Water Research 183 (2020) 116091 Contents lists available at ScienceDirect Water Research journal homepage: www.elsevier.com/locate/watres Bloom-forming toxic cyanobacterium Microcystis: Quantification and monitoring with a high-frequency echosounder * Ilia Ostrovsky a, 1, Sha Wu a, b, c, 1, Lin Li b, , Lirong Song b a The Yigal Allon Kinneret Limnological Laboratory, Israel Oceanographic and Limnological Research, Migdal, 14950, Israel b Key Laboratory of Algal Biology, Institute of Hydrobiology, The Chinese Academy of Sciences, Wuhan, 430072, China c University of Chinese Academy of Sciences, Beijing, 100049, China article info abstract Article history: Harmful cyanobacterial blooms pose a serious environmental threat to freshwater lakes and reservoirs. Received 1 November 2019 Investigating the dynamics of toxic bloom-forming cyanobacterial genus Microcystis is a challenging task Received in revised form due to its huge spatiotemporal heterogeneity. The hydroacoustic technology allows for rapid scanning of 17 June 2020 the water column synoptically and has a significant potential for rapid, non-invasive in situ quantification Accepted 19 June 2020 of aquatic organisms. The aim of this work is to develop a reliable cost-effective method for the accurate Available online 22 June 2020 quantification of the biomass (B) of gas-bearing cyanobacterium Microcystis in water bodies using a high- frequency scientific echosounder. First, we showed that gas-bearing Microcystis colonies are much Keywords: Backscattering signal stronger backscatterers than gas-free phytoplanktonic algae. Then, in the tank experiments, we found a fi Gas-bearing cyanobacterium strong logarithmic relationship between the volume backscattering coef cient (sv) and Microcystis B Gas vesicle proxies, such as Microcystis-bound chlorophyll a (Chl aMicro) and particle volume concentration. The sv/B Remote quantification ratio remained unchanged over a wide range of B concentrations when the same source of Microcystis Vertical distribution material was used. Our measurements in Lake Dianchi (China) also revealed strong logarithmic rela- Surface scum tionship between sv and Chl aMicro. The biomass-calibrated echosounder was used to study the diurnal variability of Microcystis B in the lake. We found a sharp increase in the cyanobacterium B and sv/Chl aMicro ratio near the water surface during the daytime and more uniform distribution of these parameters during the nighttime. We argue that the variations in B and sv/Chl aMicro ratio could be associated with temporal changes in thermal stratification and turbulent mixing. Our data suggest that the sv/Chl aMicro ratio positively correlates with (i) the percentage of larger colonies in population and/or (ii) the content of free gas in cells. The last properties allow Microcystis colonies to attain rapid floating, which enables them to concentrate at the water surface at conducive ambient conditions. The sv/Chl aMicro ratio can be a new important variable reflecting the ability of Microcystis colonies to migrate vertically. Monitoring of this ratio may help to determine the early warning threshold for Microcystis scum formation. The pro- posed acoustic technology for in situ quantification of Microcystis biomass can be a powerful tool for accurate monitoring and assessment of this cyanobacterium at high spatiotemporal resolution in water bodies. © 2020 Elsevier Ltd. All rights reserved. 1. Introduction (Chorus and Bartram, 1999; Paerl and Otten, 2013; Qin et al., 2010; Srivastava et al., 2013). We lack a comprehensive understanding of Cyanobacteria blooms have major environmental, social, and the role of different ecological factors in the development of economic impacts. In particular, Microcystis blooms and the asso- Microcystis blooms, and as a result, the control of such blooms is a ciated algal toxin microcystin have been implicated in human and challenging task. The development of suitable methods for moni- animal illnesses and are causing increasing worldwide concern toring cyanobacterial blooms for purposes of research and man- agement became an important issue in recent decades (Anderson, 2009). Various physical and chemical approaches are used to * Corresponding author. quantify Microcystis biomass, including microscopic counting E-mail address: [email protected] (L. Li). (Geider et al., 1997; Srivastava et al., 2013), measurements of 1 Co-first authors, both authors contributed to the work equally. https://doi.org/10.1016/j.watres.2020.116091 0043-1354/© 2020 Elsevier Ltd. All rights reserved. 