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Article

Comparative Study on Phytoplankton Treatment Effectiveness of the Ballast Water Management System with Four Different Processes

by
Yan Zhang
1,2,
Wei Feng
1,2,
Yating Chen
1,2,
Junzeng Xue
1,2 and
Huixian Wu
1,2,*
1
College of Marine Ecology and Environment, Shanghai Ocean University, 999th, Huancheng Road, Pudong New District, Shanghai 201306, China
2
Centre for Research on the Ecological Security of Ports and Shipping, Shanghai Ocean University, 999th, Huancheng Road, Pudong New District, Shanghai 201306, China
*
Author to whom correspondence should be addressed.
Water 2024, 16(15), 2098; https://doi.org/10.3390/w16152098
Submission received: 9 July 2024 / Revised: 23 July 2024 / Accepted: 24 July 2024 / Published: 25 July 2024
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Abstract

:
Ballast water (BW) poses the risk of introducing species. Therefore, ships install the ballast water management system (BWMS) to reduce the risks caused by BW. To gain a deeper understanding of the treatment effectiveness of the BWMS, in this study we compared the effectiveness of four different treatment processes of BWMSs on seawater phytoplankton, which were electrochlorination treatment, hydroxyl radical oxidation treatment, membrane separation and deoxygenation treatments, and UV irradiation treatment. The results showed that all four BWMSs had a reduction in phytoplankton density of over 99%. In terms of phytoplankton taxa, the effectiveness of the four BWMSs was different. The taxa removal rates of the four BWMSs were 81.25%, 39.58%, 59.31%, and 74.49%, respectively. Electrochlorination treatment and UV irradiation treatment were significantly more effective than hydroxyl radical oxidation treatment and membrane separation and deoxygenation treatments. The residual phytoplankton taxa were mainly dinoflagellate and diatoms, such as Cucumeridinium, Prorocentrum, Navicula, and Skeletonema. Taxa that can tolerate treatment may be more likely to survive and reproduce. There is still a need to continue to strengthen the development and research on the BWMS in the future to promote the development of BW management.

