Next Article in Journal
Applications of RIM-Based Flow Visualization in Fluid-Solid Interaction Problems: A Review of Formulations and Prospects
Previous Article in Journal
Hydro–Solar Hybrid Plant Operation in a Hydropower Plant Cascade: Optimizing Local and Bulk System Benefits
Previous Article in Special Issue
Heavy Metal Concentrations in Wild and Cultured Oplegnathus fasciatus from the East China Sea and Associated Health Risks
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Water
Volume 16
Issue 14
10.3390/w16142054
water-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Coupling Imports of Dissolved Inorganic Nitrogen and Particulate Organic Matter by Aquaculture Sewage to Zhangjiang Estuary, Southeastern China

by
Shuang He
1,
Ta-Jen Chu
1,2,
Zhiqiang Lu
1,2,* and
Danyang Li
1,2,*
1
Fisheries College, Jimei University, Jimei District, Xiamen 361021, China
2
State Key Laboratory of Mariculture Breeding, Jimei University, Xiamen 361021, China
*
Authors to whom correspondence should be addressed.
Water 2024, 16(14), 2054; https://doi.org/10.3390/w16142054
Submission received: 13 June 2024 / Revised: 4 July 2024 / Accepted: 17 July 2024 / Published: 20 July 2024
(This article belongs to the Special Issue Coastal Ecology and Fisheries Management)
Browse Figures
Versions Notes

Abstract

:
Estuary ecosystems serve as crucial connectors between terrestrial and marine environments, thus playing vital roles in maintaining the ecological balance of coastal marine ecosystems. In recent years, the eutrophication in estuaries caused by aquaculture sewage has been revealed, highlighting the necessity to understand its influence on the nutrient conditions and carbon storage of estuaries. In this study, δ15N and δ18O were used to indicate the contribution of aquaculture-derived sewage to dissolved inorganic nitrogen in Zhangjiang Estuary, and δ13C and C:N ratio were used to reveal its effects on the particulate organic matter. The major results are as follows: (1) Aquaculture water contributed 62~86% and 60~100% of the total nitrate and ammonium in Zhangjiang Estuary, respectively, and the drainage periods of the cultured species has a great influence on the content and composition of dissolved inorganic nitrogen. (2) Aquaculture water was also the major source of particulate organic matter (24~33% of the total content) here, most of which may be derived from crab ponds. (3) The imports of nutrients by aquaculture water may potentially regulate particulate organic matter in Zhangjiang Estuary by promoting the growth of phytoplankton and zooplankton. Our study revealed the coupling effects of aquaculture activities on the nitrogen and carbon storage in an estuarine ecosystem. It also indicates that isotopes may be efficient in the monitoring of a coastal environment, which may further aid the management of inshore cultivation.