2 I. Ostrovsky et al. / Water Research 183 (2020) 116091 chlorophyll a (Chl a) concentrations (Cullen, 1982; Iriarte et al., Medwin, 1977). Thus, a scattering cross-section of a small GV- 2007; Yentsch and Menzel, 1963), laser particle analysers (Karp- containing cell, cell-containing colony, and closely spaced popula- Boss et al., 2007; Li et al., 2014), the flow-cytometer method tion of colonies do not equal the sum of cross-sections of their (Wang et al., 2014; Wert et al., 2013), and satellite remote sensing respective components. While much effort has been made to study (Kahru, 1997; Wu et al., 2015). Despite this, there is no satisfactory the physical characteristics of Microcystis colonies, their backscat- method for fast and accurate monitoring of the spatiotemporal tering acoustic properties are still unknown. organization of cyanobacterial blooms. For instance, microscopic Echosounder and ADCP measurements made during an intense counting is a widely used method for identifying phytoplankton Microcystis sp. bloom in Lake Kinneret (Israel) suggested that the species composition; however, microscopic observations are time- presence of GVs in cells make this cyanobacterium acoustically consuming and only allow for analysis of a small number of water visible, which also allows for observing its spatiotemporal vari- samples. Other commonly used methods, such as Chl a measure- ability and vertical migrations (Ostrovsky et al., 2017, 2018). To ment, laser particle analysers, and flow-cytometry measure proxies thoroughly examine the possibility to quantify the cyanobacterial of Microcystis biomass in limited volumes may not be able to biomass with an echosounder, we carried out intensive measure- distinguish Microcystis from other phytoplankton organisms. These ments of acoustic backscattering signal at different concentrations methods are labour and time-intensive, thus hampering the rapid of the cyanobacteria in an outdoor tank and a lake. monitoring of the Microcystis biomass in a dynamic and spatially The main aims of this study were: (1) to investigate the rela- heterogeneous environment. In contrast, satellite remote sensing tionship between the acoustic backscattering signal from Micro- may provide detailed spatial information on phytoplankton distri- cystis and its biomass under controlled experimental conditions bution over large aquatic areas, but it only detects phytopigment and in the field; (2) to elaborate a simple cost-effective acoustic densities in the near-surface water layer at relatively large time method for high resolution quantitative in situ monitoring and intervals (Bok et al., 2010; Kim et al., 2010) and is highly dependent accurate investigations of the spatiotemporal variability of Micro- on weather conditions (Kim et al., 2018). Therefore, more accurate cystis in water bodies; (3) to demonstrate the advantages of the methodologies are urgently needed to monitor Microcystis vari- acoustic technology based on 24-h observations on Lake Dianchi. ability at a high spatiotemporal resolution, in the entire water column, over large aquatic basins. 2. Materials and methods Contrary to the above-mentioned methods, acoustic remote- sensing methods allow quasi-synoptic surveys of large volumes of 2.1. Measurements design and instrumentation water. Scientific echosounders provide high-resolution data on organism abundance in both space and time, and have been widely Acoustic data were collected with a Simrad EY60 scientific used to quantify fish, zooplankton (Huber et al., 2011; Simmonds echosounder equipped with a 200-kHz narrow-beam (7) trans- and MacLennan, 2005; Stanton et al., 1994), and gas bubbles ducer ES200-7. The system was used to measure the acoustic (Ostrovsky, 2003). However, acoustic methods cannot typically backscattering signal from Microcystis colonies in an outdoor classify individual targets taxonomically. Small gas-bearing fish experimental tank (the Guanqiao field station, Wuhan, China) and larvae and zooplankton are strong sound scatterers and thus can be Lake Dianchi (Kunming, China). The main purposes of the tank detected with scientific echosounders and Acoustic Doppler Cur- experiments were: (1) to evaluate the contribution of GVs to a rent Profilers (ADCP) (Lorke et al., 2004; Potiris et al., 2018). Recent Microcystis colony backscattering signal and (2) to quantify the studies showed that spatial and temporal variability of gas- relationships between the acoustic backscattering signal and containing cyanobacteria could be observed with acoustic devices Microcystis sp. abundance over a wide range of biomasses. We used at ultrasonic frequencies (Godlewska et al., 2018; Hofmann and Chl a concentration and particle volume concentration (PVC) as Peeters, 2013). To date, no reliable methods have been developed common biomass proxies. for in situ acoustic quantification of bloom-forming cyanobacteria First, we compared the acoustic backscattering signal from and monitoring their populations. intact