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Article

Investigating the Role of Terminal Stolon of Marine Invasive Green Macroalga Caulerpa taxifolia in the Removal of Inorganic Nitrogen from Seawater

by
Bingxin Huang
1,2,
Zhan Wang
2,
Yue Chu
1 and
Lanping Ding
1,2,*
1
Tianjin Key Laboratory of Animal and Plant Resistance, College of Life Sciences, Tianjin Normal University, Tianjin 300387, China
2
Marine Biology Institute, Shantou University, Shantou 515063, China
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2023, 11(1), 43; https://doi.org/10.3390/jmse11010043
Submission received: 21 November 2022 / Revised: 6 December 2022 / Accepted: 20 December 2022 / Published: 28 December 2022
(This article belongs to the Special Issue New Insights in the Study of Harmful Algal Bloom)
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Abstract

:
The marine benthic green macroalga Caulerpa taxifolia is an invasive seaweed found in Europe, America, and Australia, and it forms into huge algal meadows on shallow seafloors with its stolon and rhizoid systems. It has bloomed along the coast of the South China Sea, causing serious environmental problems. However, its ecological impact has not been well studied. Therefore, this study investigated the changes in concentration of NH4-N and NO2-N in artificial seawater in which C. taxifolia was cultivated under laboratory conditions during the circadian rhythm. Results showed that concentrations of NH4-N and NO2-N decreased with the increase in culture time during the circadian rhythm. In 24 h, the NH4-N-removal efficiency increased during the light period, and the maximum reached 71.4%; that of NO2-N increased with time extension in the dark period, and the maximum reached 9.2%. The absorption of NH4-N and NO2-N by terminal stolon of C. taxifolia was different. NH4-N was absorbed more preferentially than NO2-N. However, there was no obvious correlation between NH4-N and NO2-N absorption. Therefore, the terminal stolon of C. taxifolia can be used to clean up inorganic nitrogen, and showed great application potential in the remediation of eutrophic waters as the algal-bacterial symbiotic system could facilitate NO2-N removal.

