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Article

Effects of Desiccation, Water Velocity, and Nitrogen Limitation on the Growth and Nutrient Removal of Neoporphyra haitanensis and Neoporphyra dentata (Bangiales, Rhodophyta)

by
Jingyu Li
1,2,
Guohua Cui
1,
Yan Liu
1,2,
Qiaohan Wang
1,2,
Qingli Gong
1,2 and
Xu Gao
1,2,*
1
Fisheries College, Ocean University of China, Qingdao 266003, China
2
Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao 266003, China
*
Author to whom correspondence should be addressed.
Water 2021, 13(19), 2745; https://doi.org/10.3390/w13192745
Submission received: 10 September 2021 / Revised: 26 September 2021 / Accepted: 27 September 2021 / Published: 2 October 2021
(This article belongs to the Special Issue Advances in Aquaculture Ecology Research)
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Abstract

:
Seaweeds have been verified to effectively reduce the nutrients of aquaculture wastewater, and to increase the economic output when commercially valuable species are utilized. Pyropia/Porphyra/Neopyropia/Neoporphyra species are important seafood resources globally, and their growth and bioremediation capacities are affected by diverse biotic and abiotic stressors. In this study, we investigated the effects of desiccation (0, 1, 2, 4, and 6 h of air exposure), water velocity (0.1, 0.2, and 0.5 m s−1), and the nitrogen limitation period (1, 2, and 3 d) on the relative growth rates (RGR) and nutrient removal rates of Neoporphyra haitanensis and Neoporphyra dentata. The RGRs and NO3-N removal rates of the two species decreased significantly with increasing desiccation periods. A higher water velocity of 0.5 m s−1 had a greater negative impact on the RGRs and NO3-N and PO4-P removal rates than 0.1 and 0.2 m s−1. N. haitanensis exhibited a greater tolerance to water motion than N. dentata. Additionally, the RGRs and NO3-N and PO4-P removal rates were significantly different among the nitrogen limitation periods. N. haitanensis and N. dentata exhibited different nitrogen usage strategies after nitrogen limitation and recovery. These results provide valuable information relating to the excessive nutrient removal from aquaculture wastewater by Neoporphyra species.

