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The contribution of attached Ulva prolifera on Pyropia aquaculture rafts to green tides in the Yellow Sea
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Hongbin Han1, 2, Shiliang Fan1, Wei Song1, Yan Li1, 3, Jie Xiao1, Zongling Wang1, 2, 3, *, Xuelei Zhang1, 3, Dewen Ding1, 2
Acta Oceanologica Sinica | 2020, 39(2) : 101 - 106
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Acta Oceanologica Sinica | 2020, 39(2): 101-106
• Marine Biology •
The contribution of attached Ulva prolifera on Pyropia aquaculture rafts to green tides in the Yellow Sea
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Hongbin Han1, 2, Shiliang Fan1, Wei Song1, Yan Li1, 3, Jie Xiao1, Zongling Wang1, 2, 3, *, Xuelei Zhang1, 3, Dewen Ding1, 2
Affiliations
  • 1 Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
  • 2 College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China
  • 3 Laboratory of Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
Published: 2020-02-25 doi: 10.1007/s13131-019-1452-0
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Green tides caused by the unusual accumulation of high floating Ulva prolifera have occurred regularly in the Yellow Sea since 2007. The primary source of the Yellow Sea green tides is the attached algae on the Pyropia aquaculture rafts in the Subei Shoal. Ulva prolifera and Blidingia (Italic) sp. are the main species observed on Pyropia aquaculture rafts in the Subei Shoal. We found that U. prolifera has strong buoyancy and a rapid growth rate, which may explain why it is the dominant species of green tides that occur in the China's sea area of the Yellow Sea. The growth rate of floating U. prolifera was about 20%–31% d–1, which was much higher than Blidingia (Italic) sp. There were about 1.7 × 104 t of attached algae on the Pyropia aquaculture rafts in May 2012. We found that 39% of attached algae could float when the tide rose in the Subei Shoal, and U. prolifera accounted for 63% of the floating algae. Our analysis estimated that about 4 000 t of attached U. prolifera floated into the surrounding waters of the Subei Shoal during the recycling period of aquaculture rafts. These results suggest that the initial floating biomass of large-scale green tides in the Yellow Sea is determined by the U. prolifera biomass attached to Pyropia aquaculture rafts, further impacting the scale of the green tide.

attached algae  /  Pyropia aquaculture rafts  /  Blidingia (Italic) sp.  /  Ulva prolifera  /  green tides
Hongbin Han, Shiliang Fan, Wei Song, Yan Li, Jie Xiao, Zongling Wang, Xuelei Zhang, Dewen Ding. The contribution of attached Ulva prolifera on Pyropia aquaculture rafts to green tides in the Yellow Sea[J]. Acta Oceanologica Sinica, 2020 , 39 (2) : 101 -106 . DOI: 10.1007/s13131-019-1452-0
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1 Introduction
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Since 2007, large-scale green tides have occurred consecutively in the China's sea area of the Yellow Sea, damaging the coastal ecology, aquaculture industry, and tourism for coastal cities in Jiangsu Province and Shandong Province (Gao et al., 2010; Wang et al., 2010; Han et al., 2013). As a consequence, green tides have become a major concern for government officials and scientists in China (Liu et al., 2009). Ulva prolifera has been identified as the dominant species of green tides in the Yellow Sea (Wang et al., 2008; Liu et al., 2010b; Zhao et al., 2013; Xiao et al., 2013), and numerous hypotheses have been proposed to explain the origin of green tides in the Yellow Sea. Hu et al. (2010) used MODIS and Landsat satellites to detect patches of floating green tides from 2000 to 2009, and concluded that green tide formation started in the southern areas of the Yellow Sea. Pang et al. (2010) argued that the micro-propagules in animal aquaculture ponds along the Jiangsu coastline were the source of the green tides. Zhang et al. (2010, 2011) suggested that U. prolifera vegetative fragments and somatic cells may serve as the source of propagules of the green tide. However, other scientists have suggested that large-scale green tides in the Yellow Sea originate from algae that are cleaned from Pyropia aquaculture rafts in the Subei Shoal (Liu et al., 2009; Hu et al., 2010; Keesing et al., 2011; Zhang et al., 2014), and this theory is now accepted widely. According to previous studies, there are many attached algae attached algae species name on Pyropia aquaculture rafts, including Blidingia (Italic) sp., U. prolifera, U. linza, U. compressa, U. intestinalis and U. clathrata (Fan et al., 2015).
