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Emergence of Brown Tides Caused by Aureococcus Anophagefferens Hargraves Et

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Emergence of Brown Tides Caused by Aureococcus Anophagefferens Hargraves Et Harmful Algae 19 (2012) 117–124 Contents lists available at SciVerse ScienceDirect Harmful Algae jo urnal homepage: www.elsevier.com/locate/hal Emergence of brown tides caused by Aureococcus anophagefferens Hargraves et Sieburth in China a b,1 a, a a Qing-Chun Zhang , Li-Mei Qiu , Ren-Cheng Yu *, Fan-Zhou Kong , Yun-Feng Wang , a c a Tian Yan , Christopher J. Gobler , Ming-Jiang Zhou a Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China b Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China c School of Marine and Atmospheric Sciences, Stony Brook University, New York, United States A R T I C L E I N F O A B S T R A C T Article history: Large-scale blooms suspected to be ‘‘brown tides’’ occurred in early summer for three consecutive years Received 24 March 2012 from 2009 to 2011 in the coastal waters of Qinhuangdao, China, and had significant negative impacts on Received in revised form 20 June 2012 the shellfish mariculture industry. To identify the causative species of the blooms, phytoplankton Accepted 20 June 2012 samples were collected from regions with and without bloom in the coastal waters of Qinhuangdao in Available online 28 June 2012 2011, and clone libraries were built using eukaryote-specific 18S ribosomal RNA gene (18S rDNA). Altogether 50 clones, including 17 clones from bloom area and 33 clones from nearby regions without Keywords: bloom were amplified. Blasted in GenBank, 17 clones amplified from the bloom area were assigned to Aureococcus anophagefferens Pelagophyceae (8 clones), Mediophyceae (2 clones), Cryptophyta (2 clones), Dinophyceae (2 clones) and Brown tide unidentified eukaryotic species (3 clones). Those from the non-bloom site were assigned to Cryptophyta, Harmful algal bloom Mariculture Eustigmatophyceae, Prasinophyceae, Coscinodiscophyceae, Mediophyceae, Raphidophyceae and 18S rDNA Dinophyceae, but not Pelagophyceae. All 8 pelagophyte clones from the bloom area were 99.7–100% similar to a single species, Aureococcus anophagefferens Hargraves et Sieburth, the causative species of brown tides on the east coast of USA. For nearly the entire length of the 18S rDNA, there were 0–6 base pair differences between the 8 amplicons and those of A. anophagefferens from USA. Furthermore, all of the 8 clones were clustered into the same well-supported clade with A. anophagefferens (posterior probability = 0.99) in a phylogenetic tree established for pelagophytes and other related microalgae. In our previous studies, the causative species of the bloom was tentatively identified as a pelagophyte, haptophyte or silicoflagellate, based on the pigment profile of the size-fractioned phytoplankton samples. Based on this study, we conclude that blooms in the coastal waters of Qinhuangdao of the Bohai Sea were brown tides caused by A. anophagefferens. As far as we know, this is the first report of brown tide events caused by A. anophagefferens in China, which is the third country in the world reporting A. anophagefferens blooms in addition to USA and South Africa. ß 2012 Elsevier B.V. All rights reserved. 1. Introduction HAB events were recorded in many areas where blooms had not occurred previously. Since the beginning of the 21st century, large- Over the last several decades, harmful algal blooms (HABs) have scale blooms of dinoflagellates began to appear in the area adjacent shown an apparent expansion in frequency, intensity and impacts to the Changjiang River estuary in the East China Sea, and the globally, due to the wide dispersal of HAB species, increased causative species was identified as Prorocentrum donghaiense aquaculture operations, intensified cultural eutrophication, and (Zhou and Zhu, 2006). From 2007 until the present, recurrent large- improved capability in detecting HABs (Anderson et al., 2012). A scale blooms of the green macroalgae, Ulva prolifera, which were similar trend was observed in the coastal waters of China, and new termed as ‘‘green tides’’ occurred in the Yellow Sea and led to large economic loses along the coast of Shangdong province and Jiangsu province. Recently, a new type of HAB event was found in the coastal waters near Qinhuangdao in the Bohai Sea, and posed * Corresponding author at: Institute of Oceanology, Chinese Academy of Sciences, significant impacts on the local shellfish mariculture industry. 7 Nanhai Road, Qingdao 266071, China. Tel.: +86 532 82898590; These blooms in the Bohai Sea were formed by a tiny microalgal fax: +86 532 82898590. E-mail address: [email protected] (R.-C. Yu). species (cell size 2 mm), and occurred for at least three 1 Equal contribution to this manuscript as the first author. consecutive years from 2009 to 2011. The blooms, which 1568-9883/$ – see front matter ß 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.hal.2012.06.007 118 Q.