1. Introduction

In recent years, with the rapid development of the blue industry in China, environmental pollution in waters has seriously affected the habitats and the spawning/feeding grounds of offshore fishery species, which has become the main obstacle in the green development of offshore fisheries [1]. It is estimated that from 2016 to 2020, the average annual total nitrogen and phosphorus inputs into the coastal waters of Bohai Bay were 14,490 and 768 tons, respectively [2]. Meanwhile, with the substantial increase in living standards, demand for aquatic products has quickly increased. The economic aquatic breeding of fish, shrimp, and other animals has significantly risen in China [3]. Excreta and remains in fishery breeding are also important pollution sources in aquaculture areas, as the concentrations of NH4-N, NO2-N, and NO3-N have substantially increased, which has consequently aggravated the eutrophication of aquaculture water. High concentrations of NH4-N and NO2-N in water cause many kinds of aquatic biological diseases [4,5,6,7,8]. Reducing high concentrations of NH4-N and NO2-N in farming water has become an urgent issue.
To remedy eutrophication by nitrogen and phosphorus in nearshore aquaculture water, scholars have actively explored methods [9,10] such as algal-bacterial symbiosis [11], higher aquatic plants [12,13,14], microalgae [15], and physicochemical methods [16,17]. Among them, the use of seaweed cultivation for controlling eutrophication has been recently proved practical [18,19].
Seaweed, a low aquatic plant, requires ample nitrogen and phosphorus for growth. Many are used as good aquaculture feeds. Seaweed cultivation plays a great role in carbon cycling and eutrophication curing. Excess nutrients can be easily taken from water by seaweed for growing. Almost all seaweed contain NO 3 − , NO 2 − , and NH 4 + as nitrogen sources, especially NO 3 − and NH 4 + [20]. However, high-concentration NH 4 + could be toxic to seaweed, and, similarly, high-concentration NO 2 − could inhibit the growth of seaweed. A previous study showed that NH4-N is the preferred form for plant absorption, and the presence of NH4-N could inhibit nitrate intake by plants [21].
Species of the genus Caulerpa belong to a type of marine green macroalgae, and are mainly distributed in tropical and subtropical waters; from intertidal zones to subtidal zones up to 50 m in depth. In recent decades, Caulerpa taxifolia has been reported to invade the Mediterranean and temperate regions of Australia, as well as other regions worldwide [22,23,24,25]. As a highly invasive species, it has biological characteristics of adaption to new environments and rapid growth [22], and overruns in sand and hard surfaces such as rocks. Its thallus is a large multinucleated tubular cell. In the evening, when the light is low or absent, its chloroplasts slowly sink into the stolons, and, in the morning, when there is light, its chloroplasts slowly rise and fill the whole lumen of the thallus, during which different parts of the thallus are able to differently absorb nutrients in day and night alternation, and its robust stolons and rhizoid system, being holdfast, can reach any substrate to be attached. When the stolon terminal thrives, their population forms a huge mat of algae covering the entire seafloor, and the thickness of the mats can reach up to 1 m. The algal mats not only block sunlight, but also hamper the exchange of nutrients from niches beneath, which may harm local coral reefs and cause ecological problems. Many such cases of serious damage have been reported in the Mediterranean region, Australia, and the USA (California). C. taxifolia in the Mediterranean is mostly distributed between Toulon in France and Genoa in Italy [26]. While it unevenly occurs in habitats, the outbreak sites of blooms are mainly located near poorly treated wastewater discharges and on decaying beds of seagrass Posidonia oceanica [27].
The explosive growth of C. taxifolia near poorly treated wastewater outfalls benefits from nutrients in untreated wastewater [28]; therefore, its strong adaptability and purification ability of wastewater has great potential for water purification. However, previous studies have largely ignored nitrogen removal from seawater. Although some businesses have claimed that Caulerpa could purify NO2-N in order to promote it as ornamental seaweed or biological purification, there is a lack of proven data. Information on the removal of nitrogen by stolons terminals is scarce, even though stolons have great influence on the invasion of C. taxifolia. Therefore, to understand the key growth components for stolon formation, further studies are necessary on nitrogen absorption as nutrients by terminal stolon.
Recently, progress has been made in purifying seawater using seaweed [18]. However, few reports are available on the purification ability of C. taxifolia. This species is widely distributed in the southern tropical coastal areas of China, especially in relatively calm water areas, with large biomass in some areas [29]. Its biological characteristics and invasion ability have been elaborated in our previous paper [30]. Because of its rapid growth, its impact on both open and closed ecosystems is dramatic, showing great potential for water purification. Therefore, concentrations of NH4-N and NO2-N in their circadian rhythms after entry into water were measured, its ability to remove nitrogen in waters was analyzed, and new countermeasures were proposed for the purification of open water and algal fish symbiotic culture water.

2. Materials and Methods

2.1. Experimental Materials

Samples of C. taxifolia were collected in Yinggehai, Huangliu on Hainan Island, South China. In the laboratory, they were placed into a 5-L glass cylinder that had been sterilized with alcohol and sun exposure, and then, about 3-L of natural seawater with salinity of 30 was added to the cylinder.

2.1.1. Experimental Instruments

A spectrophotometer (UV-2450, SHIMADZU, Kyoto, Japan), salinity indicator (SALscan20, BANTE instruments, Shanghai, China), and photometer (ST-80C, Beijing Shida Photoelectric Technology Co., Ltd., Beijing, China) were used. Some experiment utensils, such as volumetric flasks (250 mL, 2500 mL), graduated cylinders (50 mL, 500 mL), 1250 mL colorimetric tubes with stoppers, beakers (100 mL, 500 mL), brown reagent bottles (500 mL), polyethylene wash bottles (500 mL), transfer pipette (1 mL, 5 mL, 15 mL), and other common instruments and equipment in the laboratory were used for the culture. The chlorophyll fluorescence parameters were determined by using a modulated fluorometer Water-PAM (PAM-Water-ED, Walz, Germany).