Despite this, the following questions remain unanswered: (1) How much does attached algae on Pyropia aquaculture rafts contribute to green tides in the Yellow Sea? (2) What happens as the attached algae on the rafts begins to float? (3) What properties of U. prolifera cause large-scale green tides, when there are many other Ulva species on the Pyropia aquaculture rafts? To address these questions, we selected three major Pyropia aquaculture areas in the Subei Shoal to calculate the biomass and species composition of algae on Pyropia aquaculture rafts in May 2012. In addition, we conducted field experiments to test the species composition of floating algae and the growth rates of floating U. prolifera and Blidingia (Italic) sp.
2 Materials and methods
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2.1 Sampling locations
Based on the distribution of Pyropia aquaculture area in the Subei Shoal, three sites were selected to sample attached algae in May 2012 (Fig. 1). These sites included Xiaoyangkou (32.68°N, 121.09°E), Gaoni (32.81°N, 121.22°E), and Niluosha (33.22°N, 121.17°E), and samples were collected when the biomass of attached Ulva species on the rafts reached the highest levels. Six rafts were randomly selected in each sampling area. Six replicate samples of green algae attached to a 30 cm long rope were collected at 10 m intervals from the ropes of each raft. A total of 36 samples were obtained at each site. The green algae samples were preserved at a low temperature of about 5°C, and transported back to the laboratory within 72 h.
2.2 Species identification, separation, and biomass measurement
Macroalgae samples were rinsed three times with sterile seawater to remove sediment, debris, and epiphytes. The green macroalgal species were identified based on the shape, branching, cell arrangement, and location of pyrenoids and chloroplasts (Tseng, 1983; Blomster et al., 1998; Ding et al., 2008; Kraft et al., 2010; Duan et al., 2012). Samples were carefully examined under the microscope using light microscopy using an Olympus CX310 microscope (KS Olympus, Tokyo, Japan). The macroalgae were dried with blotting paper and weighed using a high-accuracy electronic balance (PL203, METTLER TOLEDO Inc., Zurich, CH). The total wet weight of each sample was calculated by the sum of the biomass of all individual species (Fan et al., 2015).
2.3 Floating experiment of attached algae on Pyropia aquaculture rafts
Green algae samples described in Section 2.1 were dispersed in an acrylic glass tank (30 cm long × 30 cm wide × 70 cm high, in triplicate), and observed after 1 h of exposure to natural sunlight. The algae mats that floated on the water surface, suspended in the middle of the water column, and sank to the bottom of the tank were categorized as “floating”, “suspension” and “sinking”, respectively. Green algae in different stages were collected and dried with blotting paper, and then weighed as described above. The species composition of floating algae was measured at 1 h, 24 h, 48 h and 72 h using species identification methods described above.
2.4 Growth experiment for U. prolifera and Blidingia (Italic) sp.
Ulva prolifera and Blidingia (Italic) sp. were the main species found on Pyropia rafts in the Subei Shoal. The floating algae that were collected in the experiment described in Section 2.3 were identified as U. prolifera and Blidingia (Italic) sp. and different species samples separately placed in 25 L bucket (in triplicate) on shipboard for 5 d. There were three buckets were used for Blidingia (Italic) sp. and three buckets for U. prolifera.The seawater used for culturing was refreshed at 12:00 every day. A RBR water quality analyzer was used to measure the temperature and salinity of the seawater, and measurements were taken at 6:00, 12:00 and 18:00 every day. The daily temperature and salinity of the bucket were determined by obtaining the average across the three time points for each day. The error bars represent the variability between the three buckets.