1. Introduction

With globalization, a significant increase in the volume of ship trade has occurred [1,2]. For the stabilization and safety of the ship voyage, ships pump natural water into ballast tanks and store it; when the ship is fully loaded, the BW is discharged [3]. With merchant ships sailing around the globe, more than 3 billion tons of BW are transferred to ports around the world every year [4]. Species are transferred around the world through the BW transfer over the years, and species migration has led to multiple and wide-ranging ecological impacts [4,5,6,7,8]. Over the past 20 years or so, many introduction events have been attributed to the transportation of BW [9,10,11]. Biological invasions caused by BW have been listed as one of the four major global threats [12].
To avoid such undesirable effects of ships’ BW [13,14,15,16], the International Marine Organization (IMO) adopted the International Convention for the Control and Management of Ships’ Ballast Water and Sediments (BWM Convention) [17]. It entered into force on 8 September 2017. The D-1 standard, i.e., Ballast Water Exchange Standard (also called Regulation D-1), is commonly used to minimize the concentration of creatures in ballast tanks [18]. The D-1 standard requires ships to exchange at least 95% of the volume of BW in open ocean waters more than 200 miles from shore in water depths of at least 200 m. To further control the migration and introduction of live organisms in BW, the IMO adopted the D-2 standard, i.e., the Ballast Water Performance Standard (also called Regulation D-2). It will be mandatory from 8 September 2024 [19]. The D-2 standard limits the concentration of living organisms in discharged BW (Table 1). In Table 1, ≥50 µm living organisms means living organisms with a minimum dimension of ≥50 µm; ≥10~50 µm living organisms means living organisms with a minimum dimension of ≥10 µm and <50 µm; and <10 µm living organisms means living organisms with a minimum dimension of <10 µm. To meet the D-2 standard, ships should install and apply the ballast water management system (BWMS) [20,21,22,23,24].
Phytoplankton is one of the richest and most diverse taxa successfully transported through BW [25,26,27]. The harmful phytoplankton species, which are toxic or capable of triggering red tides, sometimes have an irreversible economic and ecological impact [28,29,30], particularly for aquaculture farmers [31]. Accordingly, it is an urgent global issue that ships’ BW serves as a vector for the spread of harmful phytoplankton species around the world [18,21,32]. Therefore, phytoplankton is often the focus of BW management and research.
In the early days, BW exchange was used as an interim BW management measure in the transitional phase of the implementation of the BWM Convention. However, the removal efficiency of BW exchange for organisms is not always optimal. The organism removal rate of BW exchange was sometimes as low as around 29 to 40% [33]. Increases in phytoplankton diversity and abundance after exchange have even been found in some studies [34,35]. BW exchange is not a method that allows discharge water to meet the D-2 standard. For example, Burkholder et al. [36] surveyed 28 warships docked in nine U.S. ports, and they found that at least 47% of the post-exchange samples had phytoplankton abundances >10 cells/mL. Harsh environmental conditions in ballast tanks can adversely affect phytoplankton living there, such as darkness, lack of oxygen, food deprivation, and predation [37,38,39]. Phytoplankton abundance and richness will decrease with increasing BW age during long-distance ship voyages [40,41]. BW with an age of more than 10 days is considered low risk [2,42,43]. However, Wu et al. [44] and Ardura et al. [45] have shown that it was found that some phytoplankton were still able to survive and even reproduce in BW older than 10 days, such as Melosira sulcata and Skeletonema costatum, which are considered tolerant species [2].
With the gradual implementation of the D-2 standard, BWMS treatment is gradually becoming the mainstream BW management method. There are many types of BWMS, and BW is usually treated using physical and chemical methods such as filtration, membrane separation, electrolytic disinfection, UV irradiation, and oxidation [46,47]. Treatment of BWMS is usually carried out in two or three steps. Typically, BWMS begins with the use of filters to remove larger organisms or substances, followed by formal treatment of the BW using chemical or physical methods. The third step is usually a second UV treatment or neutralization after chemical treatment. BWMS treatment reduces the risk of organisms in BW more than BW exchange, and phytoplankton abundance in BWMS-treated samples is typically lower than in samples after BW exchange [20,48,49]. To date, more than 80 BWMSs have been recognized and approved for use by the IMO, and more than 10,000 BWMSs have been installed and put into service on board ships [50]. However, while the BWMS was able to bring BW into compliance with the D-2 standard in the type approval test, numerous studies have shown that noncompliance still exists in the discharged water of the ships that have installed and are using the BWMS [51,52,53]. Some external factors may affect the treatment effectiveness of BWMSs, such as season and water quality [50]. Incorrect installation, operation, or maintenance can also result in BWMS not performing treatment effectively [32,54]. Different phytoplankton taxa have different tolerances to treatment, and phytoplankton in the resistant life stage are more difficult to remove by BWMS [55,56]. Last but not least, while BWMS has been able to significantly reduce the risk of plankton introduction in BW, this does not mean that the treated discharge water is completely safe. Stehouwer et al. [50] showed that phytoplankton in treated discharge water still had the potential to regrow.
BW treatment is one of the most mature and promising BW management approaches. Therefore, innovation and development of BW treatment technologies and BWMS, as well as further evaluation and research on the effectiveness and stability of BWMS treatment, are necessary. Most of the past studies on the treatment effect of BWMS have been on the testing and evaluation of a single BWMS [57,58,59]. Few direct comparisons have been made between the treatment effectiveness of BWMSs with different treatment processes. In this study, we conducted BWMS seawater trials with phytoplankton to compare the treatment effectiveness of BWMS with four different treatment processes: electrochlorination treatment, hydroxyl radical oxidation treatment, membrane separation and deoxygenation treatment, and UV irradiation treatment. This study will improve our understanding and assessment of the effectiveness of BWMS and will provide a more comprehensive and scientific basis for the development of BW treatment technology and BW management.

2. Materials and Methods

2.1. Trial Design

During the period from 2019 to 2021, 36 seawater trials of BWMS treatment were thus conducted at the Shanghai Ocean University’s land-based testing site located in Shanghai, China. By using a simulated ballast tank environment and BWMSs provided by the manufacturer, the process of treating BW by the BWMS was simulated. The experimental environment provided by the base includes a 500 m3 water preparation tank, a 250 m3 test tank, a 50 m3 fresh water tank (for pipe flushing), and a sedimentation tank. An aeration device is installed in the bottom of the water preparation tank to effectively mix the substances and organisms in the test water. Treated water (BW) is normally stored in test tanks. The interior wall of the test tank is covered with ballast tank coatings, to better simulate the environmental conditions inside the ballast tanks [60]. Trials followed the Environmental Technology Verification protocol (U.S. Environmental Protection Agency, Environmental Technology Verification Program). The Environmental Technology Verification protocol is an environmental technology evaluation system designed to test and evaluate environmental technologies through third-party assessment organizations. It contains the Generic Protocol for the Verification of Ballast Water Treatment Technology which is used to guide BWMS performance testing [61].
The BWMS treatment process used for the trials was as follows: (1) Filtration + Electrochlorination + Neutralization (FEN, Sunrui Marine Environment Engineering Company Ltd., Qingdao, China). The filter unit is an automatic backwashing filter with a filtration accuracy of 50 µm. The electrolysis unit produces a highly concentrated sodium hypochlorite solution by electrolyzing a portion of the BW. The solution is then mixed with the main BW and diluted to a specific concentration to sterilize the water. When the residual chlorine concentration is greater than the IMO-specified value, the neutralization system is activated to inject a neutralizer into the drain to neutralize the residual oxidant. (2) Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO, Headway Technology Group (Qingdao) Co., Ltd., Qingdao, China). The filtration unit is an automatic backwashing filter with a filtration accuracy of 50 µm, and the catalytic unit kills organisms in the water by generating a large number of highly active oxidizing substances such as hydroxyl radicals. (3) Filtration + Membrane separation + Deoxygenation (FMD, JIANGSU NANJI MACHINERY Co., Ltd., Taixing, Jiangsu, China). The filtration unit is a 50 µm automatic backwashing filter. The membrane separation unit is a microfiltration membrane with a pore size of 10 µm. The nitrogen generation unit utilizes a PSA to generate nitrogen by alternately adsorbing oxygen from the air and filling the ballast tank to create an anoxic environment. (4) Filtration + UV (FUV, Shanghai Electric Cyeco Environmental Technology Co., Ltd., Shanghai, China). The filters have a filtration accuracy of 40 µm and the UV unit uses medium-pressure UV lamps (effective UV wavelengths of 200–280 nm).