1. Introduction

Aquaculture was one of the fastest-growing commercial activities in the last few decades. The production of marine organisms has broken historical records, reaching 114.5 million tonnes in 2018 [1]. In terms of the increasing storage of natural resources, the recirculating aquaculture system (RAS) has become one of the most sustainable models of marine animal aquaculture [2,3,4]. Due to high density cultivation with limited volumes of seawater, the wastewater from RAS usually contains high concentrations of nutrients, posing a potential risk to the surrounding environment [3,5,6]. Much research has been performed to look for bioremediation technologies that could solve this problem and ensure its environmental sustainability [7,8,9]. Recently, due to their low cost and high uptake efficiency, seaweeds have become a feasible alternative in the bioremediation of eutrophic wastewater [10,11,12]. It is very critical to select appropriate seaweed species with great nutrient demands and high economic value for RAS.
Intertidal seaweeds are subjected to cyclical immersion and emersion because of their periodic exposure to tidal fluctuations. During low tide, the intertidal seaweeds are exposed to air and experience various environmental stresses, such as drastic temperature shifts, high osmotic pressure, and desiccation [13,14,15]. Desiccation with different periods and frequencies is unavoidable for seaweeds growing in different vertical zones, and their physiological and metabolic activities, including growth and nutrient assimilation, are significantly affected [16,17,18]. Besides desiccation, water velocity is another important abiotic factor affecting the metabolism of seaweeds [15,19]. Adverse hydrodynamic conditions in the sea can produce different degrees of influences on the productivity of natural and cultivated seaweeds, which depends on their different environmental tolerances and nutrient utilization performances [20,21,22,23]. Similarly, under laboratory conditions, the growth and nutrient uptake of diverse seaweed species have been identified to be significantly inhibited by immoderate water velocity [24,25].
Moreover, the nutrient uptake and growth of seaweeds are greatly affected by diverse biotic factors, including the species, competition, growth phase, and nitrogen level in the algae [15,26,27]. Nitrogen and phosphorus are two essential nutrient components to be incorporated into physiological compounds that are crucial for seaweed growth and development [28]. In recent years, ambient nitrogen deficiency has been reported to cause aggravated damage to the seaweed mariculture systems due to the reduced environmental tolerance of algae caused by an undesirable internal nutrient status [29,30,31]. Nevertheless, as a physiological strategy in response to nutrient deprivation, it was found that the nitrogen uptake ability of seaweeds was enhanced under the condition of nitrogen limitation [32,33,34], and was positively associated with the degree of nitrogen limitation [35]. Therefore, the assessment of the potential of nitrogen limitation in aquaculture water purification with seaweeds is considered to have significant ecological and commercial values.
Macroalgae of the genus Neoporphyra are considered edible, delicious and nutritious, and were recently separated from the genus Porphyra [36]. Neoporphyra species are important commercially available marine crops in China, and have been massively cultivated because of great demand [17,37,38]. Due to their extremely high surface area to volume ratio, they are capable of the rapid assimilation of nutrients, which promotes high rates of growth in these algae [39,40,41]. As a result, they have been proven to contribute to the purification of seawater in aquaculture ponds and nearshore farming areas in China, with total nitrogen and PO4-P removal rates of 65.8–80.2% and 71.1–84.6% [42,43]. These facts suggest that this genus is one of the most promising candidates for bioremediation and integrated aquaculture [40,41,44].
Neoporphyrahaitanensis and Neoporphyra dentata are two common Pyropia species inhabiting the intertidal zone of rocky shores along the coast of southern China [45]. Their optimal temperature ranges for growth are 19–23 °C and 17–23 °C, respectively [46,47], which are generally consistent with the cultivation temperature of economic marine animals such as turbot and grouper [48,49]. These provide advantageous conditions for aquaculture wastewater purification using these two species. As one of the major commercial species, N. haitanensis has received extensive attention for its physiological and metabolic responses to biotic and abiotic stressors for aquaculture production optimization [50,51,52,53,54]. N. dentata is a promising species for cultivation in South China, and has been farmed on an experimental scale over the past few years [46,47,55]. Nevertheless, the nutrient removal capacities and potential application in aquaculture wastewater purification have been rarely investigated in these species. Furthermore, it is very vital to understand the correlation between the nutrient removal capacities and diverse biotic and abiotic factors.
In the present study, three short-term laboratory experiments were conducted to investigate the respective effects of desiccation, water velocity and nitrogen limitation on the growth and NO3-N and PO4-P removal of N. haitanensis and N. dentata. The results of this study are expected to provide valuable information to improve aquaculture wastewater management and to assess the bioremediation potential of these two high-valued cultivars in China.

2. Materials and Methods

2.1. Sample Collection and Maintenance

Gametophytic thalli of N. haitanensis and N. dentata were collected from cultivated populations on Nanao Island, Guangdong, China (23°28′ N, 117°06′ E) in December 2018. These samples were rinsed several times with filtered seawater to remove epiphytic organisms and detritus. The surface seawater temperature at the sampling site was measured at the same time. The samples were promptly transported to the laboratory under low-temperature conditions. Healthy thalli were then selected and cultured in several plastic tanks containing sterilized seawater. For the subsequent experiments, these thalli were maintained at 23 °C (the surface seawater temperature at the sampling site), with an irradiance of 100 µmol photon m–2 s–1 and a 12:12-h light/dark cycle for 2 days.

