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Giantism and Its Role in the Harmful Algal Bloom Species Phaeocystis Globosa

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Giantism and Its Role in the Harmful Algal Bloom Species Phaeocystis Globosa Deep-Sea Research II ] (]]]]) ]]]–]]] Contents lists available at SciVerse ScienceDirect Deep-Sea Research II journal homepage: www.elsevier.com/locate/dsr2 Giantism and its role in the harmful algal bloom species Phaeocystis globosa Walker O. Smith Jr.a,n, Xiao Liu a,1, Kam W. Tang a, Liza M. DeLizo a, Nhu Hai Doan b, Ngoc Lam Nguyen b, Xiaodong Wang c a Virginia Institute of Marine Science, College of William & Mary, Gloucester Pt., VA 23062, United States b Institute of Oceanography, Vietnam Academy of Science & Technology, 01 Cau Da, Nha Trang, Viet Nam c Research Center for Harmful Algae and Aquatic Environment, Jinan University, Guangzhou, China article info abstract The cosmopolitan alga Phaeocystis globosa forms large blooms in shallow coastal waters off the Viet Keywords: Nam coast, which impacts the local aquaculture and fishing industries substantially. The unusual Phaeocystis feature of this alga is that it forms giant colonies that can reach up to 3 cm in diameter. We conducted Colonies experiments designed to elucidate the ecophysiological characteristics that presumably favor the Size development of giant colonies. Satellite images of chlorophyll fluorescence showed that the coastal Envelope bloom was initiated in summer and temporally coincident with the onset of monsoonally driven DOC upwelling. While determining the spatial distribution of Phaeocystis was not feasible, we sampled it in Sinking the near-shore region. A positive relationship was found between colony size and colonial cell densities, in contrast to results from the North Sea. Mean chlorophyll a concentration per cell was 0.45 pg cellÀ1, lower than in laboratory or temperate systems. The contribution of mucous carbon ranged from 63–95% of the total carbon; furthermore, mucous carbon per unit of colony surface area appeared to decrease with colony size, suggesting that the mucoid sheath became thinner as colonies grew larger. Sinking rates averaged 189 m dÀ1, strongly suggesting that giant colonies could only persist in shallow, turbulent environments. No relationship between colony size and sinking rates was observed. DOC concentrations of intracolonial fluid averaged 5940 mM, 25 times greater than ambient concen- trations. Estimated diffusion coefficients of ions across the mucous envelope were ca. 1.070.3 Â 10À7 cm2 sÀ1 for colonies with diameters of ca. 1.0 cm. In total, the characteristics of the giant colonies suggest that the Vietnamese strain is substantially different from that found in temperate environ- ments, and that it has a number of unusual features that influence its growth and development in coastal Vietnamese waters. & 2012 Elsevier Ltd. All rights reserved. 1. Introduction spherical during rapid growth, and generally are from 0.03– 1.0 mm in diameter. However, in recent years there have been The species Phaeocystis globosa has a cosmopolitan distribution reports of P. globosa colonies forming blooms in Southeast Asia and forms large blooms in a number of locations in the ocean, and reaching diameters of up to 3 cm (Qi et al., 2004), an order of such as the waters of the North Sea and coastal China (Schoemann magnitude larger than colonies that are usually found. Such et al., 2005). Although one strain has been reported to have ‘‘giant’’ colonies represent a major deviation from ‘‘normal’’-sized hemolytic properties (He et al., 1999), the species is considered a phytoplankton. A potential major advantage of such large colony harmful algal bloom species due to the significant indirect effects size is that the grazing by herbivores is largely reduced; however, it has on local systems via its high biomass and oxygen depletion possible disadvantages include increased sinking rates, decreased upon its degradation. All of the three major species in this genus nutrient uptake capabilities, self-shading, physical disruption due have a complex life cycle that includes stages of solitary cells and to turbulence, and large photosynthetic carbon requirements to large colonies (Schoemann et al., 2005). The balloon-like colonies produce the mucoid sheath. Given that the dominant size of are formed by small cells embedded in an organic mucilage that phytoplankton in the ocean is on the order of a few microns, the encloses a fluid-filled intracolonial space. These colonies are adaptations of giant colonies of P. globosa are of broad interest. Today it is generally acknowledged that blooms of harmful algae are correlated with and can be triggered by inputs of n Corresponding author: Tel.: þ1 804 684 7709; fax: þ1 804 684 7399. nutrients (Anderson et al., 2002; Glibert et al., 2005), especially E-mail address: [email protected] (W.O. Smith Jr.). 