Growth and nutrient uptake of Myriophyllum spicatum under different nutrient conditions and its potential ecosystem services in an enclosed sea area in the East China Sea

Marine Pollution Bulletin 151 (2020) 110801

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Growth and nutrient uptake of Myriophyllum spicatum under different nutrient conditions and its potential ecosystem services in an enclosed sea area in the East China Sea ⁎

T

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Yanlin Baoa,1, Yuanzi Huoa,b,1, Yuanliang Duana, , Peimin Hea, , Meiqin Wua, Na Yanga, Bin Suna a b

College of Marine Ecology and Environment, Shanghai Ocean University, Shanghai 201306, China Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science, 146 Williams St., Solomons, MD 20688, United States

A R T I C LE I N FO

A B S T R A C T

Keywords: Myriophyllum spicatum Low salinity Ecosystem service Nutrient bioextraction Carbon sequestration efficiency

We investigated the growth and nutrient uptake of Myriophyllum spicatum under different nutrient conditions and evaluated its implications for ecosystem services in an enclosed area of Jinshan. The specific growth rate ranged from 1.29%–4.37%/day, and the dissolved inorganic carbon and nitrogen, and phosphorus uptake rates were 1.30–1.62, 0.040–0.453, and 0.003–0.027 mg/(g∙day), respectively, under different nutrient conditions. The O2production and carbon-sequestration efficiencies in the field were 154.30 and 1.25 mg/(g DW∙h), respectively. The average removal efficiencies of NH4+-N, NO3−-N, NO2−-N, and PO43−-P were 43.05%, 97.03%, 64.26%, and 59.24%, respectively, in M. spicatum-cultivated areas compared with in the open sea. Harvesting of M. spicatum removed 12,936.87, 1289.97 and 114.81 kg of carbon, nitrogen, and phosphorus, respectively, from seawater in Jinshan in Nov, 2018. In conclusion, M. spicatum is a good candidate for integrated macrophyte/ animal multi-trophic aquaculture in terms of nutrient extraction and economic diversification in low-salinity environments.

1. Introduction Nutrients are added to coastal seawater through natural processes such as ocean upwelling and geological weathering (Bricker et al., 2008). Furthermore, the rapid expansion of intensive monoculture systems in line with increasing demand for fish supplies (Ferreira et al., 2014) results in large amounts of feces and uneaten feed from traditional marine cage farms entering the marine environment (Chopin et al., 2001). It has been estimated that approximately 80%–88% of the carbon, 52%–95% of the nitrogen, and 85% of the phosphorus contents of the feed inputs into marine fish culture systems were lost through fish excretion and uneaten feed (Skriptsova and Miroshnikova, 2011). This sudden increase in nutrients upsets the natural balance and causes eutrophication, which represents a major threat to the seawater environment (Victor et al., 2002), especially lagoons (Bell, 1992; Lloret et al., 2008; Lapointe et al., 2015). Domingues et al. (2017) speculated that future nutrient enrichments may lead to accelerated growth of specific functional groups and species in the Ria Formosa coastal lagoon. High riverine nutrient loads caused poor water quality, low water transparency and an unsatisfactory ecological status in the Szczecin

(Oder) Lagoon, the Baltic Sea (Friedland et al., 2019). Numerous management measures and experiments have been carried out to ameliorate the symptoms of eutrophication and improve seawater quality in relation to mariculture (Yu and Yang, 2008; Huo et al., 2012; Tedesco et al., 2014). However, it has been recognized that the high nutrient load of coastal seawater cannot be resolved immediately by reducing pollution sources alone, given that other forms of nutrient input, such as benthic nutrient recycling and submarine groundwater discharge, may continue to impact on the environment, even without causing overload (Grenz et al., 2000; Moore, 2010). Methods using macroalgae to treat mariculture-system effluents were first developed in the mid-1970s (Fei et al., 1999; Chung et al., 2002; Neori et al., 2004), and the cultivation of seaweed to minimize the impact of nutrient addition offshore has recently received increasing attention as a method of in situ remediation (Xiao et al., 2017). The large-scale cultivation of red seaweed (Porphyra yezoensis) could be used to alleviate eutrophication and control harmful algal blooms in the open sea (Wu et al., 2015a). Moreover, macroalgae have higher photosynthetic efficiencies than terrestrial plants and are more efficient at capturing carbon (Packer, 2009). They have developed carbon-

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Corresponding authors. E-mail addresses: [email protected], [email protected] (Y. Duan), [email protected] (P. He). 1 These authors contributed equally to this work https://doi.org/10.1016/j.marpolbul.2019.110801 Received 2 September 2019; Received in revised form 15 November 2019; Accepted 3 December 2019 Available online 29 January 2020 0025-326X/ © 2019 Published by Elsevier Ltd.

