Accepted Manuscript

Review

Recent advances in ultrasonic treatment: challenges and field applications for

controlling harmful algal blooms (HABs)

Jungsu Park, Jared Church, Younggyu Son, Keug-Tae Kim, Woo Hyoung Lee

PII: S1350-4177(17)30095-0
DOI: http://dx.doi.org/10.1016/j.ultsonch.2017.03.003
Reference: ULTSON 3580

To appear in: Ultrasonics Sonochemistry

Received Date: 25 November 2016

Revised Date: 4 March 2017
Accepted Date: 5 March 2017

Please cite this article as: J. Park, J. Church, Y. Son, K-T. Kim, W.H. Lee, Recent advances in ultrasonic treatment:
challenges and field applications for controlling harmful algal blooms (HABs), Ultrasonics Sonochemistry (2017),
doi: http://dx.doi.org/10.1016/j.ultsonch.2017.03.003

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1 Recent advances in ultrasonic treatment: challenges and field applications for
2 controlling harmful algal blooms (HABs)
3
4
5 Jungsu Park1, Jared Church2, Younggyu Son3, Keug-Tae Kim4, and Woo Hyoung Lee2,*
6
1
7 Water Quality Research Center, Korea Water Resources Corporation, Daejeon, 34350, South
8 Korea
9
2
10 Department of Civil, Environmental, and Construction Engineering, University of Central
11 Florida, Orlando, FL, 32816-2450, USA
12
3
13 Department of Environmental Engineering, Kumoh National Institute of Technology, Gumi,
14 Gyeongbuk, 39177, South Korea
15
4
16 Department of Applied Biotechnology, University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo,
17 113-8657, Japan
18
19 * Corresponding author: Department of Civil, Environmental, and Construction Engineering,
20 University of Central Florida, 12800 Pegasus Dr. Suite 211, Orlando, FL 32816-2450, USA.
21 Phone: +1 407 823 5304; Fax: +1 407 823 3315; E-mail: woohyoung.lee@ucf.edu
22
23

1
24 ABSTRACT
25 Algal blooms are a naturally occurring phenomenon which can occur in both freshwater
26 and saltwater. However, due to excess nutrient loading in water bodies (e.g. agricultural runoff
27 and industrial activities), harmful algal blooms (HABs) have become an increasing issue globally,
28 and can even cause health effects in humans due to the release of cyanotoxins. Among currently
29 available treatment methods, sonication has received increasing attention for algal control
30 because of its low impact on ecosystems and the environment. The effects of ultrasound on algal
31 cells are well understood and operating parameter such as frequency, intensity, and duration of
32 exposure has been well studied. However, most studies have been limited to laboratory data
33 interpretation due to complicated environmental conditions in the field. Only a few field and
34 pilot tests in small reservoirs were reported and the applicability of ultrasound for HABs
35 prevention and control is still under question. There is a lack of information on the upscaling of
36 ultrasonication devices for HAB control on larger water bodies, considering field influencing
37 factors such as rainfall, light intensity/duration, temperature, water flow, nutrients loading, and
38 turbidity. In this review article, we address the challenges and field considerations of ultrasonic
39 applications for controlling algal blooms. An extensive literature survey, from the fundamentals
40 of ultrasound techniques to recent ultrasound laboratory and field studies, has been thoroughly
41 conducted and summarized to identify future technical expectations for field applications. Case
42 studies investigating spatial distribution of frequency and pressure during sonication are
43 highlighted with future implications.
44
45 Keywords: Algal blooms; Cyanobacteria; Field application; Harmful algal blooms (HABs);
46 Sonication; Ultrasound
47

