifera was slightly elevated. The average biomass of freefloating green algae was 3.20 gm2, and the total biomass was 1.37 105 tons, which was 62 times greater than that in early May. In late May, the average biomass of free-floating green algae was 5.81 g m2, and the total biomass was 2.5 105 tons, which was 1.8 times greater than that in mid-May. The percentage of Ulva prolifera continued to increase and was higher than 99% in the algal patches. In early June, the average biomass of free-floating green algae was 8.47 gm2, and the total biomass was 3.64 105 tons, which was 1.5 times greater than that in late May. Ulva prolifera was found at the highest proportion in the green algal patches at 99.4%. 3.3. The development of green tides The observed data in our study (Fig. 2aed) basically matched the RS data (Fig. 3aed). The results demonstrated the whole process of Ulva prolifera bloom development drifting from the south to the north in the Yellow Sea. In early May, algal patches were mainly distributed approximately 33 450 N ~ 34100 N and 120 350 E ~ 120 520 E, and the affected area was 2916 km2 (Fig. 3a). In our cruises, algal patches was found approximately 33 300 N ~ 35 N and 120 300 E ~ 121300 E (Fig. 2a). Thus, the affected area based on our observation was higher than that estimated from RS images and reached 5700 km2 as shown in Table 1. In mid-May, RS data showed that the patches began to move north, and the affected area increased to 8748 km2 (Fig. 3b). An identical trend was found during our cruises (Fig. 2b). As with the previous cruises, we observed a considerable amount of green algal patches approximately 33 300 N ~ 35 200 N and 120 E ~ 121300 E in the cruises, and the actual affected area of algal patches was 14,000 km2 (Table 1). In the last two cruises, the algal patches continuously expanded, and the affected area increased rapidly from 32,076 to 36,450 km2
4.1. Rapid increase in green algal biomass The biomass of floating green algae increased 165 times from 2nd May to 6th June 2012 (Table 1). The question of why the rapid growth of Ulva prolifera was triggered during this period should be asked. In essence, Ulva prolifera is the predominant green tide species, with high rates of nutrient uptake (Raven and Taylor, 2003). During the blooming period, the dissolved inorganic nitrogen (DIN) concentrations was 7.84e13.53 mmolL1 in the southern Yellow Sea in 2012 (Shi et al., unpublished data) which was certainly sufficient for the Ulva prolifera bloom (Liu et al., 2010, 2013). However, the relationship between the increased nutrient levels and the appearance of macroalgal blooms is a complex issue (Raven and Taylor, 2003). Previous work has proved that macroalgal blooms only occurred when other factors, such as temperature, are not limiting even if the nutrient concentrations in water were high enough (Aubert, 1990; Devries et al., 1996; Fletcher, 1996; Taylor et al., 2001; Raven and Taylor, 2003). The optimum temperature range for the growth of Ulva prolifera is from 15 C to 25 C (Wu et al., 2000; Xin et al., 2009). During our cruises, the SST was from 13.6 C on May 6th to 20.9 C on June 4th, which is in the optimum temperature range. Thus, a favorable temperature combined with sufficient nutrient concentration accelerated the growth of Ulva prolifera and facilitated the algal blooms during the drifting period. The average daily specific relative growth rate of green algae along the Rudong coast was approximately 23.2e23.6 % d1 (Zhang et al., 2013). If we calculate the biomass of free-floating algae according to a daily growth rate (DGR) of 23% per day, the total biomass would reach 4.9 104 tons in mid-May (Fig. 4). However, the estimated value is 2.8 times lower than actual value in the in situ survey (1.37 105 tons). Fan et al. (2015) found that Ulva prolifera dominated the Porphyra rafts before the clean-up of the rafts. When P. yezoensis was harvested in May (Shang et al., 2008), the attached macroalgae was dislodged from ropes, rafts and other attachments from late April to late May. This caused the continuous input of U. prolifera into adjacent waters. Thus, the biomass increase of U. prolifera in the first two cruises is attributable not only to the high growth rate but also to continuous input from Porphyra rafts.
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X. Liu et al. / Estuarine, Coastal and Shelf Science 163 (2015) 17e22
Fig. 2. (a~d) The total biomass of free-floating green algae in the southern Yellow Sea.