2.2. Test-Water Preparation

The test water is natural seawater taken from the sea near Shanghai Port (30.64° N, 122.04° E). Before the trial begins, the seawater is usually pumped into a sedimentation tank to allow the larger particles in the seawater to settle. After that, it is pumped into the water preparation tank for test-water configuration. The test water was configured in full compliance with the G8 guidelines issued by the IMO: when the test water is marine water (28~36 PSU), DOC > 1 mg/L, POC > 1 mg/L, and TSS > 1 mg/L; when the test water is brackish water (10~20 PSU), DOC > 5 mg/L, POC > 5 mg/L, and TSS > 50 mg/L; the density of ≥10~50 µm living organisms is >103 cells/mL, and the density of ≥50 µm living organisms is >105 cells/m3. In this study, the quality of test water in different treatment groups is shown in Table 2.

2.3. Sample Collection and Detection

2.3.1. Sample Collection

The test process begins with the test water in the water preparation tank being pumped into the test tank via a ballast pump. This simulates a ship ballasting natural water into the ship’s ballast tanks. Test water needs to be treated by BWMS before pumping into the test tank. The BW is discharged after a period of storage in the test tank. Throughout the test, untreated test water samples (uptake water) and treated discharge water samples were collected. Throughout the ballasting and unloading process, we continuously collected at least 100 L of water through a sampling tube into a bucket. A total of 1 L of water from the bucket was taken as a phytoplankton sample and placed in a brown plastic bottle. Once sampling is complete, it should be stored at room temperature and tested within 6 h. The trials conducted in this study were designed to provide a service for manufacturers to evaluate the performance of BWMSs. The number of trials performed by different BWMSs varies due to different manufacturers’ requirements. We collected as many samples and data as we could. In this study, 4 pairs of samples were collected from the electrochlorination (FEN) treatment group, 8 pairs of samples from the hydroxyl radical oxidation (FEO) treatment group, 10 pairs of samples from the membrane separation and deoxygenation (FMD) treatment group, and 14 pairs of samples from the UV irradiation (FUV) treatment group.

2.3.2. Sample Detection

The FDA/CMFDA stain method recommended by the Generic Protocol for the Verification of Ballast Water Treatment Technology [47] was used for the analysis of the samples. There is a combination of Fluorescein Diacetate (FDA, Thermo Fisher Scientific Inc., Carlsbad, CA, USA) and 5-chloromethylfluorescein diacetate (CMFDA, Thermo Fisher Scientific Inc., Carlsbad, CA, USA). Living phytoplankton cells are stained and fluoresce strongly in green when exposed to blue light, while dead cells do not fluoresce. The procedure was as follows: (1) remove 1 mL from the well-mixed phytoplankton sample into a centrifuge tube; (2) add FDA to the sample at a final concentration of 5 µm/mL. Add CMFDA to the sample at a final concentration of 2.5 µm/mL, and (3) mix the sample thoroughly and store it away from light for 10 min to allow for adequate staining of the sample; (4) when the staining is complete, load the 1 mL sample into a Sedgewick Rafter counting chamber, excited with blue light (wavelength 450 nm to 435 nm), and examine under a fluorescence microscope. Here we consider ≥10~50 µm living organisms under the microscope as phytoplankton and examine them. A total of 3 mL of uptake water subsamples and 6 mL of discharge water subsamples were analyzed for each trial. Since the fluorescence signal will fade out with time, the examination time should not exceed 20 min.