2.2. Desiccation Experiment

A culture experiment was conducted over a period of 4 days after five periods of desiccation: 0, 1, 2, 4, and 6 h of air exposure. The water loss percentages of N. haitanensis and N. dentata were 34.4% and 41.4% after 1 h of desiccation, 55.2% and 59.2% after 2 h of desiccation, 70.5% and 71.9% after 4 h of desiccation, and 77.6% and 81.2% after 6 h of desiccation, respectively. There were a total of 10 experimental treatments for each species, and each treatment was performed in three replicates. Before the culturing, 5 g thalli were randomly selected for each replicate. After being blotted dry, those thalli at 1–6 h of desiccation treatments were transferred into autoclaved Petri dishes (10 cm in diameter) containing a layer of gauze soaked with a small amount of culture medium (NO3-N: 50 mg L−1; PO4-P: 5 mg L−1), which was made using a nutrient solution and sterilized seawater from the coast of Taipingjiao, Qingdao, with a salinity of approximately 31 psu. Next, these Petri dishes were placed into incubators at 23 °C for 1, 2, 4, and 6 h, respectively. After desiccation, the thalli of each replicate were moved into a side-arm flask with 500 mL culture medium and GeO2, which were then gently aerated. During this experiment, a temperature of 23 °C, a 12:12-h light/dark cycle, and an irradiance of 100 μmol photon m–2 s–1 were maintained.
The fresh weights of all of the thalli before and after the experiment were measured after removing excess seawater on the surface. The relative growth rate (RGR; % day–1) of each replicate was calculated using the following Equation (1):
RGR (% day–1) = 100 × (ln Wt – ln Wo)/t
where Wo is the initial fresh weight, Wt is the final fresh weight, and t is the time of the culture in days.
For all of the treatments, the culture media before and after the experiment were separately collected, and the concentrations of NO3-N and PO4-P were analyzed using the cadmium column reduction method and the phosphomolybdenum blue spectrophotometric method, respectively [56,57]. The removal rates of NO3-N and PO4-P were estimated using the following Equation (2):
RN, P = (C0−C4)/C0 × 100%
where RN, P are the removal rates of NO3-N and PO4-P (%); C0 is the initial concentration of NO3-N and PO4-P (mg L−1); and C4 is the final concentration of NO3-N and PO4-P (mg L−1) after 4 days.

2.3. Water Velocity Experiment

In order to examine the effect of the water velocity on the growth and nutrient removal of these two species, they were cultured for 4 days at three water velocities (0.1, 0.2, and 0.5 m s−1) with three replicates. For this experiment, a total of 18 side-arm flasks were prepared, and each contained 500 mL culture medium with GeO2 and 5 g thalli. During the experimental period, a temperature of 23 °C, a 12:12-h light/dark cycle, and an irradiance of 100 μmol photon m–2 s–1 were maintained. At the end of this experiment, the calculations of the RGR and the removal rates of NO3-N and PO4-P were the same as for the desiccation experiment.

2.4. Nitrogen Limitation Experiment

In order to investigate the effect of nitrogen limitation on the growth and nutrient removal of these two species, a total of 18 side-arm flasks including three replicates for each treatment were prepared. Each flask contained 500 mL culture medium with GeO2 and 5 g thalli. These two species were incubated for 4 days after three different periods of nitrogen limitation (1, 2, and 3 day). We used nitrogen-deficient seawater (NO3-N: 5 mg L−1) to achieve different nitrogen levels in the algae. During the 4-day experiment, a temperature of 23 °C, a 12:12-h light/dark cycle, and an irradiance of 100 μmol photon m–2 s–1 were maintained. The RGR and removal rates of NO3-N and PO4-P were calculated in the same way as described above.

2.5. Statistical Analysis

Two-way analysis of variances (ANOVA) were used to analyze the effects of desiccation and the species, water velocity and the species, and nitrogen limitation and the species on the RGR and NO3-N and PO4-P removal rates. Prior to the ANOVA tests, all of the data were confirmed to show a normal distribution and homogeneity of variance. When a significant difference was identified by the ANOVA, Tukey’s multiple comparisons test was used to determine which levels of each factor produced significant differences (p < 0.05). All of the analyses were performed using STATISTICA version 7.0 software.