2.1.2. Experimental Samples and Pre-Treatment

After the algal activity recovered, sundries such as insects, eggs of aquatic biota, other mixed algae, sandstone, etc., were removed under a stereoscopic microscope. Growth activity was regularly measured by a chlorophyll fluorescence instrument. The samples were carefully washed with a brush in tap water, then they were put back into the glass cylinder to conduct temporary aeration culture for 2 days. A few leftover leaves of samples were snipped using sterilized scissors, and the stolons were cut at random, ensuring that the terminal stolons were all longer than 3 cm. After that, the snipped terminal stolon was put back into the glass cylinder for 2 days of ventilation recovery. The activity of the sample was measured using a chlorophyll fluorescence meter, which met the experimental requirements.

2.2. Experimental Methods

2.2.1. Formulation for Culture Solution

The culture water used in this experiment was artificial seawater (EASW Medium) ([31]) (3 L) added with 0.8 mg (NH4)2SO4 and 0.5 mg NaNO2. An amount of 3 L of artificial seawater was filtrated by 0.45 μm filter membrane, sterilized by autoclave, then aerated with sterilized airstones for 24 h, and 0.8 mg (NH4)2SO4 and 0.5 mg NaNO2 were added. Finally, the initial pH of the artificial seawater was 8.18 and salinity was 30.6.

2.2.2. Experimental Scheme Design

One blank group (B) and six experimental groups (E1~E6) were set in triplicate (Table 1). Transparent plastic bottles were washed and rinsed with distilled water and then put in a draught cupboard to be air-dried. Each plastic bottle was added with 100 mL of artificial seawater. No sample was added to the blank group for measuring the initial concentrations of NH4-N and NO2-N in the artificial seawater. The temporary cultured terminal stolons mentioned above were put on etamine to remove water at the surface, and eighteen parts on average weighed from 0.248 to 0.258 g for the triplicates. Then, these terminal stolons were placed into the plastic bottles that were uniformly sealed with silver paper to prevent indoor NH4-N from entering the bottle and randomly tagged with labels from No.1 to No. 18. They were cultured in a light incubator at 25 °C at a light intensity of 1000 lux. During incubation, three plastic bottles with samples were randomly taken every four hours for water analysis. The concentration of the blank group (B) was measured in the first four hours. The filtering apparatus used was soaked in dilute hydrochloric acid to remove any possible remnant NH4-N (1:6) on the instrument. All of the water samples were filtrated by a 0.45 μm filter membrane.

2.2.3. Analytical Methods

NH4-N and NO2-N were measured by hypobromite oxidation and naphthalene ethylenediamine spectrophotometry as per China’s national standard GB 17378.4-2007 [32], for which reagents were configured and standard curves plotted. The concentrations of NH4-N and NO2-N were calculated according to the changes in the absorbance value of the cultured water.
The data were statistically analyzed using ANOVA and Duncan tests. Differences were defined significant if p < 0.05 and all the data were expressed as mean ± standard deviation (SD) (n = 3).

3. Results

3.1. Effect of Cultured Time Interval on NH4-N and NO2-N Concentrations

3.1.1. Effect of Cultured Time Interval on NH4-N Concentration

The NH4-N concentration of artificial seawater significantly decreased in the first 24 h after the terminal stolon was put into the artificial seawater (Figure 1). Except for groups E4 and E6, the longer the culture time intervals were, the more the concentrations decreased. The NH4-N concentration in the culture water was higher than that of the blank after the first four hours. When incubation time was extended to a 4-h dark period, such as that shown in group E4, the NH4-N concentrations were higher than those for the 12-h light period only. The minimum NH4-N concentration 0.02 mg/L occurred in the first 8 (E2) and 16 (E4) hours of the experiment. Interestingly, the data considerably varied among the triplicates of groups E1 and E2. NH4-N concentration in E1 exceeded the initial ones.