48

2
49 1. Introduction
50 Harmful algal blooms (HABs), caused by excess nitrogen (N) and phosphorus (P) input
51 from industrial and agricultural sources into water bodies (e.g. lakes, reservoirs, and dams), have
52 become a serious problem, threatening marine life, local residents’ wellbeing, and the local
53 tourism-based economies. Recently, an exceeding proliferation of harmful algal species has led
54 to the declaration of a state emergency in four South Florida counties in the United States (US)
55 [1]. HABs are often found in water bodies which receives nutrient loads from non-point sources
56 (e.g. stormwater runoff and septic tank-impacted groundwater inflow) [2] and can produce toxins
57 like microcystins, requiring additional removal steps for processing of drinking water [3-6]. In
58 particular, excess growth of cyanobacteria (blue-green algae) in reservoirs causes various
59 technical problems in water supply plants such as unfavorable odor and taste, and toxins [7-9].
60 Even though algae are inactivated during water purification processes, the dead algal cells can
61 still cause filter blockages in filtration processes [10, 11]. In addition, the increased dissolved
62 organic carbon (DOC) can cause unintended disinfection by-products (DBPs) during chlorination
63 and pH increase from algal metabolism can reduce efficiency of coagulation [11, 12]. Purcell et
64 al. reported that an overall treatment cost of a water utility in the United Kingdom (UK)
65 increased by 25% to solve the problems caused by algal blooms [12]. To mitigate and prevent
66 HABs, it is essential to reduce nutrient loads from the watershed to reservoirs or streams [13, 14];
67 however, given that a considerable proportion of nutrients are discharged from non-point sources,
68 it is difficult to reduce and control HABs by tracking the sources of contaminants or stimulants
69 [15].
70 Various physical, chemical, and biological processes have been developed and used to
71 remove and control algae in natural water systems. These include algaecides (e.g. copper sulfate),
72 sediment capping agents (e.g. calcium chloride) [5, 15], barley straw [16-18], wetland (or
73 floating) island, ultrasonication [19], and increasing grazing pressure (e.g. Daphnia) [20].
74 Among them, ultrasound has attracted recent attention because of its simple and easy operation
75 with low impact on ecosystems and the environment. For decades, ultrasonics have been widely
76 studied for controlling cyanobacteria and the ultrasonic mechanism of algal cell disruption has
77 been well accepted [19]. However, most studies are limited to laboratory scale tests under
78 controlled environments and there are still knowledge gaps in operating sonication for algae
79 control at larger scales where water bodies have flow. The purpose of this article is to discuss the
80 fundamentals of ultrasound techniques, the recent technology advances, and future technical
81 expectations. We will also identify considerations and challenges of field applications for better
82 ultrasonication practice.
83
84 2. Theory of algal control using ultrasound devices
85 Ultrasound radiation reduces the growth of algae by structural or functional destruction of
86 algal cells [19, 21, 22]. This is possible because ultrasound radiation in water can generate
87 cavitation bubbles which collapse and cause localized temperatures and pressures to reach as
88 high as 5,000°C and 500 atmospheres of pressure [23]. This extreme environment can destroy
89 buoyancy of algae by collapsing the gas vacuoles in cyanobacteria and cause inhibition of
90 photosynthesis by sedimentation, destruction of the cell membrane (i.e. lysis) and free radical
91 species production [24-27]. Cavitation produced by ultrasound radiation in water is agreed as a
92 primary reason for algal disruption in the operation of sonic devices for the control of algal
93 blooms [19]. In this process, algal cell membranes are compromised by intense shock waves and
94 shear forces which are caused by the collapse of acoustic cavitation bubbles [28, 29]. The

3
 95 collapse of algal cells can lead to sedimentation which inhibits photosynthetic processes and thus
96 reduces the algal biomass in water [24]. In addition, the chemical process by free radicals (i.e.,
97 HO˙ and H˙) which are created from the decomposition of water vapor within the collapsed
98 bubbles can also cause destruction of cell walls [29, 30]. Recent studies suggested that not only
99 the collapse of cells but also other subsidiary effects may affect algal removal. Although
100 collapsed gas vacuoles can be reformed after sonication [25, 31], buoyancy was not fully
101 recovered, resulting in the loss of the photosynthetic ability [25].
102
103 3. Influencing factors for ultrasonication efficiency
104 There are three important operational parameters for using sonication as an algal control
105 strategy which are frequency, intensity (or power), and duration of exposure [19]. Recent studies
106 suggested that different algal species may require different operating frequencies to maximize
107 the inhibition of algal growth [12, 24, 32]. Table 1 summarizes the recent (after 2013) laboratory
108 and field studies of ultrasound on various algal species.
109
110 3.1. Frequency and ultrasonic intensity (or power)
111 Frequencies used for sonication studies were mostly in the range of 20–1,144 kHz (Table 1).
112 While lab tests used the wide range of frequencies, all field tests used relatively low frequencies
113 (< 50 kHz) probably due to operational costs. A few studies investigated the effect of high
114 frequencies (e.g. 1.7 MHz) on algal cell disruption [32, 33]; however, it was found that there
115 were no distinguishable results of using excessively high frequencies in algal control. In
116 assessing the effects of frequencies on algal control, there is often a disagreement with the
117 sonication results between lab scale tests and field applications. While lab scale tests clearly
118 showed the beneficial effect of ultrasound on algal removal under controlled environment, the
119 field data were inconsistent due to different field conditions (e.g. surface area, flow, and depth).
120 Hao et al. tested the effect of different ultrasound frequencies (20 kHz, 200 kHz, and 1.7
121 MHz) on cyanobacteria and observed a reduction in cell biomass of Spirulina (filamentous
122 cyanobacterium) in a laboratory setting with a duration of 5 min and a constant power of 40 W
123 [32]. After sonication and consecutive 6 days of cultivation, the chlorophyll concentrations
124 decreased by 19, 37 and 5 % for the frequencies of 1.7 MHz, 200 and 20 kHz, respectively,
125 indicating that 200 kHz had greater efficiency for algal removal. However, they found no
126 significant differences in algal removal with powers ranging from 20 to 80 W [32]. Zhang et al.
127 observed the removal of M. aeruginosa cells using a home-made ultrasound device in their lab
128 tests [34]. When various frequencies ranging from 20 to 1,320 kHz were applied, the algal
129 removal followed the first order reaction with a rate constant (k) of 0.0224 min-1 at 20 kHz (80
130 W) and 0.114 min-1 at 1,320 kHz (80 W), showing that the higher frequency resulted in faster
131 removal of cells [34]. Joyce et al. also tested the removal of M. aeruginosa under various
132 frequencies (20, 40, 580, 864 and 1,146 kHz) and showed that the order of the efficiency of algal
133 removal was 20 < 1,146 < 864 < 580 kHz. The 40 kHz result is excluded because of a rise in
134 algal concentration after 30 min with no reason, suggesting that there may have been unknown
135 influencing factors besides ultrasonic frequencies for algal control [35]. They also evaluated the
136 effects of intensity using 0.0018, 0.0210, and 0.0490 W cm-3 at 580 kHz for 30 min and found
137 that increasing the ultrasonic intensity (or power) further reduced the algal cell concentration. In
138 their study, low frequencies (e.g. 20 and 40 kHz) resulted in the declumping of algae after initial
139 loss in cell concentrations from inactivation, producing more individual cells with increased
140 algal concentrations based on OD after 20 min of sonication [35]. Rajasekhar et al. also observed