1. Introduction

Due to the increasing world population, the demand for seafood has continued to increase in recent decades, thus stimulating the expansion of aquaculture. Up until 2022, global fisheries and aquaculture production surged to 223.2 million tonnes, with 62% harvested in marine areas and 31% from inland waters [1]. China has the world’s largest mariculture industry, accounting about 36% of the global total aquaculture production [1]. In southeastern China, aquaculture ponds are usually set around estuaries, causing a wide variety of environmental problems, among which the contaminants of water were the primary focus [2,3,4]. As an estuary ecosystem serves as the link between terrestrial and marine environments, it plays a vital role in maintaining the ecological balance of coastal marine ecosystems [5,6]. Thus, it is necessary to reveal the long-time impacts of aquaculture pollutants on the environment of estuaries.
Aquaculture pollutants mainly consist of a large amount of dissolved inorganic nitrogen (DIN) and organic matters derived from excessive feeds, residual baits, and animal wastes [7]. The exportation of DIN and organic matter from aquaculture ponds may affect regional environment by the following paths: (1) The large amounts of nutrients may stimulate the production of algae [8,9,10] and hence increase the amount of biogenic organic matter, which is usually characterized by higher bio-availability [11,12]. (2) The residual baits and the animal wastes in aquaculture waters and sediments may directly increase the amount of particulate organic matter (POM) in the surface of the estuary [8,13]. (3) The simultaneous increases of the contents and the bio-availability of organic matter, as well as the contents of DIN, may accelerate the coupling cycles of carbon (C) and nitrogen (N) in such areas [8,9,11]. The decomposition of the imported organic matter and algae residues may deplete water oxygen, thus posing a threat to fish, shellfish, and other marine organisms [14,15]. Additionally, the coupling imports of DIN and organic matter may further promote heterotrophic microbial N removal here, thus increasing the release of N2O, the by-product of microbial N removal [9,16,17,18]. It has been reported that N2O is approximately 300 times more potent than CO2 in holding heat in a 100 year timescale [19]. Therefore, it is an urgent need to reveal the coupling effects of aquaculture water on DIN and organic matter in the estuary environment. However, until now, quantifying the sources of DIN and organic matter to the river and linking these sources to specific land uses and point-sources of pollution has been less reported. As most of the residual feeds and animal baits are in particulate forms, the source analysis of DIN and POM based on isotopic characteristics (δ15N for NO3−, NH4+ and PN, δ18O for NO3−, and δ13C for POC) may provide help in this region [20,21,22,23,24].
Zhangjiang Estuary (117.40–117.50° E, 23.88–23.93° N) is a semi-enclosed estuary in southeastern China [25]. The climate in this area is subtropical with an annual precipitation of 1680 mm and seasonal mean temperatures ranging from 15.9 to 28.8 °C. The eutrophication caused by the imports of human-derived sewage has been reported here for several years [13,16,25,26], and thus it may provide an ideal site to reveal the effects of aquaculture water on DIN and POM in estuary. During our previous study in December 2021, the IsoSource mixing model was used to reveal the sources of POM here, indicating that sewage was the major source of POM [27]. However, it has been suggested that the Mixsir mixing model may be more suitable for the source analysis of organic matter or nutrients based on isotopic values [28,29]. Therefore, in this study, the Mixsir mixing model was employed for the DIN and POM source analysis, and the major source of POM in December 2021 was also re-analyzed. The main aims of this study are as follows: (1) to observe the distribution characteristics of nitrate (NO3−), ammonium (NH4+), and POM in Zhangjiang Estuary; (2) to observe the specific contribution of aquaculture water to the total DIN and POM here, as well as reveal its possible regulators. Our results will provide new insights in the monitoring and management of the coastal environment and offer more information regarding the sustainable development of aquaculture.

2. Materials and Methods

2.1. Sample Collection

Field sampling was conducted in May 2023. Water samples were collected at 8 stations, among which S1 was set at the shrimp ponds, and S2~S8 were set from upstream to downstream of Zhangjiang Estuary (Figure 1). In this study, S1 and S2 were set to observe the isotopic values of DIN and POM derived from aquaculture water and freshwater. Another station was set at the up in the neighboring Dongshan Bay to observe the isotopic values of DIN and POM derived from seawater. Surface water (≈0.5 m) at all stations was collected by Niskin bottles in one day to observe the contents of NO3−, NH4+, POC, PON, and their isotopic values (δ15N for NO3−, NH4+, and PN; δ18O for NO3−; and δ13C for POC). All samples were treated with ZnCl2 after collection and kept at 4 °C until analysis [20,22]. Basic parameters, including temperature (T), salinity (S), the contents of dissolved oxygen (DO), phycoerythrin, and chlorophyll a (Chl a) were measured in situ using YSI 6600 multi-probe sensors (Yellow Springs Instrument Co., Yellow Springs, Ohio, OH, USA). Apart from samples in May 2023, the source of POM in December 2021 was re-analyzed by the Mixsir mixing model. The details of stations in December were shown in our previous study [27].

2.2. Contents and Isotopic Characteristics of Nitrate and Ammonium

Water samples were filtered by precombusted (450 °C, 4 h) GF-75 filters (47 mm, 0.3 μm pore size). Concentrations and δ15N of NO3− and NH4+ were determined using a MAT 253 gas stable isotope ratio mass spectrometer interfaced with Gas-Bench II (Thermo Fisher, Waltham, MA, USA). The δ15N and δ18O of NO3− were measured using the “denitrifier method” [30,31], with the analytical precisions of the δ15N and δ18O less than 0.5‰ and 1‰, respectively. The δ15N of NH4+ were determined following the methods described by Koba et al. [32]. In brief, NH4+ was concentrated on the glass fiber filter using the diffusion method and digested to NO3− using persulfate [33,34,35]. After that, the δ15N of the converted NO3− from NH4+ was measured using the denitrifier method [30,31]. The analytical precisions for δ15N and δ18O were less than 0.2‰ and 1‰, respectively.