2.4. Data Analysis

This study deals with the interpretation of Density (cells/mL), Species Richness, Frequency (%), Dominance (Y), and Shannon–Wiener index ( H ′ )as follows:
Density is the number of individual phytoplankton per unit volume of sample; species richness is the number of phytoplankton taxa identified from the samples; frequency in this study is the ratio of the number of samples in which a particular phytoplankton genus was identified to the total number of samples.
Dominance (Y):
Y = ( n i / N ) × f i
where n i is the amount of phytoplankton genus i; N is the total amount of phytoplankton; and f i is the frequency of phytoplankton genus i.
Shannon–Wiener index ( H ′ ):
H ′ = − ∑ i = 1 s p i l n p i
where s is the number of taxa; and p i is the relative abundance of taxa i in the sample.
Paired t-tests and independent samples t-tests were used to test for differences between samples. This study analyzed the data and created graphs by using GraphPad Prism 9.0, IBM SPSS Statistics 25, and Microsoft Excel 2016.

3. Results

3.1. Change in Phytoplankton Density

In the untreated uptake water, the mean phytoplankton densities of the FEN, FEO, FMD, and FUV groups were approximately 1075.38 cells/mL, 1087.58 cells/mL, 1154.55 cells/mL, and 1164.81 cells/mL. The densities of phytoplankton in the discharge water after treatment in the four treatment groups were 0.67 cells/mL, 2.10 cells/mL, 4.82 cells/mL, and 2.65 cells/mL. After treatment, phytoplankton density was significantly reduced in all samples (p < 0.05) and the D-2 standard was met in all samples (Figure 1). As far as phytoplankton density is concerned, the treatment effect of BWMS varies among the different processes. The mean values of the removal rate of phytoplankton (density) were 99.94% (FEN group), 99.80% (FEO group), 99.58% (FMD group), and 99.77% (FUV group), respectively (Figure 2).

3.2. Change in Phytoplankton Species Richness and Composition

In the uptake samples, a total of 19 species or taxa from 5 phyla of phytoplankton were identified, namely Dinophlagellata, Heterokontophyta, Charophyta, Chlorophyta, and Cyanobacteria. The number of phytoplankton species or taxa in each phytoplankton phylum was seven, eight, one, two, and one. In the treated discharge samples, a total of 14 species or taxa from 3 phyla of phytoplankton, Dinophlagellata, Heterokontophyta, and Cyanobacteria, were identified. The number of phytoplankton species or taxa in each phytoplankton phylum was six, seven, and one, respectively (Table 3). In the uptake water, the Shannon–Wiener index was 1.60 (FEN group), 1.19 (FEO group), 1.03 (FMD group), and 1.38 (FUV group) for each treatment group, The highest index was found in the FEN group and the lowest in the FMD group. In the discharged water, the Shannon–Wiener index was 0.14 (FEN group), 1.16 (FEO group), 0.78 (FMD group), and 0.25 (FUV group) for each treatment group. The highest index was found in the FEO group and the lowest in the FEN group.
In the uptake water samples, the mean values of phytoplankton species richness were 7 (FEN group), 6.63 (FEO group), 7.80 (FMD group), and 6.35 (FUV group), respectively. The mean phytoplankton species richness values in the treated discharge samples from the four treatment groups were 1.25 (FEN group), 4 (FEO group), 3.1 (FMD group), and 1.64 (FUV group), respectively (Figure 3). The species richness of phytoplankton in the uptake and discharge water was significantly different (p < 0.05) by t-test. This indicates that BW treatment can significantly reduce phytoplankton species richness. After treatment, phytoplankton species richness was reduced in most of the samples, and the reduction in species richness ranged from 0 to 100%, with a mean value of about 63.27%. In terms of species richness, different BWMSs had different effectiveness in removing phytoplankton taxa. The mean values of removal of phytoplankton taxa by BWMS were 81.25% (FEN group), 39.58% (FEO group), 59.31% (FMD group), and 74.49% (FUV group), respectively (Figure 4).
The dominance (Y) of each phytoplankton genus is shown in Table 4. In the uptake water of the FEN group, the dominant genera were Cucumeridinium (Y = 0.4170), Nitzschia (Y = 0.0880), and Navicula (Y = 0.0865), etc. (only the top three dominant phytoplankton genera are shown), and the dominant genera in the discharge water were Cucumeridinium (Y = 0.4375) and Navicula (Y = 0.0156); in the uptake water of the FEO group, the dominant genera were Chaetoceros (Y = 0.2094), Pleurosigma (Y = 0.1286), and Cucumeridinium (Y = 0.0959), etc., and the dominant genera in the discharge water were Chaetoceros (Y = 0.0928), Prorocentrum (Y = 0.0928), and Navicula (Y = 0.0842); in the uptake water of the FMD group, the dominant genera were Prorocentrum (Y = 0.7150), Nitzschia (Y = 0.0523), and Peridinium (Y = 0.0418), etc., and the dominant genera in the discharge water were Prorocentrum (Y = 0.5512), Chaetoceros (Y = 0.1682), and Discostella (Y = 0.0540); in the uptake water of the FUV group, the dominant genera were Cucumeridinium (Y = 0.4037), Discostella (Y = 0.1493), and Skeletonema (Y = 0.1475), etc., and the dominant genera in the discharge water were Cucumeridinium (Y = 0.6454), Discostella (Y = 0.0730), and Skeletonema (Y = 0.0096).