4
141 that sonication at low frequency (20 kHz) with high intensity (0.32 W cm-3) was effective in
142 inhibiting Microcystis cell growth [36].
143 In general, higher ultrasonic frequencies are more effective for controlling algal growth due
144 to their proximity to the resonance frequency of gas vacuoles in cyanobacteria [19]. Higher
145 frequency sonication also tends to produce more free radicals which can damage algal cells [37]
146 and thus show better efficiency for the inhibition of cyanobacterial growth than lower frequency
147 [36]. However, higher frequency also requires more electric power to generate cavitation. For
148 example, 10 times more power is needed for generating cavitation at 400 kHz than 10 kHz [38].
149 Lower frequencies require more applied time to form cavitation bubbles which can remove
150 cyanobacteria more efficiently with less power [19]. Continuous low power ultrasound at sub-
151 cavitation levels is the approach that most existing field tests use (Table 1); however, it should
152 also be noted that low frequency ultrasound (e.g. 20–40 kHz) can cause algal declumping which
153 may change the overall OD of a test solution. However, given that ultrasonic intensity may be
154 attenuated from the source, it is critical to determine the optimal range of the frequencies for
155 economic and effective control. Although relatively wide ranges of frequencies have been
156 studied to test the algal removal efficiency of ultrasound, the optimal frequency for the removal
157 of algae is still unclear.
158 The ideal frequencies of ultrasound for algal control in the field would be frequencies that
159 can collapse the gas vacuoles while minimizing the damage to the cell structure in order to
160 prevent undesired toxin release from damaged algal cells, while minimizing the required power
161 (i.e. low operational costs). In addition, the optimal frequencies may be different for each species
162 and more systematic approach would be needed to evaluate the selectivity of frequencies
163 depending on algal species.
164
165 3.2. Duration of sonication
166 The required exposure time of sonication for controlling algae varies depending on
167 ultrasonic frequencies and intensities, algal biomass concentrations and distribution, and
168 environmental conditions. In many laboratory tests, effective damage of algal cells by ultrasound
169 were observed within a wide range from several seconds to several hours. Hao et al. observed
170 continuous decrease in cyanobacterial cell density with an exposure time over 10 min at 20 kHz
171 and 40 W [32] and Ma et al. also observed continuous reduction of M. aeruginosa with
172 ultrasound radiation at 20 kHz and 30 W for 9 min [33]. From Table 1, effective removal of algal
173 cells was observed with exposure times less than 10 min in laboratory tests, while in field
174 reservoirs at least several weeks of exposure time were needed for the effective removal of algae
175 probably due to the water flow or cycle.
176 Generally, exposure time is proportional to the degradation of cyanobacterial biomass.
177 However, long periods of sonication can not only release cyanotoxins but also reduce the
178 released toxins (see the section 4 for algal toxin removal). Better understanding of the
179 relationships between frequencies, intensities, and durations of ultrasound in terms of toxin
180 release and reduction is required for effective algal control.
181
182 3.3. Morphological shape
183 Purcell et al. investigated the effect of ultrasound on four different algal species in their lab
184 scale studies [12] (Table 1). For two non-filamentous species M. aeruginosa and Scenedesmus
185 sub., the removal efficiencies by sonication were less than 20% at various frequencies from 20 to
186 1,144 kHz and intensities from 0.19 to 133 kWh m-3. However, Aphanizomenon flos-aquae