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concentrating mechanisms that can generate high CO2 concentrations around rubisco (Moulin et al., 2011), or can use HCO3– as a direct source of carbon (Klenell et al., 2004). These mechanisms play an important role in slowing global warming and ocean acidification. Duan et al. (2019) proposed Gracilaria cultivation as a useful technique for nutrient (carbon, nitrogen, and phosphorus) bioextraction in coastal waters. Moreover, several macroalga species are currently used as biofilters to reduce aquaculture-derived inorganic nutrients (Klinger and Naylor, 2012; Handå et al., 2013; Kim et al., 2014). However, although seaweed cultivation has developed dramatically, not all coastal areas are suitable for the growth of marine macroalgae, such as lowsalinity (< 10) bays, which usually have higher nutrient loads (Liu et al., 2018). The flocculant polyaluminium chloride and lanthanummodified bentonite were used to inhibit cyanobacterial bloom and prevent eutrophication of lagoon (de Magalhães et al., 2019), and whether there are potential hazards is unknown. It is therefore essential to study the nutrient-removal ability of algae that are able to survive in low-salinity sea areas. Myriophyllum spicatum is a submerged freshwater macrophyte that can absorb nutrients from both the sediment and water in lakes and rivers (Planas, 1981; Angelstein et al., 2009). This plant can also tolerate a degree of salinity (10.0–16.6) under controlled indoor conditions (Haller et al., 1974). M. spicatum was also shown to release polyphenols that influenced the epiphytic bacterial community in the brackish Schaproder Bodden on the Baltic coast (Hempel et al., 2008). Large-scale cultivation of M. spicatum can aid nutrient bioextraction and inhibit microalgal growth in low-salinity marine water bodies (Liu et al., 2018). However, to the best of our knowledge, the nutrient tolerance and carbon-sequestration ability of M. spicatum has not yet been reported. The aim of this study was to determine the nutrient uptake rates (carbon, nitrogen, and phosphorus) of M. spicatum cultivated under different nutrient conditions, and to evaluate its potential ecosystemservice role in an enclosed mariculture sea area (Jinshan sea, 121°34′73.57″E, 30°70′86″N) in Hangzhou Bay on the coast of the East China Sea. The results of this study will provide a scientific basis for the use of M. spicatum for nutrient bioextraction in low-salinity lagoons worldwide.

Fig. 1. Study area. Location of the Jinshan enclosed sea area in Hangzhou Bay on the East China Sea coast. Table 1 Concentrations of nitrogen and phosphorus in the different experimental treatment groups.

2. Materials and methods 2.1. Growth and nutrient uptake in M. spicatum under different nutrient conditions in the laboratory Myriophyllum spicatum was collected from its cultivation area in an enclosure of the Jinshan sea area in Aug, 2018 (Fig. 1). Epiphytes and debris were removed from the surface using a soft brush, and M. spicatum was then rinsed with sterile seawater and cultured aseptically in Hoagland medium in illuminating incubators at 25 ± 2 °C, salinity 6.9 ± 0.2, and irradiance of 4000 lx, with a photoperiod of 12 h light: 12 h dark. M. spicatum was acclimated to the culture environment for 1 week before experimentation. A total of 16 combinations of nitrogen and phosphorus concentrations were used in the present study (Table 1). The nitrogen concentration in the medium was adjusted to 5, 15, 25, and 50 mg/L with NaNO3, referred to as N1, N2, N3, and N4, respectively. The phosphorus concentration was adjusted to 0.5, 1.5, 2.5, and 5 mg/L with Na2HPO4, referred to as P1, P2, P3, and P4, respectively. The inoculation biomass of M. spicatum was set at 0.200 ± 0.02 g. Samples were cultured in 50mL colorimetric tubes containing 50 mL experimental medium. All experiments were performed separately at least in triplicate, with aseptic techniques employed in all experimental steps. The experiments lasted for 5 days, and samples were collected at baseline and every day until the end of the experiment. The fresh weight of M. spicatum was also measured at baseline and every day until the end of experiment, and the specific growth rate

Combination

NO3−-N (mg/L)

PO43−-P (mg/L)

N1P1 N1P2 N1P3 N1P4 N2P1 N2P2 N2P3 N2P4 N3P1 N3P2 N3P3 N3P4 N4P1 N4P2 N4P3 N4P4

5 5 5 5 15 15 15 15 25 25 25 25 50 50 50 50

0.5 1.5 2.5 5 0.5 1.5 2.5 5 0.5 1.5 2.5 5 0.5 1.5 2.5 5

(SGR, %/day [%/d]) was calculated according to the following equation:

SGR =

(ln Wi + 1 − ln Wi ) × 100 t

where the Wi+1 represents the fresh weight at time i + 1, Wi represents the fresh weight at time i, and t represents the time between i + 1 and i. The pH was measured with a pH meter, dissolved inorganic carbon (DIC) was determined using a total organic carbon analysis meter (TOCVCPH, Shimadzu, Japan), and the concentrations of NO3−-N and PO43−P were measured according to the protocols of the Joint Global Ocean Flux Study (JGOFS 1994). The nutrient uptake rate (NUR, mg/(g∙day) [mg/(g∙d)]) of M. spicatum was estimated based on the following equation (Xu and Gao, 2012):

NUR =

(C0 − Ct ) × V W×t

where the C0 represents the DIC and nutrient concentrations at the beginning (mg/L), Ct represents the DIC and nutrient concentration at time t (mg/L), V represents the volume of the culture medium (L), t represents the time interval of sampling (d), and W represents the fresh 2

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experiment (mg/L), V represents the bottle volume (L), W represents the dry weight of M. spicatum (g), and t represents the duration of the experiment (h).

weight of M. spicatum cultured in the experiment (g). 2.2. Ecosystem services of M. spicatum cultivated in an enclosure of the Jinshan sea area

2.2.3. Growth and nutrient-removal rates of M. spicatum in Jinshan sea area Four sampling sites were established in the M. spicatum-cultivation area and the weight of M. spicatum was measured and the biomass was calculated at each sampling site. Surface water samples were collected (four sampling sites in M. spicatum-cultivation area and one sampling site in the open sea close to the Jinshan sea area). Temperature and salinity were measured directly in the field. The concentrations of NH4+-N, NO2−-N, NO3−-N, and PO43−-P were measured in the laboratory. The samples were brought back to the laboratory under cold conditions as soon as possible. The experiment ran from Jun 15 to Nov 15, 2018. Samples were collected at the beginning of the experiment and every month until the end of the experiment.

2.2.1. Study area The study was conducted in an enclosure of the Jinshan sea area, located on the East China Sea coast (Fig. 1). The seawater temperature and salinity during the study period were 24.7 °C–30.7 °C and 4.5–7.7, respectively. 2.2.2. Photosynthetic rate and nutrient uptake efficiency of M. spicatum in the Jinshan sea area The black and white bottle method was used in this experiment. Samples of M. spicatum (12.00 ± 0.05 g) were placed in black and white bottles, respectively, filled with in situ-filtered seawater. The experiment was divided into three groups: white bottle + M. spicatum (WM), black bottle + M. spicatum (BM), and control white bottle (WC). The bottles were suspended in the M. spicatum cultivation area for 4 h (9:30–13:30) on a sunny day. Nutrient (DIC, NH4+-N, NO2−-N, NO3−N, and PO43−P) and dissolved oxygen (DO) levels were determined. The carbon-sequestration efficiency (RDIC, mg/(g DW∙h)) of M. spicatum was calculated according to the following equation:

2.3. Data analysis The location of this study was created using Surfer 8.0 software (Golden Software, USA). All statistical analyses were performed using SPSS 19.0 software (SPSS Inc., Chicago, Illinois, USA). Duncan's range test was used to test the difference between means. Tests of homogeneity of variance and separate one-way analysis of variance were performed to test for differences in physicochemical parameters and growth properties between different experimental groups. Least significant difference was used to make post hoc comparisons between different experimental groups, and a P-value of < 0.05 was considered statistically significant. All data are presented as mean ± standard deviation.

RDIC = RWM − RBM − RWC RWM =

(DIC0 − DICWM ) × V W×t

RBM =

(DIC0 − DICBM ) × V W×t

RWC =

(DIC0 − DICWC ) × V W×t

3. Results

where RWM, RBM, and RWC represents the carbon-sequestration efficiencies of M. spicatum in the WM, BM, and WC groups, respectively (mg/(g DW∙h)); DIC0 represents the DIC at baseline (mg/L); DICWM, DICBM, and DICWC represent the DICs in the WM, BM, and WC groups, respectively, at the end of the experiment (mg/L), V represents the bottle volume (L), W represents the dry weight of M. spicatum (g), and t represents the duration of the experiment (h). The O2-production efficiency (RDO, mg/(g DW∙h]) of M. spicatum was calculated according to the following equation (Yao et al., 2013):