1 Present address: Department of Earth Sciences, University of Southern in stratified waters. Enhanced concentrations of harmful dino- California, Los Angeles, CA 90089, Unites States. flagellates in Vietnamese coastal waters were first noted 15 years 0967-0645/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.dsr2.2012.12.005 Please cite this article as: Smith, W.O. Jr., et al., Giantism and its role in the harmful algal bloom species Phaeocystis globosa. Deep-Sea Res. II (2013), http://dx.doi.org/10.1016/j.dsr2.2012.12.005i 2 W.O. Smith Jr. et al. / Deep-Sea Research II ] (]]]]) ]]]–]]] ago (Nguyen et al., 2004), but the haptophyte Phaeocystis globosa allocation. We found that giant colonies of Phaeocystis globosa are was not observed until 2002 (Tang et al., 2004); however, it has highly unusual in their adaptations, and suggest that giantism in bloomed along the south central coast every summer since then the colonies is an adaptation to the turbulent coastal environ- (Doan et al., 2010) as well as in Ha Long Bay (Nguyen et al., 2012). ment. The adaptations allow the species to reach high concentra- Its general appearance is similar to that noted in the North Sea, in tions and have harmful impacts on the coastal ecosystem. that it reaches a high biomass, and eventually generates large amounts of organic foam that appears on beaches (Blauw et al., 2010). These blooms are characterized by the appearance of giant colonies. The outbreaks appear to be associated with the south- 2. Materials and methods west monsoon, which is characterized by upwelling, substantial riverine discharges due to precipitation on land, and stratified 2.1. Experimental procedures water columns that result from solar heating. During 2002 nearly 90% of all animal and plant species in the tidal reefs of Phan Ri Bay Giant Phaeocystis globosa colonies (Fig. 1) were sampled in July (Binh Thuan Province, Viet Nam) were eliminated by the 2009, August 2010 and July 2011 off the coast of Phan Thiet, Binh P. globosa bloom, causing a substantial loss to the local economy Thuan province, South central Viet Nam (Fig. 2). Once observed, (Doan et al., 2003). Blooms of giant colonies have been reported colonies were collected very gently with small containers in the throughout much of Southeast Asia, including China (Qi et al., coastal surf zone, placed in ambient seawater at ambient tem- 2004), Viet Nam (Tang et al., 2004; Doan et al., 2010), Thailand, perature, and maintained in a shaded area. Colonies were Pakistan, Myanmar (P. Harrison, pers. comm.) and Arabian Sea replaced by newly collected ones ca. every 3 h. Only spherical, (Madhupratap et al., 2000). Interestingly, giant colonies have not non-collapsed colonies were used in experiments. Abundance of been reported from temperate waters, contrary to the suggestion colonies in the water column was not quantified due to the of Verity et al. (2007) that cold water enhances colony formation. difficulty of quantitative sampling, but visual observations sug- À1 Large size can be both an advantage and disadvantage. The gested an approximate abundance of ca. 1 giant colony L . obvious advantage over solitary cells (diameter ca. 7 mm) is the Colonies of a wide size range were selected and transferred to uncoupling from grazing by small zooplankton (size mismatch: a Petri dish filled with filtered seawater and allowed to settle to Jakobsen and Tang, 2002). A corollary to this concept is that as the bottom (but retain their spherical shape). A ruler was placed colonies form, the cells are encased in a polysaccharide envelope under the Petri dish to measure the diameters of individual that also may deter grazers due to its chemical and physical colonies (resolution 0.2 mm). Immediately after colony size mea- properties. The sheath has been reported to be extremely perme- surement, individual colonies were placed under a Nikon inverted able to oxygen (Ploug et al., 1999), so presumably it does not act microscope for quantifications of colonial cell size and colonial as a barrier to nutrient and solute exchange. Additionally, the cell abundance (Jakobsen and Tang, 2002). Total cell abundance in envelope has been suggested to be a reserve for carbon and other the entire colony was determined by multiplying cell abundance elements required for cellular metabolism that can be utilized per unit area (cell density) and total surface area of a colony. during periods unfavorable for net photosynthesis (Lancelot and Colonial cell size was estimated with a calibrated reticule. Mathot, 1985; Lancelot et al., 1987; Davidson and Marchant, After sizing, colonies were filtered under low vacuum through 1987). It has a tough polysaccharide composition (Hamm, 2000) Whatman GF/F filters for measurements of either chlorophyll or that may be resistant to microbial degradation and alter the particulate organic carbon (POC). Chlorophyll samples were overall carbon:nitrogen ratio of the pelagic ecosystem (Lancelot placed in 90% acetone and extracted for at least 24 h in cold et al., 1998; Verity et al., 2007). Possible disadvantages of and dark conditions; the chlorophyll was then measured on a giantism, however, are many. If colonies sink according to Stoke’s Turner Designs TD-700 fluorometer (JGOFS, 1996).
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