Cyanobacterial bloom dynamics in Lake Taihu

Cyanobacterial bloom dynamics in Lake Taihu

J O U RN A L OF E N V I RO N M EN TA L S CI EN CE S 32 (2 0 1 5 ) 2 4 9–2 5 1 Available online at www.sciencedirect.com ScienceDirect www.journals.e...

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J O U RN A L OF E N V I RO N M EN TA L S CI EN CE S 32 (2 0 1 5 ) 2 4 9–2 5 1

Available online at www.sciencedirect.com

ScienceDirect www.journals.elsevier.com/journal-of-environmental-sciences

Cyanobacterial bloom dynamics in Lake Taihu Katherine Z. Fu1 , Birget Moe1 , Xing-Fang Li, X. Chris Le⁎ Division of Analytical and Environmental Toxicology, Department of Laboratory Medicine and Pathology, University of Alberta, Edmonton, Alberta T6G 2G3, Canada

AR TIC LE I NFO Available online 7 May 2015 Keywords: Cyanobacteria Blue-green algae Microcystin Natural toxins Water quality Nutrients Nitrogen and phosphorus Carbon dioxide

Lake Taihu is the third largest freshwater lake in China and serves as an important drinking water source for the local populace; however, decades of excessive nutrient loading fueled by anthropogenic activities have resulted in hypertrophic conditions, promoting the annual formation of nuisance phytoplankton blooms (Chen et al., 2003; Duan et al., 2009). In May 2007, unseasonably warm spring temperatures combined with the problematic hypertrophic conditions led to the formation of a massive bloom composed of cyanobacteria of the genus Microcystis (Guo, 2007; Yang et al., 2008; Qin et al., 2010). Because some strains of Microcystis are capable of producing potent hepatotoxins, called microcystins (MCs), this bloom was particularly alarming (WHO, 2003). In an attempt to flush the massive bloom from the lake using water diverted from the Yangtze River, lake management efforts resulted in the unintended formation of a current that funneled the majority of the cyanobacterial bloom directly into the intake of the Wuxi city drinking water plant (Qin et al., 2010). As a result, clean drinking water was inaccessible to over

⁎ Corresponding author. E-mail: [email protected] (X.C. Le). 1 These authors contributed equally.

2 million people in Wuxi, Jiangsu Province, for a week, creating a public health emergency (Guo, 2007; Qin et al., 2010). The Wuxi drinking water crisis of 2007 placed a spotlight on the importance of understanding the influence of anthropogenic activities on cyanobacterial bloom occurrence to protect valuable drinking water sources. In Lake Taihu, this is particularly important, as Microcystis species have been shown to dominate in summer blooms, contributing up to 60% of total phytoplankton biovolume (Deng et al., 2014). Although not all strains of Microcystis produce MCs, significant concentrations of MCs have been detected in both water samples and aquatic organisms from Lake Taihu, including the MC variant MC-LR (Song et al., 2007; Sakai et al., 2013), a potent toxin that has also been classified as a possible human carcinogen (Grosse et al., 2006; IARC, 2010; Liu and Le, 2015). However, a clear understanding of the relationship between anthropogenic activities and cyanobacterial bloom occurrence is complicated by the fact that bloom growth can be influenced by a variety of factors, such as temperature, daylight, water turbulence, pH, and water nitrogen and phosphorus content (WHO, 2003). Hence, elucidating the influence of anthropogenic activities on each of these factors is paramount to the establishment of effective lake management strategies to control bloom outbreaks. In two new studies published in the Journal of Environmental Sciences (JES), researchers at the State Key Laboratory of Lake Science at the Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, have examined two of these key aspects of cyanobacterial blooms: macronutrient enrichment (Ma et al., 2015) and atmospheric carbon dioxide levels (Yu et al., 2015). Macronutrient enrichment from urban, agricultural, and industrial sources, such as fertilizer use, human waste, and storm-water runoff, is a historically well-documented promoter of cyanobacterial bloom formation and persistence (Paerl and Otten, 2013). More recently, the rapid rise in atmospheric CO2 levels caused by increasing consumption of fossil fuels is gaining more attention for its influence on cyanobacterial blooms due to its effects on the pH of aquatic water bodies (O'Neil et al., 2012). Both highlighted

http://dx.doi.org/10.1016/j.jes.2015.04.003 1001-0742/© 2015 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. Published by Elsevier B.V.