3. Results

3.1. Effect of Desiccation on Growth and Nutrient Removal

The results of the two-way ANOVA showed that the RGRs of N. haitanensis and N. dentata were significantly affected by desiccation, but they did not significantly differ between the two species (Figure 1; Table 1). A significant interaction between desiccation and the species was not detected. The RGRs of the two species decreased significantly with increasing desiccation periods from 0 to 6 h.
The NO3-N removal rates of N. haitanensis and N. dentata were significantly affected by desiccation, but they did not significantly differ between the two species. A significant interaction between desiccation and the species was detected. The NO3-N removal rates of N. haitanensis and N. dentata decreased significantly with increasing desiccation periods, with ranges of 87.2–72.4% and 89.2–67.1%, respectively.
The PO4-P removal rates of N. haitanensis and N. dentata were not significantly affected by desiccation, and also did not significantly differ between the two species. A significant interaction between desiccation and the species was not detected. The PO4-P removal rates of N. haitanensis and N. dentata ranged from 88.9 to 98.0%, and from 90.9 to 98.2%, respectively.

3.2. Effect of the Water Velocity on Growth and Nutrient Removal

The RGRs of N. haitanensis and N. dentata were significantly affected by the water velocity, and also differed significantly between the two species (Figure 2; Table 2). A significant interaction between the water velocity and species was detected. The RGRs of N. haitanensis and N. dentata at 0.1 and 0.2 m s−1 were significantly greater than those at 0.5 m s−1. The RGR of N. dentata at 0.2 m s−1 was significantly greater than that at 0.1 m s−1. The RGRs of N. haitanensis were significantly greater than those of N. dentata at all three water velocities.
The NO3-N removal rates of N. haitanensis and N. dentata were significantly affected by the water velocity, but they did not significantly differ between the two species. A significant interaction between the water velocity and species was detected. The NO3-N removal rates of N. haitanensis and N. dentata at 0.1 (N. haitanensis: 86.2%; N. dentata: 80.5%) and 0.2 m s−1 (N. haitanensis: 83.7%; N. dentata: 89.9%) were significantly greater than those at 0.5 m s−1 (N. haitanensis: 44.6%; N. dentata: 48.4%). There were no significant differences in the NO3-N removal rates between 0.1 and 0.2 m s−1 for both species.
The PO4-P removal rates of N. haitanensis and N. dentata were significantly affected by the water velocity, and also differed significantly between the two species. A significant interaction between the water velocity and species was detected. The PO4-P removal rate of N. haitanensis at 0.1 m s−1 (86.9%) was significantly greater than those at 0.2 (70.3%) and 0.5 m s−1 (64.8%). The PO4-P removal rates of N. dentata at 0.1 (62.4%) and 0.2 m s−1 (65.9%) were significantly greater than that at 0.5 m s−1 (45.4%). The PO4-P removal rate of N. haitanensis was significantly greater than those of N. dentata at 0.1 and 0.5 m s−1.

3.3. Effect of Nitrogen Limitation on Growth and Nutrient Removal

The RGRs of N. haitanensis and N. dentata were significantly affected by nitrogen limitation, and also differed significantly between the two species (Figure 3; Table 3). A significant interaction between nitrogen limitation and the species was detected. After 4 day nitrogen recovery, the RGRs of N. haitanensis at 2 and 3 day nitrogen limitation were significantly greater than that at 1 day nitrogen limitation. There were no significant differences in the RGRs among the three nitrogen limitation levels for N. dentata. The RGR of P. dentata was significantly greater than that of N. haitanensis at each nitrogen limitation level.
The NO3-N removal rates of N. haitanensis and N. dentata were significantly affected by nitrogen limitation, but they did not significantly differ between the two species. A significant interaction between nitrogen limitation and species was detected. After 4 day nitrogen recovery, the NO3-N removal rate of N. haitanensis at 3 day of nitrogen limitation (91.8%) was significantly greater than those at 1 day (78.4%) and 2 day of nitrogen limitation (80.0%). The NO3-N removal rate of N. dentata increased significantly from 1 to 3 day nitrogen limitation (1 day: 72.9%; 2 day: 82.0%; 3 day: 93.3%).
The PO4-P removal rates of N. haitanensis and N. dentata were significantly affected by nitrogen limitation, and differed significantly between the two species. A significant interaction between nitrogen limitation and the species was detected. After 4 day of nitrogen recovery, the PO4-P removal rate of N. haitanensis at 1 day of nitrogen limitation (80.3%) was significantly greater than those at 2 (64.4%) and 3 day of nitrogen limitation (59.5%). The PO4-P removal rates of N. dentata at 1 (68.9%) and 2 day of nitrogen limitation (62.4%) were significantly greater than that at 3 day of nitrogen limitation (48.3%). The PO4-P removal rates of N. haitanensis were significantly greater than those of N. dentata at 1 and 3 day of nitrogen limitation.