Meanwhile, we found that the observed biomass was lower than the predicted value on June 5 (Fig. 4). At that time, the input of algal mats from Porphyra rafts had ended, and the growth of U. prolifera declined and entered the stationary phase (Zhang et al., 2013). 4.2. Movement and expansion of green algal patches during drifting period The surface currents imposed by winds were the main driving force that conveyed floating green algae to the adjacent waters of
the Shandong Peninsula (Yi et al., 2010; Qiao et al., 2011; Keesing et al., 2011). Southeasterly winds prevailed in the southern Yellow Sea from May to early June (http://manati.star.nesdis.noaa.gov/ datasets/OSCATData.php).We found northward drifting of algal patches in both cruise observations and RS data, which matched the direction of the wind and was consistent with previous studies (Zhang et al., 2009; Qiao et al., 2011). Meanwhile, the wind velocity in the southern Yellow Sea was up to 4.5 m s1 (http://manati.star. nesdis.noaa.gov/datasets/), which supported the rapid movement of green algal patches.
X. Liu et al. / Estuarine, Coastal and Shelf Science 163 (2015) 17e22
21
Fig. 3. (a~d) The distribution and evolution of green macroalgae in the southern Yellow Sea in the summer of 2012. The area affected by green algae is marked by a black line. These images are edited versions of the false-color satellite images taken from http://kosc.kiost.ac/kosc_web/GOCI_download/SatelliteData. (a: May 6th; b: May 16th; c: May 28th; d: May 31st).
4.3. The importance of cruise observation on the management of green tides The annual occurrence of green tides leads to enormous economic loss in aquaculture and a large expense in cleanup (State Oceanic Administration, China, 2008e2012; Ye et al., 2011). Although RS techniques can predict the drifting path of green patches (Qiao et al., 2009), it cannot predict the biomass of these
floating patches. This inability might limit the application of RS to management of the risks of green tides. The precise biomass data obtained from cruise observation will help decision makers to prepare enough vessels and workers for the cleanup of the algal mats. Meanwhile, an in situ survey could provide basic data for model construction, which will also ‘enable adaptation and strategic planning to organize cleanups and control conditions before a green tide can develop’ (Liu et al., 2013).
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X. Liu et al. / Estuarine, Coastal and Shelf Science 163 (2015) 17e22
References
Fig. 4. Calculated total biomass of free-floating green algae at a DGR of 23% in one month (calculated biomass is the biomass of green algae with a net growth rate of 23%; actual biomass is based on results of the in situ green algal biomass survey).
5. Conclusions From May to June 2012, we observed the blooming process of Ulva prolifera green tides in the southern Yellow Sea. The biomass of floating green algae continuously increased with a stunning speed, from 2.2 103 to 3.64 105 tons in one month, and the affected area expanded dramatically from 2916 to 36,450 km2. The northern border of the green algal patches reached the southern Shandong Peninsula. Combined with RS techniques and cruise observations, estimation of biomass and determination of moving velocity and direction of the algal patches can be determined more precisely. It will help governors take the best measures to provide early warning of green tides and cleanup of algal mats.
Acknowledgements We thank Mr. Mingyuan Zhu and Dr. Dongyan Liu for their valuable comments and thank Dr. Weibing Guan for providing the SST data. We also thank Captain Guohua Zhou and the crew on ‘RUNJIANG-1’ for their assistance in the sample collection. This work was supported by the National Basic Research Program of China (973 Program, 2010CB428703), National Natural Science Foundation of China ‘The ecological mechanism for the origin and early development of massive green tides in the Yellow Sea’ (No. 41276119), MOST International S&T Cooperation Program (No. 2010DFA24340), marine public welfare research special project (No. 201105023-2) and Qingdao public domain to support science and technology project (No. 13-4-1-68-hy).