3.1. Growth and nutrient uptake in M. spicatum under different nutrient conditions in the laboratory 3.1.1. M. spicatum growth rate The SGRs of M. spicatum under different nutritional conditions are shown in Table 2. The SGRs in all 16 groups initially increased and then decreased with time. All SGRs were lowest on the first day and peaked on the third day, with the highest peak (4.37%/d) for N2P2 and the lowest (1.29%/d) for N4P4. Analysis of variance showed that nitrogen and phosphorus both had significant effects on the M. spicatum SGR (nitrogen, P < 0.001; phosphorus, P = 0.045 for 1 day and P < 0.001–0.002 for 2–5 days). The SGRs in the N1 and N2 groups were significantly higher than those in the N3 and N4 groups (P < 0.001–0.010), except for 1 and 5 days (P = 0.094–0.133). The effect of phosphorus on the SGR varied, with a significant difference between the P4 and other groups (P < 0.001–0.024), but no significant difference among the other groups (P = 0.068–0.915).

RDO = RWM − RBM − RWC RWM =

(DOWM − DO0) × V W×t

RBM =

(DOBM − DO0) × V W×t

RWC =

(DOWC − DO0) × V W×t

where RWM, RBM, and RWC represent the O2-production efficiencies of M. spicatum in the WM, BM, and WC groups, respectively (mg/(g DW∙h)), DOWM, DOBM, and DOWC represent the DO in the WM, BM, and WC groups, respectively, at the end of the experiment (mg/L), DO0 represents the DO at the beginning of the experiment (mg/L); V represents the bottle volume (L), W represents the dry weight of M. spicatum (g), and t represents the duration of the experiment (h). The nutrient uptake efficiency (R, μg/(g DW∙h)) of M. spicatum was calculated according to the following equation:

R=

3.1.2. Effects of M. spicatum on water pH under different nutritional conditions The initial pH of the nutrient solution was 8.41–8.61. The pH then increased over time in all groups (Fig. 2), reaching 9.02, 9.76, and 10.00 at 1, 3, and 4 days, respectively. Analysis of variance showed that nitrogen only had a significant effect on the pH at 1 and 4 days (P = 0.026 and P = 0.034, respectively), while phosphorus had a significant effect on pH (P < 0.001).

(CWC − CWM ) × V W×t

3.1.3. Nutrient uptake rates of M. spicatum under different nutrient conditions The DIC uptake rates decreased over time in all groups. The DIC was highest on the first day, with maximums of 1.30 mg/(g∙d) and 1.62 mg/ (g∙d) for N2P1 and N2P2, respectively. The DIC uptake rates on the first

where CWC represents the concentrations of nitrogen and phosphorus in the WC at the end of the experiment (mg/L), CWM represents the concentrations of nitrogen and phosphorus in the WM at the end of the 3

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Table 2 Specific growth rates of M. spicatum in the different experimental treatment groups (%/d). Concentration

Time (d)

P1 (0.5 mg/L)

P2 (1.5 mg/L)

P3 (2.5 mg/L)

P4 (5 mg/L)

N1

1 2 3 4 5 1 2 3 4 5 1 2 3 4 5 1 2 3 4 5

0.637 2.586 2.871 2.451 0.855 0.602 2.990 3.983 2.534 0.951 0.563 1.950 2.572 1.542 0.670 0.419 1.117 1.726 1.017 0.446

0.719 2.365 3.042 2.382 0.964 0.634 3.306 4.372 2.598 0.968 0.574 1.649 2.056 1.494 0.615 0.427 1.053 1.643 0.831 0.441

0.619 1.773 2.883 2.199 0.986 0.642 2.497 4.001 2.784 0.913 0.611 1.645 1.895 1.310 0.596 0.450 1.072 1.683 0.800 0.380

0.628 2.504 3.024 2.061 0.797 0.569 2.515 3.325 2.220 0.920 0.449 1.629 1.944 1.367 0.510 0.463 0.917 1.288 0.545 0.387

(5 mg/L)

N2 (15 mg/L)

N3 (25 mg/L)

N4 (50 mg/L)

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.010 0.036 0.053 0.045 0.031 0.041 0.057 0.042 0.051 0.005 0.069 0.039 0.038 0.044 0.043 0.037 0.088 0.046 0.050 0.046

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.038 0.040 0.036 0.038 0.032 0.080 0.051 0.316 0.122 0.028 0.041 0.044 0.085 0.003 0.059 0.032 0.063 0.032 0.085 0.041

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.055 0.069 0.077 0.057 0.003 0.046 0.061 0.055 0.050 0.068 0.070 0.042 0.028 0.058 0.098 0.043 0.056 0.072 0.042 0.048