2.3. Particulate Organic Matter

The large detritus in the water samples was removed with a 200 μm mesh, and then the particulate organic matter (POM) in water samples was collected by filtering 4 L of water through GF-75 filters (47mm, 0.3 μm pore size). The filters were previously combusted for 4 h at 450 °C to remove organic matter. All water samples were then filtered through a 200 μm mesh sieve to remove large detritus. Then, water samples (without large detritus) were filtered by the precombusted GF-75 filters to collect particulate organic carbon (POC) and nitrogen (PN). The GF-75 filters were quickly washed using Milli-Q water following filtration and frozen at −20 °C until analysis. In the laboratory, the filters were treated with HCl vapor (48 h) to remove inorganic carbon and then dried at 60 °C. The content of POC, PN, and the δ13C and δ15N of POM (δ13CPOM, δ15NPOM) were measured using a Finnigan Delta V Advantage isotope ratio mass spectrometer (Thermo Fisher Scientific, Waltham, MA, USA) interfaced with a Carlo Erba NC 2500 elemental analyzer (CE Instruments Ltd., England, United Kingdom). The analytical precision was <0.2‰ in this study.

2.4. Statistical Analysis

Pearson’s correlations analysis was conducted using the Statistical Package for Social Sciences program (version 19.0). The source analysis of nitrate and POM based on the δ15N and δ18O of NO3− and the δ13C and C:N ratio of POM were conducted by the Mixsir mixing model, using R (4.3.3 version).

3. Results

3.1. Physicochemical Parameters

The basic physicochemical parameters of the surface water in Zhangjiang Estuary (S2 to S8) are shown in Table 1. Surface temperatures (T) and surface salinity (S) in Zhangjiang Estuary ranged from 23.7 to 25.5 °C (24.4 ± 0.7 °C, n = 7) and 12.7 to 30.1‰ (21.4 ± 6.4‰, n = 7). Generally, surface T decreased from upstream to downstream, and surface S had the opposite distribution. The content of dissolved oxygen (DO) ranged from 6.6 to 7.4 mg L−1 (6.9 ± 0.3 mg L−1, n = 7), with the maximum observed at S2 and the minimum at S4. The contents of phycoerythrin and Chl a ranged from 0.6 to 10.1 μg L−1 (2.9 ± 3.4 μg L−1, n = 7) and 2.0 to 6.4 μg L−1 (3.5 ± 1.5 μg L−1, n = 7), respectively, with the maximum observed at S2 and S4, and the minimum at S5 and S7, respectively. When compared with the values observed in December 2021 [27], the contents of DO, phycoerythrin, and Chl a were obviously higher in May 2023 (Figure 2).

3.2. Concentration and Isotopic Values of Nitrate and Ammonium

The concentrations of NO3−-N and NH4+-N in May 2023 ranged from 0.20 to 1.33 mg L−1 (0.78 ± 0.42 mg L−1, n = 7) and 0.13 to 0.65 mg L−1 (0.44 ± 0.17 mg L−1, n = 7), respectively. Our previous study indicates that the content of NO2−-N in the study area was nearly under the detection limits [27], and thus it was not considered in this study. The content of total dissolved inorganic nitrogen (DIN) was calculated by summing the contents of NO3−-N and NH4+-N, which ranged from 0.32 to 1.90 mg L−1 (1.22 ± 0.58 mg L−1, n = 7). NO3−-N was the major type of DIN, accounting for 55~72% of the total DIN (Figure 3). Generally, the concentrations of NO3−-N and NH4+-N both decreased from S2 to S8 (Figure 3). Compared to the results in December 2021, the contents of NO3−-N and NH4+-N observed in May 2023 was lower, with relatively less spatial variation (Figure 3). Another difference was that the content of NH4+-N in November 2021 was obviously high, which accounted for more than 90% of the total DIN at most stations [27].
The δ15N of NO3− and NH4+ and the δ18O of NO3− were only determined in May 2023. The δ15N and δ18O values of NO3− ranged from 10.40 to 20.47‰ (16.16 ± 3.28‰, n = 7) and 6.13 to 9.83‰ (8.22 ± 1.34‰, n = 7), with the maximums observed at S3 and S4, respectively, and the minimums both observed at S2. The δ15N of NH4+ ranged from 0.13 to 0.65‰ (0.44 ± 0.17‰, n = 7), with the maximum observed at S3 and the minimum at S8 (Table S1). Generally, there were no obvious characteristics for the distribution of δ15N and δ18O.

3.3. The Contents and the Isotopic Characters of Particulate Organic Matter

The concentrations of POC and PN in May 2023 ranged from 7.8 to 57.6 μmol L−1 (24.9 ± 16.3 μmol L−1, n = 7) and 2.3 to 9.7 μmol L−1 (5.5 ± 2.6 μmol L−1, n = 7), respectively, with the maximum both observed at S2, and the minimum at S4 and S8, respectively (Figure 4a). The C:N ratio of POM ranged from 3.0 to 6.0 (4.3 ± 1.0, n = 7), with the maximum observed at S2 and the minimum at S4 (Figure 4a). The δ13C of POM in May 2023 ranged from −27.4 to −24.5‰ (−26.1 ± 1.0‰, n = 7), with the maximum observed at S6, and the minimum at S3 (Figure 4a). Compared to December 2021, the content of PN was higher in May 2023, while the content of POC and the C:N ratio were lower (Figure 4). The δ13C of POM in May 2023 was similar to that observed in December 2021.