Aubert, M., 1990. Summer time proliferation of toxic plankton. Recherche 21, 916e919. Devries, I., Philippart, C.J.M., De Groot, E.G., Toll, M.W.M., 1996. Coastal eutrophication and marine benthic vegetation: a model analysis. In: Schramn, W., Neinhuis, P. (Eds.), Ecological Studies, Marine Benthic Vegetation: Recent Changes and the Effects of Eutrophication, vol. 123. Springer-Verlag, Berlin, pp. 79e114. Ding, L.P., Luan, R.X., 2009. The taxonomy, habit, and distribution of a green alga Enteromorpha prolifera (Ulvales, Chlorophyta). Oceanol. Limnol. Sinica 40 (1), 1e4 (in Chinese with English abstract). Fan, S., Fu, M., Li, Y., Wang, Z., Fang, S., Jiang, M., Wang, H., Sun, P., Qu, P., 2012. Origin and development of Huanghai (Yellow) Sea green-tides in 2009 and 2010. Acta Oceanol. Sin. 34 (6), 187e194 (in Chinese with English abstract). Fletcher, R.L., 1996. The occurrence of “Green Tides” e a review. In: Schramm, W., Neinhuis, P. (Eds.), Ecological Studies, Marine Benthic Vegetation, vol. 123. Springer-Verlag, Berlin Heidelberg, pp. 7e43. Keesing, J.K., Liu, D., Fearns, P., Garcia, R., 2011. Inter- and intra-annual patterns of Ulva prolifera green tides in the Yellow Sea during 2007e2009, their origin and relationship to the expansion of coastal seaweed aquaculture in China. Mar. Pollut. Bull. 62, 1169e1182. Liu, D., Keesing, J.K., Xing, Q., Shi, P., 2009. World's largest macroalgal bloom caused by expansion of seaweed aquaculture in China. Mar. Pollut. Bull. 58 (6), 888e895. Liu, D., Keesing, J.K., Dong, Z., Zhen, Y., Di, B., Shi, Y., Fearns, P., Shi, P., 2010. Recurrence of the world's largest green-tide in 2009 in Yellow Sea, China: Porphyra yezoensis aquaculture rafts confirmed as nursery for macroalgal blooms. Mar. Pollut. Bull. 60, 1423e1432. Liu, D., Keesing, J.K., He, P., Wang, Z., Shi, Y., Wang, Y., 2013. The world's largest macroalgal bloom in the Yellow Sea, China: formation and implications. Estuar. Coast. Shelf Sci. 129, 2e10. Qiao, F., Dai, D., Simpson, J., Svendsen, H., 2009. Banded structure of drifting macroalgae. Mar. Pollut. Bull. 58, 1792e1795. Qiao, F., Wang, G., Lü, X., Dai, D., 2011. Drift characteristics of green macroalgae in the Yellow Sea in 2008 and 2010. Chin. Sci. Bull. 56 (21), 2236e2242. Raven, J.A., Taylor, R., 2003. Macroalgal growth in nutrient-enriched estuaries: a biogeochemical and evolutionary perspective. Water, Air, Soil Pollut. 3, 7e26. Shang, Z., Jiang, M., Pu, M., 2008. Analysis of general situations of laver culture in Jiangsu province and its climatic suitability. J. Anhui Agric. Sci. 36, 5315e5319 (in Chinese with English abstract). State Oceanic Administration People’s Republic of China (SOA), 2008e2012. The National Bulletins of Marine Environment Quality Status. SOA Publication, Beijing. Taylor, R., Fletcherb, R.L., Raven, J.A., 2001. Preliminary studies on the growth of selected 'green tide' algae in laboratory culture effects of irradiance, temperature, salinity and nutrients on growth rate. Bot. Mar. 44, 327e336. Wu, H.X., Xu, A.G., Wu, M.N., 2000. Preliminary study on experimental ecology of Enteromorpha prolifera (Miill). J. Zhejiang Ocean Univ. Nat. Sci. 19 (3), 230e234 (in Chinese with English abstract). Xin, D., Ren, S., He, P., Liu, F., Zhang, L., Xu, R., Cheng, X., 2009. Preliminary study on experimental ecology of Enteromorpha in Yellow Sea. Mar. Environ. Sci. 28 (2), 190e192 (in Chinese with English abstract). Ye, N., Zhang, X., Mao, Y., Liang, C., Xu, D., Zou, J., Zhuang, Z., Wang, Q., 2011. “Green tides” are overwhelming the coastline of our blue planet: taking the world's largest example. Ecol. Res. 26, 477e485. Yi, L., Zhang, S., Yin, Y., 2010. Influence of environmental hydro-meteorological conditions to Enteromorpha prolifera blooms in Yellow Sea, 2009. Period. Ocean Univ. China 40 (10), 15e23 (in Chinese with English abstract). Zhang, S., Liu, Y., Zhang, G., et al., 2009. Analysis on the hydro-meteorological conditions from remote sensing data for the 2008 algal blooming in the Yellow Sea. Period. Ocean Univ. China 39 (5), 870e875 (in Chinese with English abstract). Zhang, J.H., Huo, Y.Z., Yu, K.F., Chen, Q.F., He, Q., Han, W., Chen, L.P., Cao, J.C., Shi, D.J., He, P.M., 2013. Gowth characteristics and reproductive capability of green tide algae in Rudong coast, China. J. Appl. Phycol. 25, 795e803. Zhang, Q., Liu, Q., Kang, Z., Yu, R., Yan, T., Zhou, M., 2015. Development of a fluorescence in situ hybridization method for rapid detection of Ulva (Enteromorpha) prolifera. Estuar. Coast. Shelf Sci. 163, 103e111.