3.1.2. Effect of Cultured Time Interval on NO2-N Concentration

As Figure 1 shows, in the 24-h circadian rhythm, NO2-N concentration showed no significant change in the experiment group with light intervals, while it significantly decreased in the dark period. The longer the dark intervals were, the more the concentrations decreased. The lowest nitrous acid concentration was 0.07 mg/L, which appeared in 24 h of the experiment, and the value of NO2-N concentration in the parallel groups were very close to each other with small standard errors.

3.1.3. Effect of Culture Time Interval on Different Forms of Nitrogen Concentration

The variations between different forms of nitrogen concentration and culture time intervals were not synchronized. Changes in the concentration of NO2-N occurred later than that of NH4-N. The variation trends of NO2-N and NH4-N concentrations were different.

3.2. Effect of Culture Time Interval on NH4-N and NO2-N Removing Efficiency

3.2.1. Change in NO2-N Removing Efficiency

As shown in Figure 2, NO2-N removing efficiency was nearly zero in the light intervals. The longer the dark intervals were, the greater the NO2-N removing efficiency was. The highest NO2-N removing efficiency of the terminal stolon of samples was 9.24% in 24 h. Half of the removing efficiencies were negative and their culture time intervals were less than 12 h.

3.2.2. Change of NH4-N Removing Efficiency in Artificial Seawater

Figure 3 shows that the variation curve of NH4-N removing efficiency was saddle shaped. The longer the culture time intervals were, the greater the removing efficiencies were in the experimental groups during the light period. However, in the dark period, absorption time intervals existed, except for in group E5, which contained a 8-h dark period; the NH4-N removing efficiencies in the experimental groups E4 and E6 were less than those in E3. The highest NH4-N removing efficiency reached 71.38%.

3.2.3. The Correlation Degree in NO2-N– and NH4-N–Removing Efficiencies

The NO2-N removal efficiency was significantly lower than that of NH4-N. In addition, there was no significant correlation between them.

4. Discussion

4.1. Artificial Seawater

The use of artificial seawater in the experiment was to simplify the influencing factors and largely decrease the unknown factors. Using artificial seawater excluded the possibility of the input of nitrifying bacteria from natural seawater. Nitrifying bacteria are ubiquitous in nature, although their amount is very small. Studies have shown there are about 10,000 nitrifying bacteria per liter of seawater [33]. Problems such as superfluous baits and excrements, as well as very complexed nutrient compositions in aquaculture wastewater, could be avoided by using artificial seawater [34].

4.2. Initial Concentrations of NH4-N and NO2-N

In our experiment, the initial concentrations of NH4-N and NO2-N were 0.09 mg/L and 0.08 mg/L, respectively, and the inorganic nitrogen concentration of the artificial seawater was 0.09 mg/L, conforming to the first-class standard of China’s national seawater quality. Generally, NH4-N and NO2-N in concentrations below 0.2 mg/L and 0.1 mg/L, respectively, could not harm the breeding organisms [35,36]. Therefore, the artificial seawater used was below the eutrophication level of aquaculture wastewater.

4.3. Activity of Caulerpa taxifolia

The experimental material was the terminal stolon of C. taxifolia only, and did not include blades or rhizoids, and it was characterized by active quick growth and strong extension ability. At present, no method for the detection of the stolon’s activity has been reported before this study, to our best knowledge. Water-PAM (PAM-Water-ED, Walz, Germany) was used to measure the effect of photosynthesis. However, the fluorescence induction curve did not agree with those of common plants. The appearance activity of terminal stolon was observed under an anatomic microscope and judged by its toughness and hardness. Stolons of groups E1, E2, and E3 occurred in the 12-h light period, observed under a microscope. Results showed that they maintained good activity and some newborn protuberance appeared. In the 20-h (E5) and 24-h (E6) experimental groups in the dark cycle, some of the terminal stolons had whitening, cell lysis at the ends, and softening, especially in the last 24-h experimental group (E6). In particular, in the last 24 h (E6) of the experiment, two groups had serious algal bleaching, and the algae were obviously softened. The data of these two parallel groups of E6 were obviously abnormal. Their NH4-N concentration did not significantly decrease, while their NO2-N concentration obviously decreased (Figure 1). NH4-N concentrations of these two parallel groups were significantly higher than that of the 20-h group E5 (Figure 1). Therefore, we speculated that the terminal stolon of C. taxifolia not only absorbed NH4-N from waters as the raw material for its nutrient synthesis, but also discharged NH4-N into the waters. However, NO2-N concentrations showed the same results between the two parallels of E6, showing the same results and were the lowest among all groups of the experiment. There was no significant correlation between NO2-N absorption and algal activity.