4. Discussion

4.1. Aquaculture Sewage as the Major Source of Dissolved Inorganic Nitrogen

During our investigation, the content of DIN (0.32~1.90 mg L−1, Table S1) was about five times higher than the reported value in the neighboring Dongshan Bay, which ranged from 0.12 to 0.35 mg L−1 [36]. The densely distributed aquaculture ponds around the study area may be the major reason for the high content of DIN here. The content and the composition of DIN exhibited obvious seasonal variations, with a notably higher content and contribution of NH4+ observed in December 2021. This discrepancy may be attributed to varying drainage periods of the aquaculture species cultivated in this region. The major cultured species in the study area include crab, clam, and shrimp [13]. The cultivation of crab was carried out entire the year, while that for shrimp and clam were carried out from May to November and October to July, respectively. Another notable distinction between the two sampling periods is that the sampling in November 2021 was conducted after the removal of the sediments in clam ponds, which typically are carried out in August–September [13]. The residues and the metabolic N of the cultured species primarily exist as NH4+-N and dissolved organic nitrogen (DON) [37,38], and thus the exports of aquaculture water or sediments may significantly increase the content of NH4+-N in the study area. Apart from NH4+, aquaculture ponds may also be an important source of NO3−, as higher levels of NH4+ in aquaculture ponds may promote the microbial nitrification here, thus producing more NO3− [37,38,39,40,41]. In this study, positive correlations between NO3−-N and T, DO, and NH4+-N were observed in May 2023 (Figure 5a), indicating the possible active nitrification in Zhangjiang Estuary. Nitrifying bacteria prefer to utilize 14N from the NH4+ pool, leading to a gradual enrichment from 14N to 15N in NO3− with the reduction of the NH4+ pool [42]. Thus, the areas with active nitrification are typically characterized by opposite variations in NO3−-δ15N and the content of NH4+-N, as well as the δ15N of NH4+ [42,43]. However, such variation was not observed in the study area. This suggests that though microbial nitrification may be facilitated by relatively higher T and DO, along with the high availability of NH4+ in the study area, it seems not to be the major source of NO3−-N here. Thus, we propose that the positive correlation between NO3−-N and NH4+-N (Figure 5b) may be mainly caused by their common major source, rather than active microbial nitrification. Due to the higher density of aquaculture ponds in the upstream of Zhangjiang Estuary, the decreasing S from downstream to upstream may reflect the increasing effects of aquaculture sewage on NO3− and NH4+, and the negative correlation between NO3−-N and S can further support this (Figure 5a).
Previous investigation has indicated that the flux of the exported N derived from the aquaculture ponds in Zhangjiang Estuary was about 97~714 Kg N ha−1 yr−1, with the maximum observed from the shrimp ponds [13]. Our previous study in December 2021, based on the statistical correlation between POM and DIN, indicated that human-derived sewage contributed 12.2% to NO3− and 100% to NH4+. Much of the N-fertilized water enters into the surface streams and then is transported downriver to the estuary [39], thus causing many problems such as the bloom of algae, as well as oxygen deficit [9,13,40]. In addition, it may also promote the microbial removal of N and thus increase the release of N2O [9]. Apart from N2O, the microbial transformation of NO3− and NH4+ were also reported to be closely related with the emission of CH4 [19]. As N2O and CH4 have been reported to be about 300 and 200 times more potent in holding heat than CO2 [19], it is an urgent need to evaluate the specific