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science journal homepage: www.elsevier.com/locate/ecss
Cruise observation of Ulva prolifera bloom in the southern Yellow Sea, China Xiangqing Liu a, b, Yan Li a, b, *, Zongling Wang a, b, Qingchun Zhang c, Xiaoqing Cai a a
The First Institute of Oceanography, State Oceanic Administration, 266061 Qingdao, Shandong, PR China Key Lab of Science and Engineering for Marine Ecological Environment, State Oceanic Administration, 266061 Qingdao, Shandong, PR China c Institute of Oceanology, Chinese Academy of Sciences, 266100 Qingdao, Shandong, PR China b
a r t i c l e i n f o
a b s t r a c t
Article history: Accepted 4 September 2014 Available online 28 September 2014
Four cruises were carried out in the southern Yellow Sea from May to June of 2012 with the aim of observing the development of green tides. Free-floating patches of green algae dominated by Ulva prolifera occurred in early May in coastal waters of the southern Yellow Sea with an average biomass of 0.05 g m2. The average biomass of free-floating green algae developed rapidly and reached 3.20 gm2 in mid-May, and the affected area reached 8.7 103 km2 with a total biomass of 1.37 105 tons. In late May, the average biomass reached 5.81 gm2, and the affected area reached 3.2 104 km2 with a total biomass of 2.5 105 tons. In early June, the average biomass reached 8.47 gm2, the affected area covered 3.6 104 km2, and the total biomass of floating green algae was 3.64 105 tons. The affected areas of green tide in our observed data were higher than those estimated from remote sensing images in the early two cruises, and basically matched the remote sensing data in the last two cruises. With the increased biomass and the expansion of the affected area, the free-floating algal patches moved progressively northward. They first appeared in coastal water of middle Jiangsu province, gradually reached 35 N in early May, and finally drifted to the southern coast of the Shandong Peninsula (36 N) after one month. This work can offer help for the early prediction and warning of a green algal bloom and provide decision-making bases for governmental departments. © 2014 Elsevier Ltd. All rights reserved.
Keywords: Ulva prolifera green tides distribution southern Yellow Sea
1. Introduction Since 2007, green tides have occurred in the southern Yellow Sea from May to July each year and caused serious damage to local tourism, aquaculture and the environment (Liu et al., 2009, 2010; Fan et al., 2012). Previous investigations have indicated that the free-floating green tides in the southern Yellow Sea were from the coastal waters of the Jiangsu province and drifted to the southern coast of the Shandong Peninsula under wind-current action (Zhang et al., 2009; Liu et al., 2009, 2010; Yi et al., 2010; Qiao et al., 2011). The above information, however, mainly came from the satellite observation and numerical modeling. Observations in situ are very limited. Due to the resolution limitation of remote sensing (RS) images, small patches less than 250 m2 cannot be detected using RS
* Corresponding author. The First Institute of Oceanography, State Oceanic Administration, 266061 Qingdao, Shandong, PR China. E-mail addresses: liyan@fio.org.cn, abclxqfi[email protected] (Y. Li). http://dx.doi.org/10.1016/j.ecss.2014.09.014 0272-7714/© 2014 Elsevier Ltd. All rights reserved.
techniques. Thus, RS images might underestimate the movement of algal patches and cannot reflect the actual process of Ulva prolifera bloom development. Thus, cruise observations in situ can compensate for the weaknesses of RS and help to illustrate the entire blooming process. Furthermore, the RS techniques cannot be applied to precisely predict and calculate the green algae biomass because the thickness of floating algal mats varied during the bloom. The varied biomass of green tide every summer made the local government difficult to prepare sufficient salvaging facilities and hire enough workers to clean up, and thus an accurate prediction on green tide biomass is important for management. Observations in situ could provide biomass data for algal mats and help administrators make decisions. Therefore, we conducted four cruises in 2012 to investigate the biomass development and spatial movement of green algal patches in the southern Yellow Sea, China. These studies will help to reveal the blooming process of Ulva prolifera and help governors manage the risks of green tides and take precautions against them.