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187 (filamentous cyanobacteria) and Melosira sp. (filamentous diatom) showed significant effects of
188 ultrasound treatment with the removal efficiency of 99% at 862 kHz and 133 kWh m-3 and 83%
189 at 20 kHz and 19 kWh m-3, respectively. The results showed that breakage of filament structures
190 may be the key mechanism of the reduction of algal growth in these two species. Filamentous
191 species which have a larger surface area seemed to be more susceptible to ultrasound than non-
192 filamentous and unicellular/colonial species [12]. This indicates that morphological shapes of
193 algal species may be a contributing factor to successful ultrasound treatment rather than a
194 traditional biological classification of algal species [12, 39].
195
196 3.4. Analytical methods for determining the sonication efficiencies
197 Various assessment methods have been used to quantify the ultrasonic effects on algal
198 control which include photography, transmission electron microscopy (TEM), scanning electron
199 microscopy (SEM), flow cytometry, chlorophyll-a (Chl-a), spectrofluoro, and electrolyte
200 measurements [25]. Generally, cell counts under a microscope and/or chlorophyll-a (Chl-a)
201 concentrations are measured to represent algal biomass [40]. OD is measured using a UV-vis
202 spectrophotometer and can be used as an indicator of cell density. A calibration curve is
203 constructed based on the relationship between OD and dry biomass weight (g/L) to convert a
204 measured OD value to its correlated biomass concentration. As other available methods, Wu et al.
205 measured algal cell reductions using a haemocytometer (HAE, Weber, BS748) and validated
206 data using OD680 [29]. However, it is important to understand the mechanism of the analytical
207 methods to assess the ultrasound performance precisely and accurately. For example, a
208 haemocytometer indicated 91.54% M. aeruginosa reduction at 1,146 kHz with intensity of
209 0.0248 W cm-3, while OD measurements showed 44.63% reduction under the same condition
210 [29]. This difference is probably because the haemocytometer measures only whole number
211 remaining, while OD measured overall suspended organisms, counting the ruptured cells in
212 suspension. Hence, the proper analytical methods need to be carefully selected to eliminate any
213 potential error and misreading.
214
215 4. Algal toxin removal
216 Ultrasound is also known to be effective for algal toxin removal such as microcystins
217 produced by M. aeruginosa. Song et al. observed about an 80% reduction of microcystin-LR
218 using ultrasound at 640 kHz for 6 min in a lab test [41]. In another study, they observed about a
219 50% reduction of geosmin and 2-methylisoborneol after 10 mins of sonication at 640 kHz and 90%
220 reduction after 40 mins of sonication [42]. Ma et al. tested various frequencies (20, 150, 410 kHz,
221 and 1.7 MHz at a constant intensity of 30 W) to investigate the degradation of microcystins by
222 ultrasound [33]. After 20 min of sonication, they found that microcystins were reduced by 70.6
223 and 65.2 % at 150 and 410 kHz, showing that intermediate frequencies produced relatively
224 improved efficiency of microcystins degradation. They also evaluated the effect of power
225 intensities (30, 60, and 90 W at a constant frequency of 20 kHz) on the degradation of
226 microcystins. After 20 min of sonication, 18.1, 50.2, and 63.6% of microcystins were degraded,
227 indicating that high sonication powers resulted in faster degradation rate [33].
228 Rajasekhar et al. observed although 5 min of sonication at 20 kHz with higher intensity of
229 0.32 W cm-3 resulted in more than 60% of M. aeruginosa removal, it also led to a significant
230 increase in the microcystin content which then decreased with increasing exposure time [36].
231 One important consideration when determining the ultrasound duration is possible release of
232 algal toxins by the collapse of algal cells. An increase of toxic microcystins due to the collapse of

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233 M. aeruginosa cells was often observed when ultrasound was applied to control algae [33, 34].
234 Zhang et al. observed an increase of microcystins by ultrasound sonication (80 W, 80 kHz) for 5
235 min from the destruction of algal cells [34]. Ultrasonic irradiation shorter than 5 min was known
236 to be effective for inhibition of algal growth, while not releasing cyanotoxins from the algal cells
237 [33]. This finding indicates that the duration of ultrasound exposure is also an important factor to
238 be considered for minimizing algal toxin release in field applications in addition to frequencies
239 and intensities. Sonication with lower intensity of 0.043 W cm-3 delayed the toxin release from
240 algal cells, however, longer exposure time (> 10 min) resulted in a large increase in extracellular
241 microcystin concentrations [36]. It is suggested that sonication with intervals (resting time)
242 would reduce algal growth by collapse of algal cells and inhibit cell division or propagation [19,
243 43].
244
245 5. Challenges and field applications of ultrasound for algal control
246 5.1. Pilot studies
247 After the concept of cyanobacterial disruption using sonication was conceived three
248 decades ago, many studies on ultrasonic inactivation of algae have been conducted. Although
249 related mechanisms of algal disruption by ultrasound are well understood, case studies aiming at
250 applying ultrasound techniques for algal blooms prevention and control in open conditions (e.g.
251 actual reservoirs or intake facilities for water supply system) are still rare [44]. This is probably
252 because it is difficult to interpret the results without controlling influencing factors of complex
253 field environments which may impact overall algal biomass concentration (e.g. input, output,
254 growth, and inactivation). Given that algae are suspended in water, water flow is an important
255 factor affecting (or attenuating) the sonication efficiency in field assessments. In water bodies
256 with flow (even slow), the sonication efficiency would be questionable when algae are
257 continuously supplied from upstream accompanying with turbidity. In addition to flow, other
258 environmental parameters that should be considered for developing proper field operational
259 manuals include: turbidity, turbulence, hydraulic retention time (HRT), light intensity,
260 temperature, and nutrient loading rates. Ultrasound operational parameters determined from
261 short-term lab tests may not work for the field sonication for algal removal in a different size of
262 water and in a longer-term operation [12]. When scaling up from lab experiments to application
263 in large bodies of water, appropriate deployment strategies of ultrasonic devices covering the
264 targeting area should be planned considering the attenuation of ultrasound power and frequencies
265 as well as water flow, and intervals and durations of ultrasound need to be economically and
266 effectively determined, considering long-term operations. Ding et al. tried to use a ultrasonic
267 boat equipped with a series of outboard transducers (20 ultrasonic probes, each 20 kHz and 40 W)
268 [45]. They removed algae from an initial 107 to 105 cells /ml after sonication, which was a
269 promising as a trial test. There was a report that shows, while commercially available low energy
270 ultrasound units only were ineffective at reducing algal numbers when tested in laboratory
271 containers (20 L) and larger volume pond (7,000 L) over periods of up to 35 days, changes to
272 flow rates using a high flow jet pump associated with the ultrasound unit provided a possible
273 impact on reservoir stratification [46].
274 In addition, it is difficult to select control sites or find a good candidate as a control in the
275 field for assessing the performance. Ahn et al. conducted a field test to investigate the efficiency
276 of a combined device consisting of an ultrasonic device (22 kHz and 630 W) and two
277 recirculating water pumps (300 L/min per each pump) in a pond (9,000 m3) in Korea for 1.5
278 months (Aug. 13th–Sept. 30th, 2003) with 85 sec sonication and 30 sec break [47]. A non-treated,