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.055 0.045 0.031 0.063 0.071 0.044 0.018 0.030 0.031 0.059 0.064 0.061 0.051 0.047 0.025 0.025 0.016 0.047 0.050 0.032

Note: ‘d’ represents the duration of the experiment (day).

significant effect on phosphorus uptake rate at 3 days (P = 0.041), but no significant effect on the other days (P = 0.293–0.777). Regarding nitrogen, the phosphorus uptake rate increased with increasing nitrogen concentration rate (P < 0.001).

day were 1.548–1.902 times higher than on the second day. The DIC uptake rate first increased with increasing nitrogen concentration and then decreased. The effect of phosphorus concentration on the uptake rate of DIC varied, with no significant effects at 1 and 3 days (P = 0.851 and P = 0.115, respectively), but significant effects at 2 (P = 0.013), 4 (P = 0.001), and 5 days (P = 0.006) (Table 3). The nitrogen uptake rate of M. spicatum initially increased and then decreased, peaking on the third day (Table 4). Compared with N1, the nitrogen uptake rates in the N2, N3, and N4 groups were increased 1.113-, 1.158-, and 0.986-fold, respectively. Nitrogen concentration had a significant effect on the nitrogen uptake rate (P < 0.001). Regarding the phosphorus concentration, the nitrogen uptake rate was higher in the 1.5 and 2.5 mg/L groups than in the other groups. Phosphorus had no significant effect on nitrogen uptake rate at 2, 3, and 5 days (P = 0.070–0.641), but did have significant effects at 4 (P = 0.014) and 1 days (P = 0.003). The phosphorus uptake rate of M. spicatum initially increased and then decreased, reaching a peak on the third day (Table 5). The phosphorus uptake rate at a phosphorus concentration of 2.5 mg/L was higher than in the other groups. Phosphorus concentration had a

12

N1:P1 N3:P1

N1:P2 N3:P2

N1:P3 N3:P3

3.2. Ecosystem services of M. spicatum in Jinshan enclosed sea area 3.2.1. Photosynthetic rates and nutrient-uptake efficiencies of M. spicatum The O2-production and carbon-sequestration efficiencies of M. spicatum were 154.30 and 1.25 mg/(g DW∙h), respectively. The nutrientuptake efficiencies of NH4+-N, NO3−-N, NO2−-N, and PO43−-P were 0.248 ± 0.004, 0.319 ± 0.003, 0.099 ± 0.000, and 0.038 ± 0.000 μg/(g DW∙h), respectively, and the removal efficiencies of these nutrients were 0.71%, 0.17%, 0.69%, and 0.14%, respectively. 3.2.2. Growth and nutrient-removal rates of M. spicatum The biomass of M. spicatum ranged from 3349.42–3706.14 g/m2. M. spicatum grew fastest in Jul and the biomass peaked in Oct (Fig. 3). A total of 297 tons (fresh weight) of M. spicatum was harvested in Nov, with a carbon content of 38.73%, nitrogen content of 3.19%, and

N1:P4 N3:P4

N2:P1 N4:P1

N2:P2 N4:P2

N2:P3 N4:P3

10

pH

8 6 4 2 0 0d

1d

2d

Time

3d

4d

Fig. 2. Changes in water pH over time. 4

5d

N2:P4 N4:P4

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Table 3 Dissolved inorganic carbon uptake rates of M. spicatum in the different experimental treatment groups (mg/(g∙d)). Concentration

Time (d)

P1 (0.5 mg/L)

P2 (1.5 mg/L)

P3 (2.5 mg/L)

P4 (5 mg/L)

N1

1 2 3 4 5 1 2 3 4 5 1 2 3 4 5 1 2 3 4 5

1.48 0.87 0.84 0.82 0.71 1.62 0.96 0.85 0.77 0.70 1.50 0.86 0.81 0.70 0.61 1.37 0.78 0.70 0.56 0.46

1.36 0.87 0.84 0.77 0.69 1.62 0.97 0.85 0.71 0.61 1.51 0.87 0.80 0.65 0.56 1.39 0.74 0.69 0.62 0.49

1.41 0.91 0.77 0.75 0.65 1.57 0.90 0.86 0.63 0.57 1.49 0.95 0.85 0.62 0.55 1.39 0.79 0.73 0.55 0.50

1.57 0.83 0.79 0.77 0.68 1.43 0.86 0.80 0.74 0.62 1.58 0.83 0.79 0.65 0.55 1.30 0.75 0.67 0.59 0.47

(5 mg/L)

N2 (15 mg/L)

N3 (25 mg/L)

N4 (50 mg/L)

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.088 0.062 0.065 0.032 0.024 0.083 0.040 0.044 0.034 0.038 0.024 0.062 0.066 0.025 0.007 0.042 0.054 0.024 0.021 0.007