effects of aquaculture sewage to the content and composition of DIN in the study area. The Mixsir mixing model based on the isotopic values of NO3− may provide help. In this study, the human-derived sewage was categorized into aquaculture, agriculture, and domestic sewage, and δ15N-NO3− and δ18O-NO3− were used to directly observe their contribution to NO3−. Though the δ15N value of NH4+ was also observed, it is hard to trace its source by a single isotope, and thus the content of NH4+ derived from aquaculture was observed based on the statistical correlation between NO3− and NH4+ contents (Figure 5b). The δ15N and δ18O of NO3− derived from the above sources are presented in Table 2. As the largest exporting flux of N was observed from shrimp ponds [13], S1 was set at the shrimp pond to observe the isotopic values of NO3− derived from aquaculture ponds. Generally, the observed δ15N-NO3− and δ18O-NO3− at S3~S8 were closer to the cover range of aquaculture water (Figure 5c). Based on the Mixsir mixing model, the specific contribution of aquaculture water to the total NO3− was observed.
The major results are as follows (Figure 6a): (1) In May 2023, most of the NO3− in the study area was derived from aquaculture water, accounting for 62~86% (71 ± 9%, n = 6) of the total NO3−. (2) Domestic sewage had a similar contribution to seawater and freshwater, which accounted for 4~13% (10 ± 4%, n = 6), 4~12% (9 ± 3%, n = 6), and 4~10% (7 ± 2%, n = 6) of the total NO3−, respectively. (3) Agricultural water accounted for only 2~3% (3 ± 1%, n = 6) of the total NO3−. Compared to the results observed in December 2021 (8~31%), the contribution of aquaculture water to the total NO3− was higher. The most possible reason was that the nitrification in aquaculture ponds may be promoted by the relatively higher T in May 2023, thus exporting more NO3− [41,42,43]. Based on the correlation between NO3− and NH4+ (Figure 5b), the contents of NH4+ derived from aquaculture sewage can also be observed, which ranged from 0.20 to 0.48 mg L−1 (0.33 ± 0.11 mg L−1, n = 6), accounting for 60% ~ 100% of the local NH4+ (Figure 6b). Compared to the results in November 2021, the contribution of aquaculture to NH4+ in May 2023 was lower. There are three possible reasons: (1) during the sampling in May 2023, the cultivation of shrimp was at the initial period, and thus the producing of NH4+ was obviously less than that in November 2021 [13]; (2) the relatively higher T in May 2023 may also promote the conversion of N from NH4+ to NO3−, mainly by microbial nitrification [41,42,43], thereby increasing the flux of NO3− and decreasing the flux of NH4+ from aquaculture ponds; (3) the sediment of clam ponds was typically washed out in August or September [13], which could increase the content of NH4+. Such influence may last for mouths and thus cause significantly higher NH4+ levels in December 2021. Conversely, the different methods for the source analysis of DIN may also be one of the reasons for the different results observed in December 2021 and May 2023, highlighting the needs of long-time monitoring of N-signal derived from aquaculture sewage.
Overall, the above results reveal the significant effects of aquaculture water on DIN in Zhangjiang Estuary. The drainage period of the cultured species here, as well as water temperature, may be the major regulator for the content and composition of DIN. The larger flux of drainage and the lower T in winter may cause the increasing content of NH4+ in Zhangjiang Estuary, while the relatively higher T in summer may promote microbial removal of NH4+. Furthermore, our results also indicate that stable isotopes may provide help in observing the specific effects of aquaculture water on the regional environments, which may be considered in the long-time monitoring and management of coastal aquaculture.