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279 neighboring pond (7,000 m3) about 200 m apart was used as a control site during the test. The
280 initial environmental conditions (e.g. pH, temp., conductivity, dissolved oxygen, nitrogen, and
281 phosphorus) were similar for both ponds. Although there was an increase of turbidity in the test
282 pond from water pump circulation, the combination of ultrasound and water pumps efficiently
283 inhibited the growth of cyanobacteria and Chl-a concentrations were low at about 10 µg L-1,
284 compared to the control where concentrations were in the range of 20 to 87 µg L-1 [47]. Although
285 this study shows effective reduction of algae by combination of ultrasound and water pumps, it is
286 hard to separate the effect of water pump (i.e. water flow) which cause turbidity in the water,
287 showing a difficulty of field studies to find conclusive results.
288 Purcell et al. tested sonication efficiency for algal control using an ultrasound device
289 (model SS-5000 or SS-500, Dynamco, London, UK) [22]. They tested the ultrasound device in
290 three different reservoirs in UK between 2000 and 2008: 1) site A: controlling diatoms in a 1.2 L
291 small reservoir (28 kHz and 40 W); 2) site B: controlling filamentous algal species in 800,000–
292 995,000 m3 reservoirs with a depth of 5.9–6 m (40–50 kHz and 40 W); and 3) site D: controlling
293 algae in a 300 m2 reservoir for 27 weeks. The results of ultrasound application were inconsistent
294 and there were no noticeable effects of ultrasound on algal degradation by measuring Chl-a. This
295 again shows how particularly hard it is to separate effects of other natural factors which may be
296 related to algal growth in these open field sites. Their results of ultrasound were limited,
297 emphasizing the importance of further studies with more systematic approaches to have enough
298 data for characterizing algal susceptibility to ultrasound.
299 Schneider et al. installed four commercially available ultrasonic devices (MPC buoys, LG
300 Sonic B.V., Netherlands) in Canoe Brook reservoir (NJ, USA) to address episodic taste and odor
301 events from spring to summer (5 months) in 2014 [24]. No details on frequencies and power of
302 ultrasound were reported in this field test. Two adjacent reservoirs which are connected to each
303 other were used: one reservoir in downstream (Reservoir #1) as a test bed and the other one
304 located upstream (Reservoir #2) as a control. The water in the control was flowed into the test
305 bed. The test results showed a 93% reduction of Aphanizomenon (cyanobacteria) based on cell
306 counts and 63% removal of Chl-a during the ultrasound application. They also reported that the
307 annual savings when using ultrasound devices instead of chemicals such as copper sulfate was
308 around $87,800, although the total cost of purchasing four ultrasound devices was $160,000. It
309 was approximated that the payback period of the ultrasound devices would be 1.8 years. Because
310 the operational cost of ultrasound is much cheaper than chemical methods for the removal of
311 algae, ultrasound would be beneficial for long periods even with relatively high initial
312 installation costs of ultrasonic devices [24].
313
314 5.2. Factors to be considered in field applications
315 Although many lab tests concluded that ultrasound is effective for algal control, their test
316 conditions may not represent the field conditions. There are several factors that should be
317 considered for field ultrasound applications. Field environmental conditions such as rainfall and
318 water quality parameters (e.g. pH, nutrients, light intensity and duration, turbidity, and
319 temperature) which affect algal biomass concentrations, photosynthetic ability, and the efficiency
320 of ultrasound during test periods need to be considered. In addition, the distribution of algae in
321 reservoirs may be subject to change depending on water flow, turbulence, or wind, resulting in
322 highly variable algal concentrations (Figure 1). In this case, therefore, appropriate sampling
323 strategies (e.g. multiple sampling) are required to minimize the experimental errors in order to
324 evaluate the ultrasound performance precisely and accurately, given that ultrasound effects are