18
X. Liu et al. / Estuarine, Coastal and Shelf Science 163 (2015) 17e22
The total biomass is calculated as follows:
2. Materials and methods 2.1. Study area and sampling methods
Wt ¼ 120 000 E
2.2. Species identification and biomass measurement Both morphological characteristics (Ding and Luan, 2009) and fluorescence in situ hybridization (Zhang et al., 2015) were used for on-site species identification. Green algal samples were washed with filtered seawater to remove impurities. The biomass Wi (tons) at station i is calculated as follows:
Wi ¼
Gi Si dL
where Gi is the fresh weight of floating green algae (g); d is the inner opening diameter of the WP2 zooplankton net (m); L is the trawling distance (m); and Si is the quadrat area of station i. Si is calculated as a rectangle, with the length and width determined as described in Fig. 1.
Wi
i¼1
122 300 E
The study area covers offshore water from to and from 33 300 N to 35 220 N range in the southern Yellow Sea (Fig. 1), where the largest macroalgal bloom in the world was observed in 2008 (Liu et al., 2009). Four cruises were conducted with 27 stations along five transections A, B, C, D and E from 2nd of May to 6th of June 2012 as listed in Table 1. The first two cruises were carried out during the clean-up of the Porphyra aquaculture raft, and the last two cruises were carried out after clean-up of the raft. We used a horizontal trawl to obtain the biomass of the macroalgal mats. WP2 zooplankton nets (mesh size 0.5 mm, inner opening diameter 0.8 m) were mounted vertical to the vessel, trawling at 3 knots for 10 min. The trawling distance was measured by global position system (GPS) for further calculation of the biomass.
n X
where Wt is the total biomass of the survey area (tons); Wi is the biomass of station i (tons). The total area of affected area is calculated as follows:
St ¼
n X
Si ;
i¼1
where St is the total quadrat area of affected stations; and Si is the quadrat area in station i. The average biomass of free-floating green algae in the survey area (g m2) is calculated as follows:
B¼
Wt ; St
where B is the average biomass of free-floating green algae in the survey area (g m2); Wt is the total biomass of survey area (tons); and St is the total area of affected stations. 2.3. Acquisitions of RS data The formation of the patches of green algae was tracked using 250 m2 resolution ‘‘MODIS” satellite images (http://oceancolor.gsfc. nasa.gov). The affected area of floating green algae is calculated using the Normalized Difference Vegetation Index (NDVI) method, which generates a strong contrast between the floating patches of algae and the turbid waters of the Yellow Sea. The pixels with floating algae had NDVI values between 0.2 and 0.75, while the areas of water around them had NDVI values between 0 and 0.1. A conservative approach by summing the area of the pixels with an NDVI value of greater than 0.24 was taken to calculate the area of the floating patches. The daily sea surface temperature (SST) was
Fig. 1. The sampling sites in the southern Yellow Sea (120 000 E ~ 122 300 E, 33 300 N ~ 35 220 N, a e rectangles with solid line represent the quadrat area of one station, b e the study area).
X. Liu et al. / Estuarine, Coastal and Shelf Science 163 (2015) 17e22
19
Table 1 The biomass, affected area, species composition and proportion of free-floating green algae during four cruises. Cruises
1 2 3 4
Date
2e6 May 14e22 May 25e29 May 31 Maye6 June
Average biomass (g m2)
0.05 3.20 5.81 8.47
Total biomass (tons)
2.20 1.37 2.50 3.64
3
10 105 105 105
Affected area (km2)
5.7 1.4 2.2 2.7
3
10 104 104 104
Species composition and proportion U. prolifera
U. linza
Blidingia sp.
Others
98.3% 98.9% 99.3% 99.4%
1.1% 0.3% e e
0.2% 0.3% 0.1% e
0.4% 0.5% 0.6% 0.6%
(“e” indicates the species was not found). The average biomass is the average biomass of free-floating green algae in survey area (g m2); the total biomass is the total biomass of survey area (tons); the affected area is the total quadrat area of affected stations in situ investigation (km2).
obtained from the towed conductivity-temperature-depth system data. 3. Results
in three days (Figs. 3c, d). The northern border of the green tides moved to 36 N (Fig. 3d). The area affected by remote sensing was consistent with our observations in these two cruises (Table 1, Fig. 2c, d).