4.2. Aquaculture Increased the Contents of Particulate Organic Matter

The δ13C, δ15N, and the C:N ratio of POM have been widely used to indicate the possible source of organic matter and the incorporation of nutrients into bacteria and phytoplankton in estuary ecosystems [28,29]. In Zhangjiang Estuary, aquaculture water may also be the major source of POM, as large amounts of bio-debris, such as the fecal and shell of the cultured species, as well as the residual algae, were exported in company with the exports of DIN [5,9,47,48]. Besides the direct exports of POM by aquaculture water, the potential increasing of POM by the nutrients derived from aquaculture ponds may also be considered. The results in Section 4.1 have revealed the significant contribution of aquaculture water on DIN in Zhangjiang Estuary, indicating its possible important contribution to POM by promoting the growth and production of algae [49,50]. Our previous study has indicted that phytoplankton contributed about 21.8% of the total POM in Zhangjiang Estuary [27]. To observe more ideal results, the Mixsir mixing model was used instead of the IsoSource mixing model [28,29] to observe the major source of POM in May 2023, and POM in December 2021 was re-analyzed to observe comparable results. Generally, the major source of POM in the study area includes the imports of freshwater, seawater, human-derived sewage, and the production of algae [51,52,53,54,55,56,57,58]. The contribution of zooplankton was also considered, as the promoted production of algae may further facilitate the growth and the metabolism of zooplankton. In addition, as Zhangjiang Estuary is fringed by a large area of natural mangroves, the contribution of mangrove sediments was also considered. The δ13C and C:N ratios of POM were used as tracers during the source analysis of POM, and the characteristic values of the above sources are shown in Table 3. As the δ13C and C:N ratio of aquaculture, agriculture, and domestic sewage have similar range [59,60,61,62], it is hard to distinguish their contribution of POM. Considering that aquaculture water has been identified as the primary source of DIN here, we suggest that its contribution to POM may be more significant than that of the agriculture and domestic sewage. Thus, the reported δ13C and C:N ratio of human-derived sewage was defined as the characteristic values of aquaculture water in this study. Generally, the observed δ13C and C:N ratio of POM during the two sampling periods fell into the cover range of aquaculture sewage, freshwater, and seawater (Figure 7).
The major results are as follows (Figure 8): (1) Aquaculture sewage was the major source of POM, accounting for 24~33% (29 ± 3%, n = 6) of the total POM in November 2021 and 24~32% (29 ± 3%, n = 6) of that in May 2023. (2) Freshwater, seawater, and zooplankton had similar contribution ratios with each other, accounting for 20~23% (22 ± 1%, n = 6), 16~25% (20 ± 3%, n = 6), and 16~23% (19 ± 2%, n = 6) of the total POM in November 2021, and 22~24% (23 ± 1%, n = 6), 17 ~ 25% (20 ± 3%, n = 6), and 15~23% (19± 3%, n = 6) of that in May 2023. (3) Phytoplankton contributed only 5~9% (7 ± 1% in November 2021 and 6 ± 1% in May 2023) of the total POM in the study area. (4) In comparison, mangrove soil had less contribution to the total POM in Zhangjiang Estuary. Compared the results of the two models, the contribution ratio of aquaculture sewage and phytoplankton observed by the Mixsir mixing model were obviously lower, even during the same sampling period. As the Mixsir mixing model cited multiple reported values (POM-δ13C and POM-C: N) and considered their variance [28,29], we propose the results in this new study may be more ideal. Comparing the results in this study, a similar contribution of aquaculture sewage to POM in November 2021 and May 2023 was observed (Figure 8).
The source analysis of DIN has revealed the influence of the cultured species and their drainage period on the content and composition of DIN (Section 4.1). In August–September, the sediments in clam ponds were washed out, thus producing higher contents of NH4+ in December 2021 (Figure 3). However, such a difference may have a limited influence on the contribution of aquaculture water to POM (Figure 8). Thus, we propose that the drainage of shrimp ponds and clam ponds may have relatively less effects on the contents of POM in Zhangjiang Estuary, and the direct contribution of POM by aquaculture in Zhangjiang Estuary may be mainly derived from crab ponds. Apart from the direct contribution, the potential contribution of aquaculture water, mainly by promoting the growth of phytoplankton and zooplankton, may also be important. The positive correlation between POC, PN, and DIN derived from aquaculture was observed (Figure 9). On one hand, the correlations between POC, PN, and DIN derived from aquaculture waters indicate the coupling imports of POM and DIN by aquaculture water. On the other hand, the correlations between POC and PN derived from phytoplankton with DIN derived from aquaculture revealed the enhanced production of phytoplankton by the imported DIN. However, the contribution of phytoplankton to the total POM was not as high as expected. The most possible reason for this is the ingesting of zooplankton, which can be further supported by the negative correlation between the contribution ratio of phytoplankton and zooplankton (r = −0.88, p < 0.05, n = 6). The contribution of phytoplankton and zooplankton may vary with seasons and nutrient conditions; thus, the long-time monitor is needed to reveal their temporal variation and response to N derived from aquaculture.
Generally, the above results indicate that aquaculture water was the primary source of POM in Zhangjiang Estuary, and most of the POM contributed by aquaculture water could be derived from crab ponds. In addition, this study also revealed the potential contribution of aquaculture water to POM, mainly by promoting the growth and metabolism of phytoplankton and zooplankton successively. As such, bio-derived POM play important roles in the biogeochemical cycle of carbon, highlighting the need of long-time investigation of aquaculture water effects on the coastal carbon cycle.

5. Conclusions

This study revealed the coupling imports of DIN and POM by aquaculture ponds in Zhangjiang Estuary. The major conclusions are as follows: (1) aquaculture sewage was the major contributor of DIN (62~86% of the total NO3− and 60~100% of the total NH4+), and the cultured species and their drainage periods have great effects on the content and component of DIN here; (2) aquaculture water also has great contribution to POM (24~33% of the total POM) in the Zhangjiang Estuary, most of which may derived from crab ponds; (3) DIN derived from aquaculture may promote the growth of phytoplankton and zooplankton in succession, thus increasing the content and bioavailability of POM in Zhangjiang Estuary. This study also indicates that the stable isotopes may be efficient in the monitoring of the coastal environment and the management of coastal aquaculture.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/w16142054/s1. Table S1: The major data in this study. Table S2: DIN, POM from different sources.