Specific growth rate (SGR, %/d) of algae was calculated using the following formula (Metaxa et al., 2006):
${\rm{SGR}} = 100\left( {{\rm{ ln}}{W_t}-{\rm{ ln}}{W_0}} \right)/t,$
where W0 is the initial wet weight (g) of the floating algae, Wt is the wet weight (g) of the floating algae on day t, and t is the culture time (d).
2.5 Statistics
Datasets were analyzed by a two-way analysis of variance (ANOVA). The difference between means was analyzed by Duncan’s new multiple range test followed by an ANOVA and P<0.05 was considered to be significant. Statistical analyses were performed using the SPSS 17.0 statistical program (SPSS Inc., Chicago, USA).
3 Results
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3.1 The species composition and biomass of attached algae on the rafts in May 2012
We collected green macroalgal species from Pyropia aquaculture rafts during May 2012, and detected the presence of Blidingia (Italic) sp., U. prolifera, U. compressa, U. intestinalis and U. clathrata. Among them, Blidingia (Italic) sp. and Ulva prolifera were the main macroalgal species on the Pyropia aquaculture rafts. Ulva compressa, U. intestinalis and U. clathrata had low biomass and were only detected in some sampling sites. Given their low prevalence, we combined the results for these three species and refer to these samples as Ulva spp. The attached total algae biomass at Xiaoyangkou, Gaoni and Niluosha were 214.2, 153.4 and 53.0 g/m, respectively (Fig. 2).
3.2 Morphology of U. prolifera and Blidingia (Italic) sp.
Ulva prolifera attached to the rafts were light green with multiple slender branchlets on the boughs. The diameter of the side branch was smaller than the chief branch, and chief branch was hollow and tubular (Figs 3a and b). There was a small gap between the two cells of the green algae with a flat air sac (Fig. 3c). Blidingia (Italic) sp. attached to the rafts were dark green with thin tubular, unbranched, and single layered cells (Figs 3d and e). Blidingia (Italic) sp. were small and closely arranged (Fig. 3f).
3.3 The state of attached algae and species composition of floating algae
We placed algae from the Pyropia aquaculture rafts in a tank and found that 39% of the algae floated on the water surface after 1 h of being dispersed (Fig. 4). Ulva prolifera accounted for about 63% of the floating algae and the percentage gradually increased and reached 91.3% after 24 h. The proportion of U. prolifera accounted for floating algae was greater than 98% after 72 h (Fig. 5).
3.4 The SGR of U. prolifera and Blidingia (Italic) sp.
The SGR of U. prolifera ranged from 20%–31% d–1 during the test period, and this was much higher than Blidingia (Italic) sp., which ranged from 1.7%–3.4% d–1 (Fig. 6). Taken together, the SGR of U. prolifera was about 15 times greater than Blidingia (Italic) sp. The average daily seawater temperatures ranged from 20.5 to 23.5°C, and the average salinity varied over time (P>0.05) with values ranging from 30.5 to 30.9, which was not a dramatic change (Fig. 7).
4 Discussion
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The Pyropia rafts usually begin to be collected in April. The culture nets will be transported back for the Pyropia crops, while the connecting ropes and bamboo poles will be cleaned in situ before they are moved back for next year’s construction. And the harvesting starts from near-shore region and progresses to the east. The cleaning process usually takes for about one month, from the mid-April to mid-May (Wang et al., 2015; Huo et al., 2015). So, there are still quite a few Pyropia rafts left on the Subei Shoal in May, especially at the east edge of Subei Shoal. As indicated by the detailed description of macroalgal assemblage on the rafts, there were large amount of Ulva on the rafts and could reach the highest in May after rapid growing of the attached algae with favorable temperature (Fan et al., 2015; Liu et al., 2016). So we collected the samples in May, when the green tide began to form. Our results showed that U. prolifera and Blidingia (Italic) sp. were the dominant species on Pyropia aquaculture rafts during the harvesting season in Subei Shoal. We found that U. prolifera accounted for 63% of the floating algae when algae samples from rafts were placed in a tank for 1 h. Ulva prolifera represented 91.3% of the floating algae by 24 h of culturing samples in a tank. In constrast, our field investigations found that U. prolifera represented more than 95% of the floating algae in the Subei Shoal (Song, 2014). The percentage of U. prolifera continued to increase as macroalgae drifted offshore, reaching 99% or higher in the algal patches of the central Yellow Sea (Liu et al., 2016). The ocean waves may stir and scatter U. prolifera and Blidingia (Italic) sp., which are initially mixed together, and this may underlie the difference we observed between the field and simulation experiments. Therefore, the percentage of U. prolifera in the field was higher over a short period of time. The resulted showed tha buoyancy capacity of U. prolifera was higher than other attached algae on Pyropia aquaculture rafts, which may be one of the reasons it has become the dominant species in the green tides of the Yellow Sea.