3.3. Phytoplankton Taxa Remaining in the Discharged Water

The occurrence frequency of phytoplankton taxa in the discharge water of each treatment group is shown in Figure 5. The residual genera in treated discharge water varied among treatment groups. The residual genera in the FEN group discharge water were Cucumeridinium and Navicula, with Cucumeridinium occurring more frequently (frequency > 50%). Among the residual genera in the FEO group were Lingulaulax, Peridinium, Cucumeridinium, Prorocentrum, Chaetoceros, Skeletonema, Pleurosigma, Navicula, Discostella, Nitzschia, and Oscillatoria, with higher frequencies of Cucumeridinium, Prorocentrum, Chaetoceros, and Navicula. The residual genera in the FMD group were Cucumeridinium, Peridinium, Prorocentrum, Chaetoceros, Skeletonema, Navicula, and Discostella, with Prorocentrum, Chaetoceros, and Discostella occurring more frequently. The residual genera in the discharge water of the FUV group were Cucumeridinium, Skeletonema, and Discostella, with Cucumeridinium being a high-frequency genus. In addition, Cucumeridinium was present in the discharge water of all four treatment groups, and Skeletonema, Navicula, and Discostella were present in the discharge water of three treatment groups.

4. Discussion

4.1. Comparative Analysis of the Effect of BWMS Treatment on Phytoplankton

In this study, the density of phytoplankton in the treated discharge water was less than 10 cells/mL in all treatment groups, meeting the requirements of the D-2 standard. All four BWMS had a reduction in density of over 99% with little difference. In terms of bio-efficacy, these four BWMS treatments were very effective. However, in terms of phytoplankton diversity, there were significant differences in the treatment effectiveness of BWMS with different treatment processes. The diversity index and richness of phytoplankton in the discharged water of the FEN group were the lowest. FEN treatment was also the most effective in removing phytoplankton species richness, with a mean removal rate of 81.25%. In this study, both in terms of diversity index and species richness, the FEN treatment process has the best treatment results. The FEN treatment process is mainly used to disinfect plankton by generating sodium hypochlorite through electrolysis of seawater [62]. The performance of FEN treatment is also quite prominent in actual BW treatment scenarios. For example, Hill et al. [63] found that sodium hypochlorite at concentrations higher than 3 ppm was able to remove 99% of bacteria, phytoplankton, and zooplankton. Currently, the FEN treatment process is the mainstream BW treatment technology in various countries. The phytoplankton diversity index and species richness in the discharged water of the FUV group were higher than those of the FEN group but lower than those of the FEO and FMD groups. The FUV treatment was second only to the FEN treatment in removing species richness, with a removal rate of 74.49%. FUV treatment causes damage to the DNA, proteins, and enzymes of organisms, and is an effective means of eliminating organisms from BW. It is also a widely used BW treatment technology [47].
Phytoplankton diversity index and species richness in the discharged water of the FMD group were higher than those of the FEN and FUV groups, but lower than those of the FEO group. In the trials, FMD treatment removed 59.31% of phytoplankton taxa, which was more effective than FEO treatment (39.58%) but less effective than FEN and FUV treatments. The FMD treatment consists of three treatment steps. The uptake water was first initially filtered using a 50 µm screen. Secondly, the uptake water is treated by membrane separation using a 10 µm microfiltration membrane. Most of the phytoplankton were trapped and removed in these two steps. Finally, by filling the ballast tanks with nitrogen, an anoxic environment was created which resulted in the death of aquatic organisms due to lack of oxygen. Prolonged hypoxia is undoubtedly harmful to most aquatic organisms, but deoxygenation treatments have not been shown to be effective for all phytoplankton [64]. The pore size of the membrane in the trial was 10 µm, and some small-sized microalgae or phytoplankton larvae might still survive in the membrane separation stage. It has been shown that microfiltration operations using membranes with a pore size of 0.1 µm are required to completely remove microalgae, such as Nannochloropsis oculate [65,66]. The FEO treatment mainly generates hydroxyl radicals with strong oxidizing ability by means of electrocatalysis and removes organisms in BW through oxidation [67]. In the study, the FEO group had the highest phytoplankton diversity index and species richness in the discharged water, and had the worst effect on the reduction of species richness, with a removal rate of only 39.58%. FEO treatment is an environmentally friendly, cost-effective, and promising technology for BW treatment. However, the treatment effectiveness of the FEO treatment process is affected by other factors, such as the efficiency of hydroxyl radical production, pollutant concentration, and complex water quality [68,69,70]. For example, low salt directly affects the formation of active substances such as hydroxyl radicals in the electrocatalytic process, which reduces the treatment effectiveness [47].
In summary, in this study, the FEN and FUV treatments are superior to the FMD and FEO in terms of the removal of phytoplankton taxa. In addition to the shortcomings of the FEO and FMD treatments mentioned above, the current research and development with respect to FMD and FEO are also not fully mature, and the stability and reliability of the system operation are poorer than that of FEN and FUV. To some extent, this explains the differences in treatment capabilities of different BWMSs.