Author Contributions

Conceptualization, D.L.; methodology, D.L.; software, S.H.; formal analysis, S.H.; investigation, S.H. and Z.L.; data curation, S.H. and D.L.; writing—original draft preparation, S.H.; writing—review and editing, D.L., Z.L. and T.-J.C.; funding acquisition, D.L. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (42306053); the Natural Science Foundation of Fujian Province, China (2021J05156); and the Open fund of the Key Laboratory of Global Change and Marine-Atmospheric Chemistry (GCMAC2310).

Data Availability Statement

Not available.

Acknowledgments

We are grateful to the Zhangjiangkou Wetland Ecosystem Field Research Base of Xiamen University for the help while sampling, as well as the sharing of background information.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. FAO. The State of World Fisheries and Aquaculture 2024; Blue Transformation in Action; Food and Agriculture Organization of the United Nations: Rome, Italy, 2024. [Google Scholar] [CrossRef]
  2. Hargreaves, J.A. Nitrogen biogeochemistry of aquaculture ponds. Aquaculture 1998, 166, 181–212. [Google Scholar] [CrossRef]
  3. Huang, X.P.; Guo, F.; Huang, L.M. Distribution characteristics and pollution of nitrogen and phosphorus in core sediments of marine culture area in Dapeng Cove. J. Trop. Oceanogr. 2010, 29, 91–97, (In Chinese with English Abstract). [Google Scholar] [CrossRef]
  4. Wu, R.; Lam, K.; MacKay, D.; Lau, T.; Yam, V. Impact of marine fish farming on water quality and bottom sediment: A case study in the sub-tropical environment. Mar. Environ. Res. 1994, 38, 115–145. [Google Scholar] [CrossRef]
  5. Alongi, D.M. Carbon cycling and storage in mangrove forests. Annu. Rev. Mar. Sci. 2014, 6, 195–219. [Google Scholar] [CrossRef] [PubMed]
  6. Bianchi, T.S. The Role of terrestrially derived organic carbon in the coastal ocean: A changing paradigm and the priming effect. Proc. Natl. Acad. Sci. USA 2011, 108, 19473–19481. [Google Scholar] [CrossRef] [PubMed]
  7. Naylor, R.; Burke, M. Aquaculture and ocean resources: Raising tigers of the sea. Annu. Rev. Environ. Resour. 2005, 30, 185–218. [Google Scholar] [CrossRef]
  8. Trott, L.A.; Alongi, D.M. The impact of shrimp pond effluent on water quality and phytoplankton biomass in a tropical mangrove estuary. Mar. Pollut. Bull. 2000, 40, 947–951. [Google Scholar] [CrossRef]
  9. Reis, C.R.G.; Reed, S.C.; Oliveira, R.S.; Nardoto, G.B. Isotopic evidence that nitrogen enrichment intensifies nitrogen losses to the atmosphere from subtropical mangroves. Ecosystems 2019, 22, 1126–1144. [Google Scholar] [CrossRef]
  10. Mckinnon, A.D.; Trott, L.A.; Alongi, D.M.; Davidson, A. Water column production and nutrient characteristics in mangrove creeks receiving shrimp farm effluent. Aquac. Res. 2002, 33, 55–73. [Google Scholar] [CrossRef]
  11. Kristensen, E.; Bouillon, S.; Dittmar, T.; Marchand, C. Organic carbon dynamics in mangrove ecosystems: A review. Aqua. Bot. 2008, 89, 201–219. [Google Scholar] [CrossRef]
  12. Guallar, C.; Flos, J. Linking phytoplankton primary production and chromophoric dissolved organic matter in the sea. Prog. Oceanogr. 2019, 176, 102116. [Google Scholar] [CrossRef]
  13. Wu, H.; Peng, R.; Yang, Y.; He, L.; Wang, W.Q.; Zheng, T.L.; Lin, G.H. Mariculture pond influence on mangrove areas in South China: Significantly larger nitrogen and phosphorus loadings from sediment wash-out than from tidal water exchange. Aquaculture 2014, 426–427, 204–212. [Google Scholar] [CrossRef]
  14. Feng, Y.Y.; Hou, L.C.; Ping, N.X.; Ling, T.D.; Kyo, C.I. Development of mariculture and its impacts in Chinese coastal waters. Rev. Fish Biol. Fish. 2004, 14, 1–10. [Google Scholar] [CrossRef]