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325 typically observed over a long term (e.g. several weeks) [24, 48]. In addition, in the presence of
326 water flow (even slow), suspended algae from upstream may continuously enter the zone of
327 ultrasound treatment. It is required to secure sufficient retention time (or exposure time) for
328 effective ultrasound treatment in water bodies with flow. Water volume under sonication is
329 another factor for field consideration. To date, most field tests reported were performed in
330 relatively small water bodies (e.g. reservoirs with diameter < 1,000 m). One of the largest field
331 tests was conducted in Canoe Brook Reservoir (NJ, USA) with a surface area of 800,000 m2 and
332 a storage capacity of 2.9 million m3; however, many reservoirs in South Korea, which have
333 experienced severe HABs events every summer, are much larger (from 22 to 2,900 million m3
334 storage capacity). There is a lack of information on how operational parameters of ultrasound can
335 affect effectiveness over specific range or larger distance in large water bodies. Secondary
336 contamination by the release of cyanotoxins from collapsed algal cells is another important
337 factor to be considered before site application of ultrasound. Rajasekhar et al. suggested several
338 guidelines to minimize release of microcystins from algal cells during sonication as follows [19]:
339 1) to maintain power intensity to less than 0.24 W ml-1 (48 W); 2) to use frequencies less than
340 150 kHz and; 3) to apply ultrasound for less than 5 min. However, given that sonication is also
341 known to remove cyanotoxins [41, 42], the compensation between toxin release and removal
342 needs to be considered with a more systematic approach for field applications. Finally, the effect
343 of ultrasound on ecological systems are not clearly identified. Lürling and Tolman observed a
344 decrease of Daphnia magna as a zooplankton grazer when applying ultrasound at a frequency
345 from 20 to 44 kHz and at 0.63W (Table 1) and pointed out ultrasound’s non-selectivity (e.g.
346 inactivation of non-target organisms) [49]. As D. magna feed on phytoplankton, the reduction
347 caused a corresponding increase of algal concentration in their lab test. The effect of ultrasound
348 for human health also needs to be evaluated. It may be necessary to restrict human access or
349 activities such as swimming during sonication in reservoirs.
350
351 6. Recent advances in ultrasonic treatment
352 6.1. Combinations with remote sensing technologies
353 The recent advance of technologies such as Internet of Things (IoT) has facilitated on-line
354 and real time monitoring of water quality [50]. Images from satellites have been widely used for
355 mapping algal blooms analyzing the spatial and temporal trends in a certain area of interest [51,
356 52]. Hyperspectral image sensor technologies have also been developed to measure algal
357 concentration in reservoirs [53, 54].
358 One advantage of these sensing technologies is that they enable remote sensing of algal
359 bloom occurrences in real-time, enabling fast and appropriate operational responses. One
360 example of these technologies is the use of unmanned surface vessel (USV) capable of
361 autonomously detecting algae and treating using an ultrasonic c tool (http://dronicproject.com/).
362 The combination of remote sensors, algal removal technologies, and internet communication
363 systems may enable a ‘search-and-treat’ strategy for algal control in large water systems.
364
365 6.2. Alternatives to ultrasonic treatment for algal removal
366 Sonication is not the only method that can produce cavitation bubbles in water body.
367 Recently, a study using hydraulic jet cavitation to destroy gas vesicles was reported as an
368 alternative to ultrasound for algal removal [5, 55]. Jančula et al. employed a hydraulic jet
369 cavitation device using a converging-diverging (CD) cavitation nozzle with inlet diameter 53
370 mm and minimum diameter of 30 mm in the throat section to produce cavitation bubbles and

9
371 observed a 99% removal of cyanobacterial biomass in a lab test [5]. Moreover, no effect on the
372 membrane integrity or metabolic activity of the cells was detected, implying that hydraulic
373 cavitation seems to be harmless in terms of release of cyanotoxins. Li et al. also utilized
374 hydrodynamic cavitation for M. aeruginosa control and observed a 88% and 94% reduction of M.
375 aeruginosa cells and Chl-a concentrations, respectively, for 10 min exposure in a lab test [56].
376 For Chlorella sp., which have no gas vacuoles, only a 63% reduction in cell density was
377 observed [56]. They also compared the algal removal efficiency (5L sample) between
378 hydrodynamic cavitation and ultrasound. The hydrodynamic cavitation setup consisted of a
379 closed loop circuit including a centrifugal pump (0.27 kW) and the cavitation was controlled by
380 the orifice valves with a velocity in orifice of 0.55–1.35 m s-1. An ultrasound device with 40 W
381 and 40 kHz was used. Both devices were applied for 20 min and algal biomass was measured
382 after 3 days incubation. Although there is a question regarding whether the equivalent cavitation
383 power was used or not, the algal reduction rate of the hydrodynamic cavitation device was 90%,
384 while it was only 51% removal for ultrasound. An addition of H2O2 to the hydrodynamic
385 cavitation process improved algal reduction (by about 8%) by promoting the production of free
386 radicals [56]. However, information on the effects of hydrodynamic cavitation is limited to lab
387 scales at this moment. In addition, due to its unique design, modification of hydrodynamic
388 cavitation setups may be required for covering a large area.
389
390 7. Case studies in laboratory and field
391 7.1. Removal of algae by ultrasound device in laboratory scale
392 In this article, we tested the feasibility of a commercial ultrasound device (LG-sonic e-tank,
393 LG Sonic B.V.) for algal control before commencement of a field trial. Two plastic containers
394 (60cm (L)×40cm (W)×33cm (D)) were filled with 50L of water from Daecheung reservoir
395 (Chungcheongbuk-do, South Korea). Microcystis sp. was inoculated into both containers and the
396 ultrasound device (LG-sonic e-tank) was installed into one container and operated for two weeks
397 from July 7 to July 21, 2016. The other container was used as a control. The number of
398 Microcystis sp. cells were counted using an optical microscopy (×200) periodically. Because the
399 ultrasound is effective for collapsing algal vacuoles and/or cells which causes the algae to sink to
400 the bottom, there was no entire mixing during the test in order to eliminate the re-rising of dead
401 cells. Microcystis sp. cell numbers were measured from the surface water after careful mixing.
402 The initial cell concentration of Microcystis sp. was about 300,000 cells/mL for both containers.
403 For the first few hours (~3.6 h), the algal cell number fluctuated and there were no
404 distinguishable differences between ultrasonic application and control (Figure 2). After 4.8 days
405 of ultrasonic exposure, Microcystis sp. cell numbers were reduced by 43% while the control had
406 only a 5% reduction from the initial cell numbers. The result from 4.8 to 7.8 days showed that
407 the ultrasonication improved cell reduction by 30–55.2 % compared to control. From the test, the
408 ultrasonication showed no immediate reduction in algal cells, requiring a certain amount of
409 sonication time (e.g. 5.8 days). However, after 11 days, both ultrasound test and control showed
410 the similar reduction in algal cells (< 92%) probably due to the lack of nutrients.
411
412 7.2. Spatial distribution of frequencies and sound pressures during ultrasonication
413 Although frequency and ultrasonic intensity were the most influencing parameters for
414 successful ultrasonic applications, the specification for these parameters has not been reported in
415 some of commercial ultrasonic devices, providing difficulties in the selection of the appropriate
416 devices to control algae. In addition, the changes (or distribution) of frequencies and ultrasonic