3.1. Species composition of free-floating patches
4. Discussion
Floating green algae were composed mainly of Ulva prolifera (>98%), with a few other green algae (e.g., U. linza and Blidingia sp.).
The important finding of our investigation was that we revealed the whole developmental process of the world's largest macroalgal bloom from two aspects. The biomass of green algal patches dominated by Ulva prolifera increased dramatically in just over one month. Meanwhile, the affected area expanded sharply to nearly 36,000 km2 and spread across two provinces in China.
3.2. Temporal variations of green algal biomass The biomass of floating green algae increased rapidly over time during MayeJune 2012 in the southern Yellow Sea as shown in Table 1. In early May, the average biomass of free-floating green algae was 0.05 gm2, and the total biomass was 2.2 103 tons in the studied area. In mid-May, we found that the biomass of freefloating green algae dramatically increased, and the percentage of Ulva prolifera was slightly elevated. The average biomass of freefloating green algae was 3.20 gm2, and the total biomass was 1.37 105 tons, which was 62 times greater than that in early May. In late May, the average biomass of free-floating green algae was 5.81 g m2, and the total biomass was 2.5 105 tons, which was 1.8 times greater than that in mid-May. The percentage of Ulva prolifera continued to increase and was higher than 99% in the algal patches. In early June, the average biomass of free-floating green algae was 8.47 gm2, and the total biomass was 3.64 105 tons, which was 1.5 times greater than that in late May. Ulva prolifera was found at the highest proportion in the green algal patches at 99.4%. 3.3. The development of green tides The observed data in our study (Fig. 2aed) basically matched the RS data (Fig. 3aed). The results demonstrated the whole process of Ulva prolifera bloom development drifting from the south to the north in the Yellow Sea. In early May, algal patches were mainly distributed approximately 33 450 N ~ 34100 N and 120 350 E ~ 120 520 E, and the affected area was 2916 km2 (Fig. 3a). In our cruises, algal patches was found approximately 33 300 N ~ 35 N and 120 300 E ~ 121300 E (Fig. 2a). Thus, the affected area based on our observation was higher than that estimated from RS images and reached 5700 km2 as shown in Table 1. In mid-May, RS data showed that the patches began to move north, and the affected area increased to 8748 km2 (Fig. 3b). An identical trend was found during our cruises (Fig. 2b). As with the previous cruises, we observed a considerable amount of green algal patches approximately 33 300 N ~ 35 200 N and 120 E ~ 121300 E in the cruises, and the actual affected area of algal patches was 14,000 km2 (Table 1). In the last two cruises, the algal patches continuously expanded, and the affected area increased rapidly from 32,076 to 36,450 km2
4.1. Rapid increase in green algal biomass The biomass of floating green algae increased 165 times from 2nd May to 6th June 2012 (Table 1). The question of why the rapid growth of Ulva prolifera was triggered during this period should be asked. In essence, Ulva prolifera is the predominant green tide species, with high rates of nutrient uptake (Raven and Taylor, 2003). During the blooming period, the dissolved inorganic nitrogen (DIN) concentrations was 7.84e13.53 mmolL1 in the southern Yellow Sea in 2012 (Shi et al., unpublished data) which was certainly sufficient for the Ulva prolifera bloom (Liu et al., 2010, 2013). However, the relationship between the increased nutrient levels and the appearance of macroalgal blooms is a complex issue (Raven and Taylor, 2003). Previous work has proved that macroalgal blooms only occurred when other factors, such as temperature, are not limiting even if the nutrient concentrations in water were high enough (Aubert, 1990; Devries et al., 1996; Fletcher, 1996; Taylor et al., 2001; Raven and Taylor, 2003). The optimum temperature range for the growth of Ulva prolifera is from 15 C to 25 C (Wu et al., 2000; Xin et al., 2009). During our cruises, the SST was from 13.6 C on May 6th to 20.9 C on June 4th, which is in the optimum temperature range. Thus, a favorable temperature combined with sufficient nutrient concentration accelerated the growth of Ulva prolifera and facilitated the algal blooms during the drifting period. The average daily specific relative growth rate of green algae along the Rudong coast was approximately 23.2e23.6 % d1 (Zhang et al., 2013). If we calculate the biomass of free-floating algae according to a daily growth rate (DGR) of 23% per day, the total biomass would reach 4.9 104 tons in mid-May (Fig. 4). However, the estimated value is 2.8 times lower than actual value in the in situ survey (1.37 105 tons). Fan et al. (2015) found that Ulva prolifera dominated the Porphyra rafts before the clean-up of the rafts. When P. yezoensis was harvested in May (Shang et al., 2008), the attached macroalgae was dislodged from ropes, rafts and other attachments from late April to late May. This caused the continuous input of U. prolifera into adjacent waters. Thus, the biomass increase of U. prolifera in the first two cruises is attributable not only to the high growth rate but also to continuous input from Porphyra rafts.