4.2. Analysis of Residual Phytoplankton Taxa in Treated Discharge Water

In our study, the phytoplankton remaining in the discharge water after treatment in each treatment group were mainly diatoms and dinoflagellates. Genera that are dominant in untreated uptake water are usually also dominant in treated discharge water. For example, the genera with the highest dominance in the uptake water of the FEN group, FEO group, FMD group, and FUV group were Cucumeridinium (Y = 0.4170), Chaetoceros (Y = 0.2094), Prorocentrum (Y = 0.7150), and Cucumeridinium (Y = 0.4037), respectively. These genera also remained the most dominant in the treated discharge water. Phytoplankton genera that are more dominant in untreated uptake water are usually more present in treated discharge water. For example, Cucumeridinium was not only present in the discharge water of all treatment groups but was also a high-frequency species in the discharge water of the FEN group, the FEO group, and the FUV group. Skeletonema, Navicula, and Discostella were found in the discharged water of three different treatment groups. In general, dominant phytoplankton taxa tend to have higher densities than non-dominant taxa, which may increase the possibility that the dominant taxa are not removed completely.
We observed that the dominance of some phytoplankton increased after treatment, such as Cucumeridinium (FEN and FUV groups), Lingulaulax (FEO group), Prorocentrum (FEO group), Navicula (FEO group), Chaetoceros (FMD group), and Discostella (FMD group). In addition to the advantage of the dominant genus, the survival of these algae may be related to their adaptations and tolerances. Dinoflagellates have diverse nutritional patterns. Many are mixotrophic and can adapt to the environment by switching between autotrophic and heterotrophic states [71]. Dinoflagellate can enter a dormant state and form cysts or dormant spores when exposed to unfavorable conditions and damage, which is an important survival strategy for dinoflagellate [72,73]. Dinoflagellate in this state is more adaptable and tolerant than before. Some diatoms can also form dormant spores or resting cells [74,75,76,77]. Some dinoflagellates have an internal dual silica skeleton structure that provides protection [78]. Prorocentrum has a similar structure, which appeared in the discharge water of both the FEO group and the FMD group. Diatoms have a highly silicified shell that can filter UV and buffer the extreme physical and chemical environment outside [77]. Many studies have shown that diatoms have a wide range of tolerance to external environmental stresses, such as temperature, salinity, and pH. The Skeletonema is a typical tolerant genus [73,79,80].
In addition, to some extent, BW treatment is selective for phytoplankton. For example, in this study, in the uptake water of the FEO group, Navicula, Discostella, and Nitzschia were not the dominant genera. However, they survived the treatment, and Navicula was even the dominant genus in the discharge water (Y = 0.0842). Lee et al. [81] showed that antioxidant activity is present in the enzymatic digests of certain diatoms, such as Navicula. Because of the high UV radiation resistance of dinoflagellate and diatoms, it is difficult for FUV treatments to remove them completely [55]. Membrane separation treatment can miss small-diameter phytoplankton or larvae, and deoxygenation treatment has limited effectiveness on phytoplankton. Stehouwer et al. [50] found that regrowth of phytoplankton in all six BWMS-treated discharge waters occurred when good growth conditions were provided. Residual taxa in treated discharge water still have the potential to grow and colonize if released into a new environment. This suggests that current BW treatment does not eliminate the risk of introducing phytoplankton.
Statistically, FEN treatment and FUV treatment currently account for more than 70% of approved and commercially available BWMSs [82]. FEN is the mainstream technology to treat BW, with good effectiveness and stability. However, FEN treatment is limited by salinity, and its effectiveness is reduced under freshwater conditions. Harmful chemicals are also generated during the electrolysis process [83]. FUV treatment is also widely used in BW treatment. FUV techniques have drawbacks such as high energy consumption and phytoplankton regrowth. High water turbidity can also limit the treatment effectiveness of FUV [84]. FEO treatment and FMD treatment have the advantages of low cost, low energy consumption, and low pollution. This makes up for the defects of FEN treatment and FUV treatment [47]. However, FEO treatment and FMD treatment are emerging technologies, current research and development is not fully mature, and performance has not been verified by time and practice. As research and development in the field of BW progress further, higher demands are placed on the treatment capacity of treatment technologies, while greater emphasis is placed on the economic applicability and environmental friendliness of the technologies. Therefore, to promote the development of BW treatment technology for ships and the development of BW management, it is still necessary to continue to strengthen the development and research on BW treatment technology and BWMS in the future.