The growth of U. prolifera is controlled by many environmental factors (Agrawal, 2009). Wang et al. (2007) found that 20–25°C was the appropriate temperature range for U. prolifera and Cui et al. (2015) showed that the growth rate of U. prolifera was higher than other floating algae at 20°C. The average daily SGR of green algae along the Rudong coast is approximately 23.2%–26.3% (Zhang et al., 2013). In our experimental conditions, the daily temperature was between 20.5°C and 23.5°C with salinity of around 30, which match with conditions that are optimal for U. prolifera growth. The daily SGR in our tank experiments was 20%–31% every day for U. prolifera, which was much higher than Blidingia (Italic) sp. the other dominnat algae species found on the Pyropia aquaculture rafts. In our study, the ambient seawater was used for culturing and refreshed every day. So the nutrients concentrations in the culturing water should be similar to the ambient seawater. With the substantial nutrient inputs from the rivers surrounded, e.g., Changjiang (Yangtze) River, Sheyang River and Guan River, high nutrients were generally found in the Subei Shoal over the past decades (Keesing et al., 2011). It was almost certainly sufficient for the U. prolifera blooms (Liu et al., 2013; Zhou et al., 2015). Similarly, the culture experiment was performed on the shipboard under the nature light. The light intensity of the sea surface was below 30 μmol/(m2·s) on the rainy days, 30–300 mol/(m2·s) on cloudy days, and generally above 300 μmol/(m2·s) on sunny days (Cui et al., 2015). Cui et al. (2015) noted that U. prolifera has better tolerance to high temperature and light intensity than the other three species. Our algae culture experiment are on the sunny days and the growth rate of U. prolifera were higher than the Blidingia (Italic) sp.
We observed an increase in the percentage of U. prolifera among the floating algae over time, and a concurrent decrease in the presence of other algae. The rapid growth rate of U. prolifera is an important reason why this species has become the dominant species of green tide in the Yellow Sea (Zhang et al., 2014; Cui et al., 2015). In our experiment, when the attached algae began to float, U. prolifera quickly became the dominant species due to its buoyancy and rapid growth rate. The other green algae could not compete with U. prolifera, and U. prolifera became the dominant species within two days. Under the influence of the southeast monsoon, U. prolifera can float northward and reach the sea area of Qingdao (Keesing et al., 2011).
Blidingia (Italic) sp. was a high percentage of the attached algae on Pyropia aquaculture rafts in May 2012. However, the species of algal micro-propagules in Subei Shoal mainly consisted of the genus Ulva, and there were only low amounts of Blidingia (Italic) sp. micro-propagules (Song et al., 2015). Therefore, we hypothesized that attached Ulva and Blidingia (Italic) sp. had different growth modes. We observed regularly arranged oval or long cylindrical germ cell cytocysts of U. prolifera under the microscope, where germ cells were clearly seen in the germ cell cytocysts (Fig. 3c). However, Blidingia (Italic) sp. were shaped differently and appeared transparent and closely arranged under the microscope. Interestingly, these Blidingia (Italic) sp. cells did not contain germ cell cytocysts (Fig. 3f). Therefore, we hypothesized that attached U. prolifera and Blidingia (Italic) sp. may mainly depend on reproductive and vegetative growth modes, respectively.