4. Discussion

Intertidal seaweeds usually experienced the stress of desiccation with different periods originating from tidal alternation because they are essentially marine organisms [15,16]. Several studies have demonstrated that desiccation significantly affects the growth and nutrient uptake of Neoporphyra species under laboratory conditions [17,18]. Similarly, in the present study, we found that different degrees of desiccation exhibited a significant inhibitory effect on the growth and nitrogen removal of N. haitanensis and N. dentata. This inhibitory effect intensified significantly with the increase of the desiccation period. This finding is supported by Cao et al. [58], showing that, due to the artificial reduction of the air exposure period, the thalli of Neoporphyra yezoensis (formerly Pyropia yezoensis) from cultivated populations were significantly larger than those from wild populations in the surrounding area. Li et al. [18] also documented that periodical dehydration could reduce the relative growth rate of N. yezoensis by 7–10% in different salinity conditions. However, the effects of desiccation on the growth and nutrient uptake of seaweeds varied from species to species, which is coordinated with their vertical distribution patterns [16,59,60]. Thomas et al. [61] found that the upper-shore species Pelvetiopsis limitata and Fucus distichus (Phaeophyceae) achieved their maximum nitrate uptake following severe desiccation that inhibited the nitrate uptake in the low-shore species Gracilaria pacififica (Rhodophyta). Kim et al. [16] suggested that species in the intertidal zone that have longer exposure times may have a higher time-use efficiency than subtidal species in terms of their nitrate uptake and growth. On the other hand, the impact of desiccation on seaweeds appears to be associated with their water-retaining abilities caused by structure features. For example, desiccation appeared to have no significant influences on the growth and photosynthesis of Ulva linza (Chlorophyta) and Gloiopeltis furcata (Rhodophyta) because of their internal hollow cavities being conductive to water retention [60,62]. The two Neoporphyra species used in this study are monolayer or bilayer membranous thalli with a weak water-retaining capacity, which may partially contribute to the inhibition of nutrient removal under desiccation stress.
Although the water loss percentages of the two experimental species in this study were as high as approximately 80% after 6 h of desiccation, they were still alive. After a 96-h culture, both species effectively recovered the capacity of nutrient absorption. Particularly, the removal rates of PO4-P were not significantly different among the desiccation periods from 0 to 6 h. These results suggest that N. haitanensis and N. dentata possess extremely strong resilience to high desiccation stress, and thus can adapt well to changeable oceanic conditions. Similarly, Gao and Wang [63] examined the effect of single dehydration on the physiological features of N. yezoensis, and found that the photosynthetic activity of N. yezoensis that lost 86% of its cellular water could be fully restored after 30 min of re-hydration. Therefore, the periodical emersion of seeded nets has been widely applied in Pyropia/Neopyropia/Neoporphyra field aquaculture to kill most fouling organisms, including diatoms and macroalgal spores [64]. Additionally, N. dentata appears to be slightly more sensitive to desiccation stress than N. haitanensis, even though their vertical distribution ranges are similar [45]. This may be closely associated with the fact that N. haitanensis has a thicker thallus (65–110 μm) with local double-layer cell tissue, whereas N. dentata only has a very thin single-layer thallus (30–55 μm) [45,65].
Water motion is a critical physical process in the marine environment that can transport the inorganic carbon and nutrients required for the growth and survival of marine macrophytes [66]. It has been demonstrated that an increased water velocity can reduce the diffusion boundary layer along the algae surface, and can thereby enhance its nutrient uptake and growth until a saturating velocity is reached [67,68]. Nevertheless, in this study, the growth of N. dentata exhibited a significant increase from 0.1 to 0.2 m s−1, but was significantly inhibited at 0.5 m s−1. Similarly, N. haitanensis had a significant lower RGR at 0.5 m s−1 compared with lower water