10
417 intensities along with the distance from the ultrasound devices have not been fully investigated
418 and explored for field applications. To better understand the spatial distribution of ultrasonic
419 frequencies and intensities in fresh water as a medium, frequencies and sound pressure (Pa) from
420 two different commercial ultrasound devices were measured using a hydrophone (TC 4034,
421 Teledyne RESON A/S, Denmark) and a spectrum analyzer (N9320B RF Spectrum Analyzer
422 (BSA), Keysight Technologies, 0–300 kHz) in a lab-scale water storage reservoir (Figure 3) and
423 a field reservoir (Daechung reservoir, South Korea) (Figure 1). In this test, frequency
424 measurements were limited to less than 300 kHz because of the detectable range of the
425 hydrophone probe. For the laboratory test, a commercial ultrasonic device (LG-sonic e-tank, LG
426 Sonic B.V.) was used and frequency and sound pressure were measured at 1m intervals (total
427 distance of 5m) (Table 2). Two to four measurements in the range between 35 and 300 kHz were
428 conducted in every six-distance point and the results showed that frequencies were stable
429 regardless of distance. However, sound pressure (Pa) was dramatically decreased even after only
430 1 m distance. The maximum sound pressure was monitored at the frequency range between 230–
431 278 kHz with 91.93 Pa of sound pressure just near the device; but, this was attenuated to 13.23
432 Pa (85.6% attenuation) at 1m and 8.72 Pa (90.5% attenuation) at 5 m from the device.
433 In the field test (Sept. 9th, 2016), a different ultrasound device (LG sonic e-XXL) was
434 applied and frequencies and sound pressures were measured at 0, 0.5, 1, 2, 3, and 10m from the
435 device. Four ranges of peak frequencies from 35 to 237 kHz were observed in each sampling
436 point within the 10m distance from ultrasound application. The field test also showed the rapid
437 attenuation of sound pressure with distance even with the stable frequencies probably due to
438 turbidity. The maximum sound pressure of 53.73 Pa was detected at 105–120 kHz just beside the
439 ultrasonic device which it was attenuated to 6.79 Pa (87.4% attenuation) after only 0.5 m. At 1m
440 distance, the sound pressure attenuation under frequencies of 35–237 kHz was reduced by 91.3–
441 95.8%. For both laboratory and field tests, it was found that although frequencies were relatively
442 constant regardless of turbidity and distance, sound pressures significantly decreased even at a
443 short distance (e.g. 0.5m). From these results, the possibility of attenuation of ultrasound
444 intensity from the device also needs to be considered in field applications. However, the
445 necessity of high intensity for controlling algae in a long-term management is still debatable.
446 Given that frequency should not change, but intensity will change, multiple devices should be
447 deployed to control algal blooms in large scale reservoirs.
448
449 8. Conclusions
450 For effective algal control in field applications, it is important to determine appropriate
451 operational parameters such as frequency, intensity, and duration based on several field trials
452 including identification of targeted algal species. Although the efficiency of ultrasonication for
453 the control of algae at large scales is still debatable, ultrasound is a tempting technique in many
454 aspects compared to other technologies for algal control. First, it is a compact, simple, and field-
455 deployable technology and can be used for the removal of algae in a relatively wide area
456 (hundreds of meters following claim of commercial manufacturers). Second, the energy
457 requirements are not demanding (e.g. power use less than 40 to 80 W) compared to other
458 treatment technologies. Lastly, ultrasound is a clean technology without generating any residues
459 or by-products unlike chemical treatments. Despite evidence supporting the effectiveness of
460 ultrasound for algal control, only a few field tests have been conducted at a full scale [24, 48]
461 and there is a lack of information on a scale-up of the technology.
462 This review highlights several considerations for the scale-up of the technology. First is the

11
463 attenuation of the ultrasonic intensity. The deployment of multiple floating ultrasonic devices or
464 mobile operational systems, such as vessels installed with multiple ultrasonic devices, may need
465 to be used to supply sufficient ultrasound intensity when controlling algal blooms in a large
466 reservoir. In addition, the entire removal of algae from a large reservoir may be neither realistic
467 nor desirable considering the economical aspect. Thus, it would be essential to determine
468 realistic goals of ultrasound sonication and confine target areas to locations near water intake
469 towers or areas where people visit frequently. Further field/pilot studies considering factors such
470 as rainfall, light intensity/duration, temperature, water flow, nutrients loading, and turbidity
471 would be required for making the technology reliable.
472