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.041 0.014 0.053 0.053 0.036 0.028 0.017 0.021 0.061 0.041 0.024 0.053 0.058 0.031 0.035 0.054 0.030 0.019 0.010 0.028

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.074 0.055 0.036 0.034 0.20 0.071 0.022 0.065 0.045 0.023 0.040 0.026 0.038 0.044 0.035 0.043 0.038 0.025 0.039 0.042

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.034 0.051 0.038 0.032 0.030 0.034 0.059 0.056 0.065 0.043 0.058 0.063 0.017 0.034 0.012 0.049 0.058 0.024 0.018 0.015

Note: ‘d’ represents the duration of the experiment (day).

area were significantly lower than those in the open sea area (P < 0.001), except in Jul (P = 0.335). Compared with the open sea area, the maximum removal efficiency of PO43−-P was 85.34% in Jun and the average removal efficiency was 59.24%.

phosphorus content of 0.34% dry weight. The harvesting activities thus removed 12,936.87 kg carbon, 1289.97 kg nitrogen, and 114.81 kg phosphorus from the seawater. Changes in dissolved inorganic nutrients are summarized in Fig. 4. The NH4+-N concentrations in the M. spicatum-cultivation area were significantly lower than those in the open sea area (P < 0.001–0.005), except in Aug (P = 0.315). Compared with the open sea area, the maximum removal efficiency of NH4+-N was 69.63% in Nov and the average removal efficiency was 43.05%. The NO3−-N concentrations in the M. spicatum-cultivation area were significantly lower than those in the open sea area (P < 0.001). Compared with the open sea area, the maximum removal efficiency of NO3−-N was 99.42% in Nov and the average removal efficiency was 97.03%. The NO2−-N concentrations in the M. spicatum-cultivation area were significantly lower than those in the open sea area (P < 0.001–0.002), except in Aug (P = 0.844). Compared with the open sea area, the maximum removal efficiency of NO2−-N was 97.45% in Jul and the average removal efficiency was 64.26%. The PO43−-P concentrations in the M. spicatum-cultivation

4. Discussion The rapid development of human ocean activities in the past few decades, especially intensive aquaculture, has resulted in extensive nutrient input into coastal marine water bodies, with adverse effects on coastal marine ecosystems (Shu et al., 2004). Hangzhou Bay, a typical estuary and coastal water system in the East China Sea, is facing severe seawater eutrophication because of nutrient inflow from the Yangtze River (Tao et al., 2017), leading to ecological imbalance and frequent red tides (Huo et al., 2011; Rose et al., 2015). Gracilaria verrucosa was used to remove nutrients from the seawater in Hangzhou Bay (salinity 11–15) from 2006 to 2007 (Huo et al., 2011), but this water body has recently become unfavorable for the growth of seaweeds such as G.

Table 4 Nitrogen uptake rate of M. spicatum in the different experimental treatment groups (mg/(g∙d)). Concentration

Time (d)

P1 (0.5 mg/L)

P2 (1.5 mg/L)

P3 (2.5 mg/L)

P4 (5 mg/L)

N1

1 2 3 4 5 1 2 3 4 5 1 2 3 4 5 1 2 3 4 5

0.017 0.029 0.042 0.037 0.032 0.066 0.086 0.139 0.128 0.110 0.098 0.141 0.250 0.196 0.186 0.177 0.272 0.424 0.345 0.312

0.019 0.027 0.044 0.039 0.035 0.070 0.090 0.147 0.125 0.114 0.107 0.166 0.244 0.205 0.189 0.185 0.264 0.426 0.407 0.342

0.016 0.027 0.043 0.036 0.031 0.060 0.084 0.147 0.108 0.105 0.097 0.157 0.254 0.191 0.188 0.184 0.280 0.453 0.342 0.341

0.019 0.025 0.040 0.034 0.032 0.053 0.084 0.141 0.119 0.105 0.102 0.155 0.244 0.187 0.179 0.166 0.266 0.402 0.367 0.324

(5 mg/L)

N2 (15 mg/L)

N3 (25 mg/L)

N4 (50 mg/L)

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.001 0.002 0.002 0.004 0.002 0.002 0.008 0.006 0.006 0.005 0.008 0.006 0.023 0.007 0.007 0.007 0.027 0.020 0.044 0.007

Note: ‘d’ represents the duration of the experiment (day). 5

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.001 0.001 0.003 0.001 0.003 0.005 0.005 0.010 0.018 0.002 0.002 0.006 0.014 0.011 0.018 0.004 0.016 0.012 0.017 0.029