5. Conclusions

The results show that four different processes of BWMS can effectively treat phytoplankton under seawater conditions. The density of phytoplankton in the treated discharge water met the requirements of the D-2 standard. However, the treatment effects of different BWMSs were different. In this study, FEN and FUV treatments were significantly better than FEO and FMD treatments, especially in the removal of phytoplankton taxa. Phytoplankton that dominated the discharge water or were present in multiple treatment groups were mostly diatoms and dinoflagellates such as Cucumeridinium, Prorocentrum, Navicula, and Skeletonema. These taxa that can survive BWMS treatments typically have a high level of adaptation and tolerance. They may be more likely to survive and reproduce when released into new environments. It is therefore recommended that future studies on BWMS treatments should focus on these phytoplankton taxa. There is still a need to continue to strengthen the development and research on BW treatment technology and BWMS in the future. This will help us to gain a more comprehensive and in-depth understanding of the effectiveness of BWMS and thus promote the development of BW management.

Author Contributions

Y.Z.: conceptualization, methodology, investigation, formal analysis, writing—original manuscript, visualization, writing—review and editing; W.F.: writing—review and editing, supervision, project administration; Y.C.: validation, writing—review and editing; J.X.: review and editing; H.W.: resources, writing—review and editing, supervision, project administration. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the National Key Research and Development Program of China grant number 2022YFC2302800. The APC was funded by Shanghai Ocean University.

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data are not publicly available due to the fact that the data are derived from BWMS performance evaluation projects undertaken by the Laboratory and are closely linked to the fundamental interests of the manufacturer. Due to laboratory policy and confidentiality agreements, we regretfully cannot share the data.

Acknowledgments

Construction of the BW Testing Laboratory for offshore Engineering Equipment is underway at the National Engineering Laboratory for Testing and Experimentation in Offshore Engineering Technology.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships which may affect the work reported here.