velocities. Their removal capacities of NO3-N and PO4-P were also inhibited at a high water velocity of 0.5 m s−1. Analogous growth and physiological inhibition caused by an over-high water velocity has also been reported for the brown algae Laminaria digitata and Sargassum siliquastrum (Phaeophyceae) [68,69]. Furthermore, Yang [70] found a clear inverse correlation between the cell growth and chlorophyll synthesis of Chlorella (Chlorophyta) species and water velocity. All of these results suggested that over-high water velocity can greatly restrict the photosynthetic and nutrient accumulation activities of algae, and can even cause direct damage to algae membranes. Furthermore, N. haitanensis appeared to exhibit a greater tolerance and less sensitivity to variable hydrodynamic conditions than N. dentata. This may still be correlated with their different structure traits. It is conceivable that thicker and more solid algae can better resist the negative impact of external forces.
In seaweed species, nitrogen can be accumulated for growth demands and stored in its inorganic form in the cellular reserve pool [15,19]. As an ecological adaption to nitrogen deficiency stress, stored nitrogen can be remobilized to support seaweed survival without an ongoing inorganic nitrogen supply [33,71]. Their physiological and metabolic activities, including growth, photosynthesis, and protein and nucleic acid synthesis, will be suppressed by nitrogen deficiency below the critical concentration [72,73]. However, nitrogen replenishment quickly reverted the nitrogen accumulation and metabolism of algae, with the reestablishment of the nitrogen reserve pool and growth promotion [33,50,74]. In this study, the nitrogen removal capacities of both species after nitrogen recovery were positively correlated with the nitrogen limitation period, exhibiting a compensatory response in nitrogen accumulation. Similar phenomena have been documented for floating Sargassum horneri (Phaeophyceae) and Agarophyton tenuistipitatum (formerly Gracilaria tenuistipitata) (Rhodophyta), showing that nitrogen limitation and then recovery significantly increased their ammonium uptake rates in comparison with a control without nitrogen limitation [34,75]. These results suggest that nitrogen limitation can lead to a deficit status of the nitrogen reserve pool. In an effort to maintain life and restore health, the algae in worse conditions must possess a stronger ability to replenish nitrogen when subjected to nitrogen resupply. Curiously, the phosphorus removal in both species did not show the compensatory responses consistent with nitrogen removal. As we known, in seaweed species, there are interactions among different nutrients, which are required in a certain ratio [19]. Perini and Bracken [76] confirmed that nitrogen availability may mediate the ability of marine primary producers to access phosphorus. Therefore, we suspect that particularly rapid nitrogen accumulation may have a negative effect on phosphorus accumulation, which is supported by a finding regarding the phosphorus absorption inhibition by an ambient high nitrogen concentration in Skeletonema costatum (Bacillariophyta) [77]. Further studies should be carried out to test our hypothesis.
Under the same nitrogen limitation and recovery conditions, N. haitanensis and N. dentata showed similar NO3-N removal rates, whereas the RGRs of N. haitanensis were significantly lower than those of N. dentata. Liu et al. [74] demonstrated that nitrogen deprivation and then recovery notably promoted the growth of Asparagus schoberioides (formerly Gracilaria lemaneiformis) (Rhodophyta), but significantly inhibited the accumulation of phycoerythrin and chlorophyll a. In contrast, Friedlander et al. [78] reported that after nitrogen limitation and recovery, although the external nitrogen concentration was sufficient, Gracilaria conferta (Rhodophyta) did not grow significantly, probably due to more internal organic synthesis. All of these findings suggest that seaweeds under nitrogen starvation show a species-specific nitrogen utilization strategy when encountering nitrogen resupply. As mentioned above, in comparison with N. dentata, N. haitanensis with a thicker thallus and more complex structure appears to require more nitrogen resources for the synthesis of the necessary organic compounds rather than growth, resulting in the significantly lower RGR and deeper color observed in our experiment.