-C. Zhang et al. / Harmful Algae 19 (2012) 117–124 discolored waters into a dark brown color with maximum cell revealed. In constructing clone libraries, 18S ribosomal RNA gene 9 À1 density around 10 cells l , initiated during late May, and (18S rDNA) has been frequently employed as a phylogenetic sustained through late June or early July. During the blooms, marker for eukaryotes due to the large number of available significant negative effects were observed on feeding activities and sequences for comparison. During many brown tides in USA, the growth of shellfish cultivated in this region, particularly bay causative species numerically dominate the eukaryotic phyto- scallop Argopecten irradians. During the bloom in 2009, about two plankton communities (Gobler and Sunda, 2012). As such, thirds of the mariculture zone (26,000 ha) was affected by the amplicons of the bloom causative species should dominate the 2 bloom. In 2010, the bloom-affected sea area reached 3350 km , 18S rDNA clone libraries established from phytoplankton samples and led to an economic loss of 0.2 billion RMB (Bulletin of Marine collected during brown tides. In the current study, samples were Disaster, 2010; Bulletin of Marine Environmental Quality, 2010). collected from regions with and without brown tides in the Bohai Large-scale blooms occurred again in 2011, although the impacts Sea near Qinhuangdao in 2011, and clone libraries of 18S rDNA of this bloom are currently unknown. In a previous study (Kong were established to identify the causative species. et al., 2012), we reported that the major pigments detected from 0 the bloom were 19 -butanoyloxyfucoxanthin (But-fuco), fucoxan- 2. Materials and methods thin (Fuco), diadinoxanthin (Diad) and Chlorophyll a (Chl a), and high content of But-fuco was the most significant characteristics of 2.1. Background of the sampling sites the causative species of the bloom. Based on the pigment composition and content, the causative species could be tentative- Phytoplankton samples were collected from the coastal water ly identified as a pelagophyte, haptophyte or silicoflagellate of Qinhuangdao in the Bohai Sea on June 22nd, 2011 (Fig. 1). 0 0 (Edvardsen et al., 2007; Zapata et al., 2004). Other features of Station Q1 (119826.578 E, 39845.500 N) was located in a region the blooms in the coastal waters of Qinhuangdao, including the that had experienced brown tides in 2009 and 2010 and was discoloration of water and the small size of cells (2 mm), experiencing a brown tide on that date. The water depth at station suggested that the blooms in this region were ‘‘brown tides’’ Q1 was about 8 m. Water temperature was 21.0 8C, and salinity similar to those reported in USA. In Maryland, USA, But-fuco was was 31. Dissolved inorganic nitrogen (DIN) concentration was considered evidence for the presence of brown tides caused by 10.36 mM, and phosphate concentration was 0.11 mM. Phyto- Aureococcus anophagefferens Hargraves et Sieburth in the early plankton samples collected from station Q1 were mainly 1990s in the Chincoteague Bay, and the content of But-fuco has composed of small solitary and spherical cells golden in color, been successfully used to estimate historical cell densities of A. which were about 2 mm in diameter. The cell density was about 9 À1 anophagefferens (Trice et al., 2004). However, it is impossible to 1 Â 10 cells l , occupying the large majority of phytoplankton positively identify the causative species of the brown tides in the cells. Besides, dinoflagellates dominated by Gyrodinium spirale and Bohai Sea without any further evidence. diatoms dominated by Navicula sp. were also presented at low Clone libraries have been frequently used to analyze species levels. Chl a content of the bulk phytoplankton sample was À1 À1 composition of environmental samples (Lo´ pez-Garcı´a et al., 2001; 10.59 mg l at the surface and 19.56 mg l at the bottom. Pico- Moon-van der Staay et al., 2001). Through sequencing the PCR sized Chl a (<2 mm) was about 80% of the total Chl a content, and amplicons of environmental samples, species composition can be nano-sized Chl a (2–20 mm) was about 20%, while micro-sized Chl Fig. 1. Illustration of the sampling stations and bloom area in the coastal waters of Qinhuangdao. Q.-C. Zhang et al. / Harmful Algae 19 (2012) 117–124 119 a (>20 mm) was less than 1%. But-fuco, Fuco, Diad and Chl a were the GenBank (http://www.ncbi.nlm.nih.gov/), with the Accession the major pigment components in the pico-sized and nano-sized Number from JQ420077 to JQ420126 (Table 1). phytoplankton samples (Kong et al., 2012). Station Q3 0 0 (119824.660 E, 39846.924 N), which was outside the bloom area, 3. Results was located at the Yanghekou Harbor and approximately 4 km away from stations Q1 (Kong et al., 2012).
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