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Water 16 02098 g001
Figure 1. Density (cells/mL) of phytoplankton in uptake and discharge water of Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups; *** significant differences at the p < 0.001 level.
Figure 1. Density (cells/mL) of phytoplankton in uptake and discharge water of Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups; *** significant differences at the p < 0.001 level.
Water 16 02098 g001
Water 16 02098 g002
Figure 2. Removal rate (%) of phytoplankton (density) by BWMS in Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups; the letters “a”, “b”, and “c” represent the significance among the groups, with the same letter indicating no significant difference and different letters indicating a significant difference.
Figure 2. Removal rate (%) of phytoplankton (density) by BWMS in Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups; the letters “a”, “b”, and “c” represent the significance among the groups, with the same letter indicating no significant difference and different letters indicating a significant difference.
Water 16 02098 g002
Water 16 02098 g003
Figure 3. Phytoplankton species richness (number of phytoplankton taxa) in uptake and discharge water of Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups; ** indicates significant differences at the p < 0.05 level and *** significant differences at the p < 0.001 level.
Figure 3. Phytoplankton species richness (number of phytoplankton taxa) in uptake and discharge water of Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups; ** indicates significant differences at the p < 0.05 level and *** significant differences at the p < 0.001 level.
Water 16 02098 g003
Water 16 02098 g004
Figure 4. The removal rate (%) of phytoplankton taxa by BWMS in Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups; the letters “a”, “b”, and “c” represent the significance among the groups, with the same letter indicating no significant difference and different letters indicating a significant difference.
Figure 4. The removal rate (%) of phytoplankton taxa by BWMS in Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups; the letters “a”, “b”, and “c” represent the significance among the groups, with the same letter indicating no significant difference and different letters indicating a significant difference.
Water 16 02098 g004
Water 16 02098 g005
Figure 5. Heat map of the frequency of occurrence of phytoplankton (at the genus level) in discharge water for Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups.
Figure 5. Heat map of the frequency of occurrence of phytoplankton (at the genus level) in discharge water for Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups.
Water 16 02098 g005
Table 1. The BW discharge standards of the IMO.
Table 1. The BW discharge standards of the IMO.
Organism TypeThe D-2 Standard of IMO
≥50 µm living organisms<10 ind./m3
≥10~50 µm living organisms<10 cells/mL
<10 µm living organisms-
Vibrio cholerae<1 CFU/100 mL
(O1 and O139)
Escherichia coli<250 CFU/100 mL
Intestinal Enterococci<100 CFU/100 mL
Table 2. Test-water-quality conditions in Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups; “marine” means that the test water is marine water (28~36 PSU), and “brackish” means that the test water is brackish water (10~20 PSU).
Table 2. Test-water-quality conditions in Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups; “marine” means that the test water is marine water (28~36 PSU), and “brackish” means that the test water is brackish water (10~20 PSU).
ParametersFENFEOFMDFUV
MarineBrackishMarineBrackishMarineBrackishMarineBrackish
TSS (mg/L)61.83 56.90 59.12 54.08 46.00 37.80 54.24 52.31
POC (mg/L)6.69 5.39 8.46 6.65 4.00 4.40 5.36 5.77
DOC (mg/L)6.20 6.61 13.26 7.29 14.14 6.54 6.52 6.44
Temperature (°C)22.25 22.38 27.77 18.70 25.64 22.16 18.57 12.23
Salinity (PSU)30.30 19.00 30.03 17.31 30.42 19.26 29.53 18.59
PH8.02 8.41 7.84 8.15 8.22 8.12 7.82 7.49
DO (mg/L)7.36 8.07 7.85 9.83 8.44 9.14 9.91 11.26
Turbidity (NTU)28.87 25.79 36.49 56.83 8.38 11.18 22.15 33.44
The density of ≥10~50 µm living organisms (cells/mL)1014.67 1136.08 1000.75 1116.53 1179.20 1129.90 1191.62 1138.00
The density of ≥50 µm living organisms (cells/m3)114,685.17 227,908.33 135,643.28 127,793.78 120,707.28 120,042.60 111,894.18 112,391.55
Number of trials2 2 2 6 5 5 7 7
Table 3. List of phytoplankton species and their occurrence in uptake and discharge samples.
Table 3. List of phytoplankton species and their occurrence in uptake and discharge samples.
PhylumTaxaUptake WaterDischarge Water
Dinophlagellata
Lingulaulax polyedra (F.Stein) M.J.Head, K.N.Mertens & R.A.Fensome++
Peridinium sp.++
Cucumeridinium coeruleum (Dogiel) F.Gomez, P.López-García, H,Takayama & D.Moreira++
Cucumeridinium sp.++
Prorocentrum micans Ehrenberg++
Prorocentrum sp.++
Protoperidinium leonis (Pavillard) Balech+
Heterokontophyta
Chaetoceros sp.++
Skeletonema costatum (Greville) Cleve++
Pleurosigma sp.++
Navicula sp.++
Discostella sp.++
Discostella stelligera (Cleve & Grunow) Houk & Klee++
Nitzschia sp.++
Fragilariopsis kerguelensis (O’Meara) Hustedt+
Charophyta
Cosmarium sp.+
Chlorophyta
Chlorella vulgaris Beijerinck+
Tetraselmis sp.+
Cyanobacteria
Oscillatoria sp.++
Table 4. Genera-level phytoplankton dominance (Y) in Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups.
Table 4. Genera-level phytoplankton dominance (Y) in Filtration + Electrochlorination + Neutralization (FEN), Filtration + Electrocatalytic Hydroxyl Radical Oxidation (FEO), Filtration + Membrane separation + Deoxygenation (FMD), and Filtration + UV (FUV) treatment groups.
Phytoplankton GenusFENFEOFMDFUV
UntreatedTreatedUntreatedTreatedUntreatedTreatedUntreatedTreated
Lingulaulax--0.0463 0.0483 ----
Peridinium0.0316 -0.0731 0.0371 0.0418 0.0028 --
Cucumeridinium0.4170 0.4375 0.0959 0.0347 0.0166 0.0135 0.4037 0.6454
Prorocentrum0.0122 -0.0452 0.0928 0.7150 0.5512 --
Protoperidinium0.0244 -------
Chaetoceros--0.2094 0.0928 0.0341 0.1682 --
Skeletonema0.0350 -0.0447 0.0223 0.0334 0.0031 0.1475 0.0096
Pleurosigma0.0203 -0.1286 0.0223 0.0059 -0.0092 -
Navicula0.0865 0.0156 0.0049 0.0842 0.0234 0.0021 0.0683 -
Discostella0.0159 -0.0026 0.0012 0.0340 0.0540 0.1493 0.0730
Nitzschia0.0880 -0.0023 0.0012 0.0523 -0.0667 -
Fragilariopsis0.0014 -------
Cosmarium--0.0001 -----
Chlorella0.0635 ---0.0003 -0.0366 -
Tetraselmis--0.0009 -----
Oscillatoria--0.0104 0.0087 ----
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Zhang, Y.; Feng, W.; Chen, Y.; Xue, J.; Wu, H. Comparative Study on Phytoplankton Treatment Effectiveness of the Ballast Water Management System with Four Different Processes. Water 2024, 16, 2098. https://doi.org/10.3390/w16152098

AMA Style

Zhang Y, Feng W, Chen Y, Xue J, Wu H. Comparative Study on Phytoplankton Treatment Effectiveness of the Ballast Water Management System with Four Different Processes. Water. 2024; 16(15):2098. https://doi.org/10.3390/w16152098

Chicago/Turabian Style

Zhang, Yan, Wei Feng, Yating Chen, Junzeng Xue, and Huixian Wu. 2024. "Comparative Study on Phytoplankton Treatment Effectiveness of the Ballast Water Management System with Four Different Processes" Water 16, no. 15: 2098. https://doi.org/10.3390/w16152098

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