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.000 0.002 0.001 0.003 0.002 0.002 0.005 0.009 0.008 0.004 0.010 0.015 0.034 0.015 0.007 0.009 0.020 0.021 0.015 0.019

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.001 0.004 0.004 0.001 0.001 0.002 0.001 0.007 0.013 0.008 0.008 0.014 0.013 0.013 0.005 0.003 0.026 0.017 0.022 0.022

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Table 5 Phosphorus uptake rates of M. spicatum in the different experimental treatment groups (mg/(g∙d). Concentration

Time (d)

P1 (0.5 mg/L)

P2 (1.5 mg/L)

P3 (2.5 mg/L)

P4 (5 mg/L)

N1

1 2 3 4 5 1 2 3 4 5 1 2 3 4 5 1 2 3 4 5

0.001 0.001 0.003 0.002 0.002 0.003 0.004 0.008 0.008 0.007 0.006 0.007 0.013 0.012 0.012 0.009 0.014 0.025 0.021 0.020

0.001 0.001 0.003 0.002 0.002 0.003 0.004 0.009 0.007 0.007 0.006 0.008 0.012 0.012 0.012 0.009 0.013 0.025 0.024 0.021

0.001 0.001 0.003 0.002 0.002 0.003 0.004 0.009 0.007 0.007 0.006 0.008 0.014 0.012 0.013 0.010 0.014 0.027 0.021 0.022

0.001 0.001 0.003 0.002 0.002 0.003 0.004 0.009 0.007 0.007 0.006 0.008 0.013 0.012 0.012 0.009 0.013 0.025 0.022 0.021

(5 mg/L)

N2 (15 mg/L)

N3 (25 mg/L)

N4 (50 mg/L)

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.001 0.001 0.000 0.000 0.001 0.001 0.001 0.000 0.001 0.001 0.001 0.003 0.001

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.001 0.000 0.000 0.000 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.002

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.001 0.000 0.001 0.001 0.002 0.001 0.000 0.001 0.001 0.000 0.001 0.001

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.001 0.001 0.001 0.001 0.001 0.001 0.000 0.000 0.001 0.001 0.001 0.001

Note: ‘d’ represents the duration of the experiment (day).

negative consequences (Nichols and Shaw, 1986). In the present study, we removed excess M. spicatum by harvesting. In addition to its growth advantages, M. spicatum was shown to tolerate high nutrient concentrations (Ge et al., 2012), similar to the current results. Best and Mantai (1978) reported that M. spicatum could meet its nitrogen requirements by root absorption from the sediment and by direct uptake from the water by its stem and leaf tissues. Liu et al. (2018) also found that M. spicatum could uptake nutrients from both the seawater and sediment. In the present study, we showed that the SGR and nutrientabsorption efficiency of M. spicatum increased significantly when it began to grow roots on the second day, implying that the roots play an important role in the process of ecological remediation by M. spicatum. Fast-growing species tend to require relatively higher external concentrations of inorganic nitrogen to saturate their growth (Pederson and Borum, 1997), but extreme high nutrient concentrations can also inhibit their growth (Duan et al., 2019), in accord with our current results. Many studies have shown that Myriophyllum can effectively remove nutrients by utilizing excess nutrients (e.g., nitrogen and phosphorus) in water bodies (Zhou et al., 2016; Liu et al., 2018; F. Liu et al., 2018; Ma

verrucosa, due to its relatively low salinity. In the present study, we successfully extracted nutrients and increased the ocean carbon sink in low salinity sea areas by cultivating the freshwater, submerged macrophyte M. spicatum. To the best of our knowledge, this is the first study to use this technique to examine the ecosystem services of M. spicatum in low-salinity sea areas. Macroalgae can remove excess nutrients such as nitrogen and phosphorus from the environment (Wei et al., 2017), and the use of seaweed to restore the ecological balance in affected regions is one of the recommended methods of remediation (Samocha et al., 2015; Duan et al., 2019). However, few macroalgae can grow in low salinity waters, and M. spicatum, which can tolerate low salinity, may thus play an important role in ecological remediation in these conditions (Liu et al., 2018). M. spicatum is highly dependent on vegetative propagation and spreads through stem fragments (Vári, 2013). This property can benefit the ecosystem by augmenting nutrient cycling and energy flow processes (Nichols and Shaw, 1986), and by reducing labor and capital investment. However, some researchers have suggested that these properties mean that the use of M. spicatum for remediation purposes must be complemented by management practices to prevent any

3800 3700 Biomass (g/m2)

3600 3500 3400 3300 3200 3100 3000 Jun

Jul

Aug

Sep

Oct

Time ˄2018˅ Fig. 3. Biomass of M. spicatum in Jinshan enclosed sea area. 6

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Fig. 4. Variations in dissolved inorganic nutrient concentrations in Jinshan enclosed sea area.