4.4. Algal-Bacterial Symbiosis

Under natural conditions, bacteria and algae live together. It is unavoidable that algae themselves bring some bacteria, although the experimental materials were repeatedly washed with seawater and their impurities were removed. Reports have shown that symbiosis bacteria exist in the cytoplasm of Caulerpa species, and the bacterial species borne varies in different Caulerpa species [37]. NO2-N can be oxidized into nitric nitrogen by nitrate bacteria; in return, the energy released during the oxidation progress would support the metabolic activity of the bacteria, and the nitric nitrogen would be absorbed by algae, which promotes the growth of algae. The oxygen released from algal photosynthesis not only raised the concentration of dissolved oxygen in water, but also provided suitable growth and reaction conditions for aerobic nitrate bacteria, which ensured the sustainability of normal life activities and the reproduction of nitrate bacteria. Therefore, a 24-h experiment was designed to reduce the influence of nitrate bacteria by shortening the culture time. At the same time, the nitrate nitrogen interference caused by nitrate bacteria and the physiological preference of plants for nitrogen fertilizer types were also considered [21]; however, detection of the interference was not studied in this study for simplicity.

4.5. Mechanism of NH4-N and NO2-N Removal

In nitrogen cycling in seawater, ammonia nitrogen is oxidized into NO 2 − , and then NO 2 − is oxidized into NO 3 − . However, in this study, NH4-N concentration in seawater continually decreased, and NO2-N concentration also decreased (Figure 1). It indicates that the conversion of NH4-N into NO2-N in water was not the main method of removing NH4-N. The pH of waters gradually decreased because of algal respiration during the dark period, which inhibited the transformation of NH4-N into NH3; meanwhile, NH4-N continuously decreased in this period. The possibility of NH4-N removal can be excluded as a large amount of NH4-N in the water was transformed into NH3, and then NH3 evaporated into the air. Therefore, we believed that the terminal stolon of C. taxifolia had a significant removal effect on NH4-N in 24 h, as shown in this study.
As for the elevated NH4-N concentration we observed for the first time, it might be explained by the ammonia nitrogen released into waters from algae and which had just entered a new environment [38]. Later, NH4-N concentration in the water decreased, proving that algae significantly changed NH4-N concentration during the whole experiment. Possibly, the algae absorbed and turned NH4-N to their own composition, or evaporated NH4-N in the form of NH3 by changing the physicochemical properties of the water. In group E2, the NH4-N concentrations obtained were significantly lower than that of the blank group, illustrating that the algae began to remove NH4-N from the water after adapting to the new water environment. During the light period, the NH4-N concentration continually decreased and its removal efficiency continuously increased as the cultured time lasted.
Of course, factors cannot be excluded that resulted in measurement errors. For example, the healthy level of algal individuals determined by those small amounts of algal samples and the selected experimental region might have had a significant influence on the experimental results. Furthermore, it is also easy to bring in ammonia during the experiment operation. However, all of these factors fell into the systematic error range.
The NO2-N concentrations of the experimental groups did not significantly change during the light cultured period. However, after entering the dark period, the NO2-N concentrations decreased as the culture time lasted and were not affected by the activity of terminal stolon. Therefore, NO2-N concentration decreased with the lasting of the dark culture time, indicating that the decrease in NO2-N concentration was not caused by the absorption of terminal stolon.
The suitable pH value for the growth of nitrate bacteria ranges from 6.0–7.5 [39]. In this study, the initial pH value was 8.18, and the final pH value was 7.5, indicating that the seawater pH value continually decreased under persistent influence from the respiration of terminal stolon after entering the dark period. Gradually, the pH value was close to the optimum growth pH range of nitrate bacteria, and could promote the nitration reaction toward nitrate formation. NO2-N was continually transformed into nitric nitrogen, and thus, the NO2-N concentration decreased.