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Fig. 2. (a~d) The total biomass of free-floating green algae in the southern Yellow Sea.
Meanwhile, we found that the observed biomass was lower than the predicted value on June 5 (Fig. 4). At that time, the input of algal mats from Porphyra rafts had ended, and the growth of U. prolifera declined and entered the stationary phase (Zhang et al., 2013). 4.2. Movement and expansion of green algal patches during drifting period The surface currents imposed by winds were the main driving force that conveyed floating green algae to the adjacent waters of
the Shandong Peninsula (Yi et al., 2010; Qiao et al., 2011; Keesing et al., 2011). Southeasterly winds prevailed in the southern Yellow Sea from May to early June (http://manati.star.nesdis.noaa.gov/ datasets/OSCATData.php).We found northward drifting of algal patches in both cruise observations and RS data, which matched the direction of the wind and was consistent with previous studies (Zhang et al., 2009; Qiao et al., 2011). Meanwhile, the wind velocity in the southern Yellow Sea was up to 4.5 m s1 (http://manati.star. nesdis.noaa.gov/datasets/), which supported the rapid movement of green algal patches.
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Fig. 3. (a~d) The distribution and evolution of green macroalgae in the southern Yellow Sea in the summer of 2012. The area affected by green algae is marked by a black line. These images are edited versions of the false-color satellite images taken from http://kosc.kiost.ac/kosc_web/GOCI_download/SatelliteData. (a: May 6th; b: May 16th; c: May 28th; d: May 31st).
4.3. The importance of cruise observation on the management of green tides The annual occurrence of green tides leads to enormous economic loss in aquaculture and a large expense in cleanup (State Oceanic Administration, China, 2008e2012; Ye et al., 2011). Although RS techniques can predict the drifting path of green patches (Qiao et al., 2009), it cannot predict the biomass of these
floating patches. This inability might limit the application of RS to management of the risks of green tides. The precise biomass data obtained from cruise observation will help decision makers to prepare enough vessels and workers for the cleanup of the algal mats. Meanwhile, an in situ survey could provide basic data for model construction, which will also ‘enable adaptation and strategic planning to organize cleanups and control conditions before a green tide can develop’ (Liu et al., 2013).
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References
Fig. 4. Calculated total biomass of free-floating green algae at a DGR of 23% in one month (calculated biomass is the biomass of green algae with a net growth rate of 23%; actual biomass is based on results of the in situ green algal biomass survey).
5. Conclusions From May to June 2012, we observed the blooming process of Ulva prolifera green tides in the southern Yellow Sea. The biomass of floating green algae continuously increased with a stunning speed, from 2.2 103 to 3.64 105 tons in one month, and the affected area expanded dramatically from 2916 to 36,450 km2. The northern border of the green algal patches reached the southern Shandong Peninsula. Combined with RS techniques and cruise observations, estimation of biomass and determination of moving velocity and direction of the algal patches can be determined more precisely. It will help governors take the best measures to provide early warning of green tides and cleanup of algal mats.
Acknowledgements We thank Mr. Mingyuan Zhu and Dr. Dongyan Liu for their valuable comments and thank Dr. Weibing Guan for providing the SST data. We also thank Captain Guohua Zhou and the crew on ‘RUNJIANG-1’ for their assistance in the sample collection. This work was supported by the National Basic Research Program of China (973 Program, 2010CB428703), National Natural Science Foundation of China ‘The ecological mechanism for the origin and early development of massive green tides in the Yellow Sea’ (No. 41276119), MOST International S&T Cooperation Program (No. 2010DFA24340), marine public welfare research special project (No. 201105023-2) and Qingdao public domain to support science and technology project (No. 13-4-1-68-hy).
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