Jinshan sea area. Overall, these results suggested that M. spicatum cultivation may provide an effective method for improving the aquatic environment in eutrophic areas. In conclusion, M. spicatum has a high carbon content and high nutrient tolerance, and is especially able to withstand low-salinity seawater. These factors make the “blue carbon” and nutrient-bioextraction benefits of M. spicatum irreplaceable for low salinity offshore waters. The widespread distribution of low salinity sea areas (lagoons) throughout the world means that M. spicatum cultivation could be recommended on a global scale. Furthermore, the development and promotion of integrated multi-trophic aquaculture systems using cocultures of M. spicatum with aquatic animals may also be viable, but requires cooperation between farmers and the government to achieve sustainable mariculture systems.

et al., 2018). The eutrophication index for Hangzhou Bay indicates that it is severely eutrophic (Li et al., 2017), which is also the case for other bays, such as Sansha Bay (Hu et al., 2013; Wei et al., 2017). The poor hydrological exchange conditions and highly intensive fish cage farming could increase the risk of fish diseases, water column nutrient enrichment, and the occurrence of red tides (Hu et al., 2013; Wu et al., 2015b). In addition, sediments serve as one of the main sources of nutrients entering the water bodies (Jiang et al., 2010; Sun et al., 2010). The current results indicated that M. spicatum showed good growth performances in the eutrophic and low-salinity conditions of Hangzhou Bay. The average removal efficiencies of M. spicatum for NH4+-N, NO3−-N, NO2−-N, and PO43−-P were 43.05%, 97.03%, 64.26%, and 59.24%, respectively, which were much greater than for the macroalga Gracilaria lemaneiformis (Duan et al., 2019). These results thus suggested that M. spicatum is an ideal bioremediation agent, with high nutrient-removal efficiencies. In addition to removing nutrients from the environment, macrophyte cultivation may also provide other ecosystem services (Sondak et al., 2017; Zhang et al., 2017). Bioenergy can result in the trapping of CO2 in geological reservoirs, representing a combination of bioenergy production and carbon capture and storage (Moreira and Pires, 2016). The total production of algae in the Asia-Pacific sea areas has exceeded 2.61 × 106 DW tons, equivalent to > 2.87 × 106 tons of CO2 being sequestered each year (Sondak et al., 2017). Carbon sequestration by macroalgae in the global continental shelf area is 700 million tons per year (He et al., 2015). In the present study, the carbon-sequestration efficiency of M. spicatum was 1.25 mg/(g DW∙h), which was lower than that of G. lemaneiformis in Sansha Bay (Duan et al., 2019) and in Sanggou Bay (Yang et al., 2005). However, a total of 297 tons of M. spicatum was harvested and 12,936.87 kg of carbon was removed from the seawater. In contrast, Wu et al. (2015b) estimated that the total production of G. lemaneiformis was 21,820 tons in Yantian Bay, equivalent to harvesting 792.39 tons of CO2. The carbon-removal efficiency of M. spicatum is thus much higher than that of G. lemaneiformis. Furthermore, the O2-production efficiency of M. spicatum was 154.30 mg/(g DW∙h), which was also much higher than that of G. lemaneiformis (Yang et al., 2005; Duan et al., 2019). In addition to the removal of carbon, 1289.97 kg nitrogen and 114.81 kg phosphorus were removed from the seawater through M. spicatum cultivation in the

Acknowledgements We thank International Science Editing (http://www. internationalscienceediting.com) for editing this manuscript. Thanks are also due to the anonymous reviewers for their valuable comments and suggestions. Funding This study was supported by the Key Projects in the National Science & Technology Pillar Program (2012BAC07B03), the Shanghai Universities First-class Disciplines Project (Discipline name: Marine Science (0707)), Shanghai Oceanic Administration Scientific Research Project (2015-02), the Plateau Peak Disciplines Project of Shanghai Universities (Marine Science 0707). Availability of data and materials All data generated and analyzed during this study are included in this published article. Authors' contributions Peimin He supported the research and Yuanliang Duan supervised 7

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the laboratory work, leaded the design and coordination of this study. Yuanliang Duan, Yanlin Bao and Yuanzi Huo participated in the design, supervision and coordination of the study, and in drafted and revision of the manuscript. Meiqin Wu, Bin Sun and Na Yang participated in the supervision and coordination of the study, especially, Meiqin Wu and Bin Sun gave more suggestion to statistical analysis. All authors read and approved the final manuscript.

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