Green macroalgae are scraped and thrown away by farmers in Subei Shoal during the Pyropia harvesting season in May (Liu et al., 2010a, 2016; Zhang et al., 2014; Wang et al., 2015). In our study, 39% of the attached algae floated after 1 h and over 98% of the floating algae were U. prolifera after 72 h of culture. We suspect that the changes in the floating state of U. prolifera may affect its growth pattern. Li et al. (2014) observed morphological differences between attached and floating U. prolifera, where floating U. prolifera has significantly more branching than attached U. prolifera. Lin et al. (2008) found that the reproductive cells of floating U. prolifera contained unreleased micro-propagules that could germinate and grow directly to create more branches. Lin et al. (2008) also found that U. prolifera relies on vegetative growth when it is in a floating state. Ye et al. (2008) suggested that U. prolifera could rapidly grow through the asexual propagation of somatic cells during floating. Zhang et al. (2016) observed four different growth and reproductive strategies of floating U. prolifera, including: (1) tubular diameter becoming larger, (2) formation of new branches, (3) release of zoids, and (4) polarized growth. The diversified reproduction strategies of U. prolifera may also underlie its dominance during green tide events at the Yellow Sea.
The algae attached to Pyropia aquaculture rafts are considered to be the origin of the green tides in the Yellow Sea (Liu et al., 2009, 2010a; Keesing et al., 2011; Huo et al., 2015; Zhang et al., 2014). Farmers begin to recycle aquaculture rafts in May and when the macroalgae are scraped off, the attached algae begin to float to form initial green tides in Subei Shoal as the tide rises (Liu et al., 2010a; Huo et al., 2015). Then, the initial green tides drifts offshore, resulting in the rapid increase in floating biomass and the formation of large-scale green tides in the Yellow Sea (Liu et al., 2010a, 2013). Our study quantitatively analyzed the contribution of attached algae to green tides in the Yellow Sea. Based on our data and the total Pyropia aquaculture area (3.8×104 hm2) in the Subei Shoal (Shang et al., 2008), we estimated the raft-fouling biomass of the green macroalgae to be about 1.70×104 t in May 2012. Our results showed that 39% of the attached algae could float and U. prolifera accounted for 63% after 1 h. Taken together, about 4 000 t U. prolifera may have began floating once the rafts were harvested in May. In the floating process, U. prolifera experienced a rapid growth rate of 20%-31%, and after 30 d of floating, U. prolifera likely reached 237 times of the initial biomass based on a daily growth rate of 20% (Fig. 8). This is enough to form a large-scale green tide of one million tons in the Yellow Sea by the end of June. Taken together, our findings highlight that the biomass of U. prolifera attached on Pyropia aquaculture rafts can affect the scale of green tide in the Yellow Sea.
Funding
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  • The National Key R&D Program of China under contract Nos 2016YFC1402104 and 2016YFC1402106; the National Natural Science Foundation of China under contract No. 41606190; the Shandong Natural Science Foundation under contract No. ZR2016DB22; the Foundation of Key Laboratory of Integrated Monitoring and Applied Technologies for Marine Harmful Algal Blooms, SOA under contract No. MATHAB 201806; the Creative Team Project of the Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology under contract No. LMEES-CTSP-2018-3.
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Article Info
doi: 10.1007/s13131-019-1452-0
  • Receive Date：2018-11-16
  • Online Date：2026-03-31
  • Published：2020-02-25
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  • Received：2018-11-16
  • Accepted：2019-01-21
Funding
The National Key R&D Program of China under contract Nos 2016YFC1402104 and 2016YFC1402106; the National Natural Science Foundation of China under contract No. 41606190; the Shandong Natural Science Foundation under contract No. ZR2016DB22; the Foundation of Key Laboratory of Integrated Monitoring and Applied Technologies for Marine Harmful Algal Blooms, SOA under contract No. MATHAB 201806; the Creative Team Project of the Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology under contract No. LMEES-CTSP-2018-3.
Affiliations
    1 Key Laboratory of Marine Eco-Environmental Science and Technology, First Institute of Oceanography, Ministry of Natural Resources, Qingdao 266061, China
    2 College of Environmental Science and Engineering, Ocean University of China, Qingdao 266100, China
    3 Laboratory of Marine Ecology and Environmental Science, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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