4.6. NH4-N Absorbency by Different Thallus Tissues

The material selected in this study was the terminal stolon of C. taxifolia. The terminal stolon used was the newborn part of C. taxifolia, without a rhizoid or erect branch. C. taxifolia contains different organizational parts, such as an erect branch, stolon, and a rhizoid system. Under natural conditions, the rhizoid system embraces many gravels or pebbles, which are the best habitat in which to enrich microbes. Just like halophytic vascular plants, C. taxifolia is capable of enhancing nitrogen fixation by releasing photosynthates into the rhizoid system [40]. Due to too much interference from abundant microorganisms, we could not explore their water quality remediation capacity. C. prolifera has been reported as a nitrophilous algae that is able to take nutrients through terminal stolon, and thus, the biomass of stolon can increase most significantly in low nitrogen conditions [41]. In this study, similar results were obtained by using the terminal stolon alone, and it was proved that terminal stolon without rhizoid systems have a strong absorption capacity of NH4-N. As an invasive species, thalli of C. taxifolia often form a large area of algal mat, which can hold abundant organic matter and low concentrations of dissolved oxygen. The low oxygen environment could lead to a lower denitrification efficiency; the NH4-N into the water would increase, and the nitrogen element into the air in nitrified and denitrified forms would decrease [42]. The terminal stolons used in this experiment were separate from the root, obtaining high concentrations of dissolved oxygen but poor organic matter, unlike its natural conditions. Moreover, they showed higher nitrification efficiency in the experimental period. At a certain nutrient concentration, the nutrition absorption rate of the thallus usually has a positive correlation with the surface area of per unit seaweed biomass [43]. The terminal stolon was the only experimental material used in this study. However, under natural conditions, C. taxifolia can generate abundant erect branches. Therefore, its surface area per unit of biomass is greater than other seaweed species, thus having a stronger removal efficiency of NH4-N and NO2-N. To ensure the same weight in each experimental group and to explore the removal ability of eugonic terminal stolon, this experiment cut off the stolons. Although they had been recovered two days in advance, the interference of enhanced respiration and injury response to the experimental data could be avoided.

4.7. Light Influx and Dark Efflux of NH4-N

This study indicates that the NH4-N concentration gradually decreased with an extension of the light period (Figure 3). However, the NH4-N concentration of group E4 with a 12-h light period and a 4-h dark period was lower than that of group E3, which had a 12-h light period only (Figure 3). Generally speaking, the NH4-N concentration of seawater rises at nighttime and falls in the daytime in a natural coastal area, whether the seafloor is covered with Caulerpa or not [44]. In this study, similar results were obtained, which illustrated that the NH4-N secretion from terminal stolon of C. taxifolia might take place in the absence of light.

4.8. Dark Influx of NO2-N

As shown in this study, NO2-N almost did not influx into C. taxifolia during the light period, but did in a gradual way the dark period (Figure 2), probably due to characteristic algal-bacterial symbiosis. According to previous reports, nitrate bacteria have a lucifugal effect in natural conditions, and the activity of nitrate bacteria can gradually resume as long as the ray of light is attenuated [45]. The suitable pH range for nitrate bacteria is 6.0–7.5 [39]. During the dark period, the respiration of the terminal stolon causes a gradual decrease in pH value to a suitable pH point for nitrate bacteria proliferation. With the gradual increase in nitrification rate, NO2-N continuously inflows into the algal-bacterial symbiosis.

4.9. Correlation between NH4-N Removing Efficiency and NO2-N Removing Efficiency

Under the same conditions, there was no correlation between NH4-N removal and NO2-N removal. However, NH4-N was more preferentially removed (Figure 2 and Figure 3), which is physiologically consistent with the rule that plants preferentially absorb NH4-N [21].