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studies from JES used self-contained bioassays to mimic the environmental conditions of Lake Taihu to assess the effects of macronutrient and CO2 levels on the growth dynamics of cyanobacterial blooms. In our first highlighted study, Ma et al. (2015) measured the effects of macronutrient enrichment on total phytoplankton biomass and growth rate over an 18 day period in water collected near Wuxi to assess the relationship between nutrient ratio and nutrient limitation in Lake Taihu. Three treatments (nitrogen (N) only, phosphorus (P) only, and N plus P) were evaluated via addition of NaNO3 and KH2PO4, and nutrient concentrations that were between 2 and 32 times that of the non-treated control lake water were examined. Total phytoplankton biomass was determined from total biovolume, which was calculated from cell number and cell size measurements in preserved phytoplankton samples. Growth rate was calculated using a modified exponential growth equation based on chlorophyll-a concentrations that were determined spectrophotometrically over the 18 day experiment. The authors found that addition of N plus P resulted in faster growth rates than addition of either N or P alone, and an addition of 8-fold N plus P was sufficient for maximal phytoplankton growth. They also reported that N limitation existed in the collected water samples, as phytoplankton growth was promoted by the addition of N alone, but not by the addition of P alone. However, there was no significant difference in growth rate for any of the tested concentrations of N-only addition, indicating that 2-fold N-only addition caused P limitation. Thus, the authors determined a nutrient ratio of total N to total P (TN:TP) of 18.9–56.7, where N limitation occurred when TN:TP was less than or equal to 18.9–56.7 and shifted to P limitation when TN:TP was greater than or equal to 18.9–56.7. Surprisingly, the TN:TP ratio determined in this study to describe the shift from N to P limitation was different from both the classically cited Redfield ratio and from ratios reported in the literature from studies of Lake Taihu and other freshwater bodies. To account for this discrepancy, the authors suggest three factors that may have been of influence. The first of these was the measurement of TN and TP that is used in most studies, as TN and TP does not reflect the bioavailable N and P present. The bioavailable fraction of N and P is known to vary widely in different freshwater bodies of water. Additionally, because key ideas related to nutrient limitation in freshwater ecosystems have been extended from individual crop plants, the complexity of Lake Taihu may have been underrepresented. Finally, it has been shown previously that the growth of some Microcystis species in Lake Taihu is iron-limited, which can confound the assessment of N and P limitation. Nevertheless, the TN:TP ratio determined by Ma and colleagues can be a valuable tool for short-term management of cyanobacterial bloom outbreaks in Lake Taihu, as it can be exploited to promote conditions of nutrient limitation. Our second highlighted study (Yu et al., 2015) measured the dynamics of MC-producing and non-MC-producing Microcystis strains during cyanobacterial blooms at high and low atmospheric CO2 concentrations. As part of the 21-day mesocosm experiment, the authors collected water from Meiliang Bay in Lake Taihu and the buckets were placed in CO2 chambers set at three CO2 concentrations: 270 μL/L

(pre-industrial concentration), 380 μL/L (current concentration), and 750 μL/L (future concentration). The N and P content of the water was kept at a constant level throughout the experiment. To determine the abundance of the total Microcystis population, the authors quantified the 16S rDNA using real-time PCR. To further differentiate the MC-producing genotypes from the total Microcystis population, they also quantified the mcyD gene, found within the microcystin synthetase gene operon (Tillett et al., 2000). While the 16S rDNA is specific to the Microcystis genus, the mcyD gene is only present in toxic MC-producing strains of Microcystis. Therefore, the real-time PCR analyses of the 16S rDNA and the mcyD gene provided quantitative information on the abundance of the MC-producing and non-MC-producing Microcystis strains. The study found that elevated atmospheric CO2 levels decreased the pH of the water samples and resulted in increased dissolved inorganic carbon concentration. Despite the changes in CO2 concentration, the abundance of total Microcystis population in the samples remained comparable to levels at other concentrations. Interestingly, the results showed that increased CO2 availability led to non-MC-producing strains to out-compete MC-producing strains, reducing the concentration of MCs present. Although the underlying reasons for these results are not understood, this work shows the potential of monitoring CO2 levels to better predict the MC-producing and non-MC-producing Microcystis strains during cyanobacterial blooms. Understanding the growth dynamics of MC-producing Microcystis strains will contribute to better management of the health risks facing populations that rely on water sources contaminated by blooms. Although both highlighted studies were able to demonstrate that anthropogenic activities can have a direct influence on the growth dynamics of cyanobacterial blooms in water from Lake Taihu, more research is needed before these findings can be adopted into lake management strategies. A limitation of both of these studies was the use of isolated bioassays using controlled parameters, which make them far less complex than an entire aquatic ecosystem. More advanced modeling studies that take into account the multiple factors that can affect cyanobacterial bloom growth are needed. These studies (Ma et al., 2015; Yu et al., 2015), however, have provided a good starting point for future research. Over the past several decades, the increase in frequency and intensity of cyanobacterial blooms in both fresh and marine waters has become a global issue (Paerl and Otten, 2013). For example, a recent episode of cyanobacterial blooms in Lake Erie in August 2014 left 500,000 people in Toledo, Ohio, without safe drinking water (Tanber, 2014; Wilson, 2014). While our highlighted studies focused on a single freshwater lake, the conclusions drawn are not limited to Lake Taihu. Nutrient limitation and CO2 enrichment can affect growth dynamics of cyanobacterial blooms worldwide and hence these studies support strategies for approaching the control of bloom outbreaks that can be applied globally when parameters specific to a body of water, such as temperature and baseline N and P content, are assessed. Ultimately, the adoption of effective lake management strategies for controlling cyanobacterial bloom outbreaks in drinking water sources is critical for the protection of human health (Paerl et al., 2014; Qu et al., 2014).

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Cyanobacterial bloom in Lake Taihu. Photo courtesy of Jianrong Ma and Li Yu, Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences.

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