5. Conclusions

Dealing with eutrophic wastewater is a major challenge for aquaculture production and water environment protection. According to the data of this study, N. haitanensis and N. dentata appear to play an important role in the removal of inorganic nitrogen and phosphorus from aquaculture wastewater, and therefore are likely to be used as efficient and environmentally friendly remediation tools. N. dentata is a more ideal candidate because of its greater environmental resistance. Our results show that desiccation, water velocity and nitrogen limitation are three significant variables affecting the growth and nutrient removal of both species. N. haitanensis and N. dentata showed different nitrogen usage strategies after nitrogen limitation and recovery. These findings provide valuable information for developing and improving wastewater treatment technologies for RAS. Moreover, apart from being a biological filter, these two Neoporphyra species can be harvested as aquaculture byproducts to increase economic income owing to their excellent growth capacities. Due to the limited physiological data in this study, further experiments measuring multiple parameters are warranted to comprehensively assess the application feasibility of wastewater purification using Neoporphyra species.

Author Contributions

Conceptualization, methodology, and writing—original draft preparation, J.L. and X.G.; writing—review and checking, X.G.; data curation, project administration, and funding acquisition, J.L.; investigation, G.C. and Y.L.; validation and resources, Q.G.; formal analysis, J.L. and Q.W. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financially supported by the National Key R&D Program of China (No. 2020YFD0900201).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data of this study are available from the corresponding author upon reasonable request.

Acknowledgments

We are grateful to Weizhou Chen of Shantou University for providing N. haitanensis and N. dentata as the experimental materials.

Conflicts of Interest

The authors declare no conflict of interest.