5. Conclusions

Obviously, the terminal stolon of Caulerpa taxifolia is proven to be capable of effective NH4-N removal, and also has strong NO2-N regulation ability. Therefore, Caulerpa taxifolia have great application potential in wastewater treatment and pollution remediation.

Author Contributions

Conceptualization, L.D.; methodology, B.H.; validation, B.H.; formal analysis, Z.W.; investigation, B.H., Z.W., Y.C. and L.D.; resources, B.H.; data curation, Z.W. and Y.C.; writing—original draft preparation, B.H. and Z.W.; writing—review and editing, L.D.; supervision, L.D.; project administration, B.H.; funding acquisition, B.H. and L.D. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China, grant numbers 31970216 and 32270219.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

The authors are grateful to Shirley Humphrey (USA), English Lecturer at Shantou University, for the revision of the manuscript. Sincere thanks are due to Shanwen CHENG, and Weizhou CHENG for their kind laboratory technical assistance and transportation of material. Sincere gratitude should be extended to Yi CHEN, Lingzhao ZENG and other students in the laboratory for their help.

Conflicts of Interest

The authors declare no conflict of interest.

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Jmse 11 00043 g001 550
Figure 1. Effect of culture time interval on NH4 -N and NO2-N concentrations in seawater. Data are means ± SD (n = 3). Asterisk signs (*, **, and ***) indicate significant differences at the 0.05, 0.01, and 0.001 levels.
Figure 1. Effect of culture time interval on NH4 -N and NO2-N concentrations in seawater. Data are means ± SD (n = 3). Asterisk signs (*, **, and ***) indicate significant differences at the 0.05, 0.01, and 0.001 levels.
Jmse 11 00043 g001
Jmse 11 00043 g002 550
Figure 2. Effect of culture time interval on NO2-N removing efficiency. Data are means ± SD (n = 3). Asterisk sign (***) indicates significant differences at the 0.001 level.
Figure 2. Effect of culture time interval on NO2-N removing efficiency. Data are means ± SD (n = 3). Asterisk sign (***) indicates significant differences at the 0.001 level.
Jmse 11 00043 g002
Jmse 11 00043 g003 550
Figure 3. Effect of culture time interval on NH4-N removing efficiency. Data are means ± SD (n = 3). Asterisk sign (*) indicates significant differences at the 0.05 level.
Figure 3. Effect of culture time interval on NH4-N removing efficiency. Data are means ± SD (n = 3). Asterisk sign (*) indicates significant differences at the 0.05 level.
Jmse 11 00043 g003
Table
Table 1. Experimental scheme.
Table 1. Experimental scheme.
GroupCKExperiment
B0E1E2E3E4E5E6
Light PeriodDark Period
Culture time interval/h44812162024
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Huang, B.; Wang, Z.; Chu, Y.; Ding, L. Investigating the Role of Terminal Stolon of Marine Invasive Green Macroalga Caulerpa taxifolia in the Removal of Inorganic Nitrogen from Seawater. J. Mar. Sci. Eng. 2023, 11, 43. https://doi.org/10.3390/jmse11010043

AMA Style

Huang B, Wang Z, Chu Y, Ding L. Investigating the Role of Terminal Stolon of Marine Invasive Green Macroalga Caulerpa taxifolia in the Removal of Inorganic Nitrogen from Seawater. Journal of Marine Science and Engineering. 2023; 11(1):43. https://doi.org/10.3390/jmse11010043

Chicago/Turabian Style

Huang, Bingxin, Zhan Wang, Yue Chu, and Lanping Ding. 2023. "Investigating the Role of Terminal Stolon of Marine Invasive Green Macroalga Caulerpa taxifolia in the Removal of Inorganic Nitrogen from Seawater" Journal of Marine Science and Engineering 11, no. 1: 43. https://doi.org/10.3390/jmse11010043

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