12
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611

612
613 Figure 1. Algae blooms in Daechung reservoir (Chungcheongbuk-do) in South Korea. Note that
614 algal concentrations are highly variable within a small area.
615

616

617

618

619

620

621

622

623

624

625

626

627

628

629

16
630

631

632
633 Figure 2. Effect of ultrasound on the number of Microcystis sp. cells at the water surface.
634

635

636

637

638

639

640

641

642

643

644

645

646

647

17
648

649

650
651 (a) lab-scale water storage reservoir

652
653 (b) an ultrasound device and a hydrophone
654 Figure 3. Frequency (kHz) and sound pressure (Pa) test of an ultrasound device (LG-sonic e-tank,
655 LG Sonic B.V.) using a hydrophone (Teledyne Reson TC4034) and a spectrum analyzer
656 (Keysight, N9320B) in a laboratory scale water storage reservoir located in K-water Institute,
657 South Korea.
658

659

18
660 Table 1. Recent studies on ultrasonication for algae removal and control
Target species Frequency Power Exposure Lab/field Results Ref.
(or time test
intensity)/ (duration)
density
Cyanobacteria, 28 kHz 40 W 5 months Field No significant effect Purcell et
Greens, Diatoms 40–50 kHz (reservoir: al. [22]
0.8–1.0
million m3)
Microcystis 20–1,144 200 W at 20 5–500s Lab < 20% cell removal Purcell et
aeruginosa kHz kHz & (1.5 L) rates. al. [12]
(cyanobacteria, (20, 582, 600 W at Species not
unicellular), 862, and other susceptible.
Scenedesmus 1,144 kHz) frequencies Possible bloom
subspicatus (green growth control
alga, colonial) 0.19–133
kWh m-3
Aphanizomenon 20–1,144 200W at 5–500s Lab 48–93% cell Purcell et
flos-aquae kHz 20kHz & (1.5 L) removal as al. [12]
(cyanobacteria, (20, 582, 600W at frequency increases
filamentous) 862, and other
1,144 kHz) frequencies

0.19–133
kWh m-3
Melosira sp. 20– 200 W at 20 5–500s Lab 83% (max.) cell Purcell et
(diatom species, 1,144kHz kHz & (1.5 L) removal at the al. [12]
filamentous) (20, 582, 600 W at lowest frequency
862, and other (20kHz) and 19
1,144 kHz) frequencies kWH m-3

0.19–133
kWh m-3
Microcystis 21.5 kHz 8.24W 10 minutes Lab Observed recovery Rodriguez-
aeruginosa (0.6 L) of collapsed gas Molares et
vesicles within 24 al. [25]
hours of sonication
Aphanizomenon N/A N/A May–Dec., Field 90% reduction of Schneider
(cyanobacteria) 2014 (reservoir: algae based on cell et al. [24]
2.9 million numbers after more
m3 ) than a week
sonication
Daphnia magna* 20–44 kHz 0.63W 25 days Lab All Daphnia were Lurling
(zooplankton as (0.8 L) killed within 30 and
grazing control) minutes. Tolman
Higher [48]
Phytoplankton
concentration
observed as
Daphonia died
661 *This zooplankton grazer was selected as non-target species to test the environmentally-friendly aspect of
662 ultrasound.

663

19
664 Table 2. Spatial distributions of frequency (kHz) and sound pressure (Pa) of ultrasound
665 (a) Result from a lab-scale water storage reservoir

Range of peak frequencies

Distance
from the 35~46 kHz 150~170 kHz 230~278 kHz 275~300 kHz
ultrasound
device Sound Sound Sound Sound
Frequency Frequency Frequency Frequency
(m) Pressure Pressure Pressure Pressure
(kHz) (kHz) (kHz) (kHz)
(Pa) (Pa) (Pa) (Pa)

0m 46 78.88 170 60.84 230 91.93 298 62.45

1m 39 12.75 154 11.21 230 13.23 278 23.46
2m 46 8.66 154 9.20 230 11.53 - -
3m 35 6.16 - - 230 12.96 - -
4m - - 154 5.95 230 7.66 - -
5m - - 154 9.14 278 8.72 298 9.50
666

667 (b) Result from Daechung reservoir, South Korea

Range of peak frequencies

Distance 35~40 kHz 105~120 kHz 169~180 kHz 237 kHz
from the
ultrasound Sound Sound Sound Sound
device (m) Frequency Frequency Frequency Frequency
Pressure Pressure Pressure Pressure
(kHz) (kHz) (kHz) (kHz)
(Pa) (Pa) (Pa) (Pa)

0m 36 49.91 105 53.73 176 46.78 237 48.91

0.5 m 35 8.38 120 6.79 169 7.58 237 5.43

1m 35 4.30 120 2.28 176 3.54 237 3.00

2m 40 2.20 120 1.34 170 2.21 237 1.81

3m 37 2.20 120 1.83 170 1.49 237 1.37

10 m 40 0.51 107 0.31 180 0.29 237 0.25

668

669

20
670 Highlights
671 • There is a lack of information on the use of ultrasonication at large scales/the field.
672 • The efficiency of ultrasonication for algal removal in field is still debatable.
673 • Attenuation of ultrasonic intensity needs to be considered in field applications.
674 • Further field data is required for the upscaling of ultrasonication devices.
675

21