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Water 13 02745 g001 550
Figure 1. The RGRs and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata cultured for 4 days under five desiccation periods. Different capital and small letters indicate statistical significance (P < 0.05) among species and desiccation periods, respectively. The data represent the mean ± SE (n = 3 replicates).
Figure 1. The RGRs and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata cultured for 4 days under five desiccation periods. Different capital and small letters indicate statistical significance (P < 0.05) among species and desiccation periods, respectively. The data represent the mean ± SE (n = 3 replicates).
Water 13 02745 g001
Water 13 02745 g002 550
Figure 2. The RGRs and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata cultured for 4 days under three water velocities. Different capital and small letters indicate statistical significance (P < 0.05) among species and water velocities, respectively. The data represent the mean ± SE (n = 3 replicates).
Figure 2. The RGRs and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata cultured for 4 days under three water velocities. Different capital and small letters indicate statistical significance (P < 0.05) among species and water velocities, respectively. The data represent the mean ± SE (n = 3 replicates).
Water 13 02745 g002
Water 13 02745 g003 550
Figure 3. The RGRs and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata cultured for 4 days after three different periods of nitrogen limitation. Different capital and small letters indicate statistical significance (P < 0.05) among species and nitrogen limitation periods, respectively.The data represents the mean ± SE (n = 3 replicates).
Figure 3. The RGRs and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata cultured for 4 days after three different periods of nitrogen limitation. Different capital and small letters indicate statistical significance (P < 0.05) among species and nitrogen limitation periods, respectively.The data represents the mean ± SE (n = 3 replicates).
Water 13 02745 g003
Table
Table 1. Analysis of variance (two-way ANOVA) examining the effects of desiccation on the RGR and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata, and the comparison of these parameters between the two species.
Table 1. Analysis of variance (two-way ANOVA) examining the effects of desiccation on the RGR and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata, and the comparison of these parameters between the two species.
FactorsdfFP
RGR
 Desiccation (D)45.973<0.01
 Species (S)11.1870.346
 Interaction (D × S)40.8512.061
NO3-N removal rate
 Desiccation (D)416.177<0.001
 Species (S)11.4650.239
 Interaction (D × S)42.935<0.05
PO4-P removal rate
 Desiccation (D)40.8342.947
 Species (S)11.1810.385
 Interaction (D × S)40.6556.421
Table
Table 2. Analysis of variance (two-way ANOVA) examining the effects of the water velocity on the RGR and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata, and the comparison of these parameters between the two species.
Table 2. Analysis of variance (two-way ANOVA) examining the effects of the water velocity on the RGR and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata, and the comparison of these parameters between the two species.
FactorsdfFP
RGR
 Water velocity (W)229.933<0.001
 Species (S)116.025<0.001
 Interaction (W × S)227.251<0.001
NO3-N removal rate
 Water velocity (W)220.070<0.001
 Species (S)10.7734.197
 Interaction (W × S)25.773<0.01
PO4-P removal rate
 Water velocity (W)218.191<0.001
 Species (S)19.966<0.001
 Interaction (W × S)211.555<0.001
Table
Table 3. Analysis of variance (two-way ANOVA) examining the effects of nitrogen limitation on the RGR and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata, and the comparison of these parameters between the two species.
Table 3. Analysis of variance (two-way ANOVA) examining the effects of nitrogen limitation on the RGR and NO3-N and PO4-P removal rates of N. haitanensis and N. dentata, and the comparison of these parameters between the two species.
Factors dfFP
RGR
 Nitrogen limitation (N)25.190<0.01
 Species (S)125.021<0.001
 Interaction (N × S)219.201<0.001
NO3-N removal rate
 Nitrogen limitation (N)223.876<0.001
 Species (S)10.4829.110
 Interaction (N × S)215.766<0.001
PO4-P removal rate
 Nitrogen limitation (N)228.171<0.001
 Species (S)18.960<0.001
 Interaction (N × S)212.095<0.001
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Li, J.; Cui, G.; Liu, Y.; Wang, Q.; Gong, Q.; Gao, X. Effects of Desiccation, Water Velocity, and Nitrogen Limitation on the Growth and Nutrient Removal of Neoporphyra haitanensis and Neoporphyra dentata (Bangiales, Rhodophyta). Water 2021, 13, 2745. https://doi.org/10.3390/w13192745

AMA Style

Li J, Cui G, Liu Y, Wang Q, Gong Q, Gao X. Effects of Desiccation, Water Velocity, and Nitrogen Limitation on the Growth and Nutrient Removal of Neoporphyra haitanensis and Neoporphyra dentata (Bangiales, Rhodophyta). Water. 2021; 13(19):2745. https://doi.org/10.3390/w13192745

Chicago/Turabian Style

Li, Jingyu, Guohua Cui, Yan Liu, Qiaohan Wang, Qingli Gong, and Xu Gao. 2021. "Effects of Desiccation, Water Velocity, and Nitrogen Limitation on the Growth and Nutrient Removal of Neoporphyra haitanensis and Neoporphyra dentata (Bangiales, Rhodophyta)" Water 13, no. 19: 2745. https://doi.org/10.3390/w13192745

APA Style

Li, J., Cui, G., Liu, Y., Wang, Q., Gong, Q., & Gao, X. (2021). Effects of Desiccation, Water Velocity, and Nitrogen Limitation on the Growth and Nutrient Removal of Neoporphyra haitanensis and Neoporphyra dentata (Bangiales, Rhodophyta). Water, 13(19), 2745. https://doi.org/10.3390/w13192745

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