  15. Graslund, S.; Holmstrom, K.; Wahstrom, A. A field survey of chemicals and. biological products used in shrimp farming. Mar. Pollut. Bull. 2003, 46, 81–90. [Google Scholar] [CrossRef] [PubMed]
  16. Chen, G.C.; Chen, B.; Yu, D.; Tam, N.; Ye, Y.; Chen, S.Y. Soil greenhouse gas emissions reduce the contribution of mangrove plants to the atmospheric cooling effect. Environ. Res. Lett. 2016, 11, 1–10. [Google Scholar] [CrossRef]
  17. Castillo, J.A.A.; Apan, A.A.; Maraseni, T.N.; Salmo, S.G. Soil greenhouse gas fluxes in tropical mangrove forests and in land uses on deforested mangrove lands. Catena 2017, 159, 60–69. [Google Scholar] [CrossRef]
  18. Ho, D.T.; Ferrón, S.; Engel, V.C.; Larsen, L.G.; Barr, J.G. Air-water gas exchange and CO2 flux in a mangrove-dominated estuary. Geophys. Res. Lett. 2014, 41, 108–113. [Google Scholar] [CrossRef]
  19. Stein, L.Y.; Lidstrom, M.E. Greenhouse gas mitigation requires caution. Science 2024, 284, 1068–1069. [Google Scholar] [CrossRef]
  20. Liu, K.K.; Kao, S.J.; Wen, L.S.; Chen, K.L. Carbon and nitrogen isotopic compositions of particulate organic matter and biogeochemical processes in the eutrophic Danshuei esturary in Northern Taiwan. Sci. Total. Environ. 2007, 382, 103–120. [Google Scholar] [CrossRef]
  21. Yang, B.; Cao, L.; Liu, S.M.; Zhang, G.S. Biogeochemistry of bulk organic matter and biogenic elements in surface sediments of the Yangtze River estuary and Adjacent Sea. Mar. Pollut. Bull. 2015, 96, 471–484. [Google Scholar] [CrossRef]
  22. Hu, J.F.; Peng, P.A.; Jia, G.D.; Mai, B.X.; Zhang, G. Distribution and sources of organic carbon, nitrogen and their isotopes in sediments of the subtropical Pearl River estuary and the adjacent shelf, Southern China. Mar. Chem. 2006, 98, 274–285. [Google Scholar] [CrossRef]
  23. Yue, F.J.; Liu, C.Q.; Li, S.L.; Zhao, Z.Q.; Liu, X.L.; Ding, H.; Liu, B.J.; Zhong, J. Analysis of δ15N and δ18O to identify nitrate sources and transformations in Songhua River, Northeast China. J. Hydrol. 2014, 519, 329–339. [Google Scholar] [CrossRef]
  24. Liu, C.Q.; Li, S.L.; Lang, Y.C.; Xiao, H.Y. Using δ15N- and δ18O-values to identify nitrate sources in karst ground water, Guiyang, Southwest China. Environ. Sci. Technol. 2006, 40, 6928–6933. [Google Scholar] [CrossRef] [PubMed]
  25. Wang, F.F.; Xiao, K.; Santos, I.R.; Lu, Z.Y.; Tamborski, J.; Wang, Y.; Yan, R.F.; Chen, N.W. Porewater exchange drives nutrient cycling and export in a mangrove-salt marsh ecotone. J. Hydrol. 2022, 606, 127401. [Google Scholar] [CrossRef]
  26. Wu, H.; Liu, J.L.; Bi, X.Y.; Lin, G.H.; Feng, C.C.; Li, Z.J.; Qi, F.; Zheng, T.L.; Xie, L.Q. Trace metals in sediments and benthic animals from aquaculture ponds near a mangrove wetland in Southern China. Mar. Pollut. Bull. 2017, 117, 486–491. [Google Scholar] [CrossRef] [PubMed]
  27. Li, D.Y.; Yan, J.P.; Lu, Z.Q.; Chu, T.S.; Li, J.; Chu, T.J. Use of δ13C and δ15N as Indicators to Evaluate the Influence of Sewage on Organic Matter in the Zhangjiang Mangrove–Estuary Ecosystem, Southeastern China. Water 2023, 15, 3660. [Google Scholar] [CrossRef]
  28. Moore, J.W.; Semmens, B.X. Incorporating uncertainty and prior information into stable isotope mixing models. Ecol. Lett. 2008, 11, 470–480. [Google Scholar] [CrossRef] [PubMed]
  29. Parnell, A.C.; Inger, R.; Bearhop, S.; Jackson, A.L.; Rands, S. Source partitioning using stable isotopes: Coping with too much variation. PLoS ONE. 2010, 5, e9672. [Google Scholar] [CrossRef]
  30. Sigman, D.M.; Casciotti, K.L.; Andréani, M.; Barford, C.; Galanter, M.; Böhlke, J.K. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal. Chem. 2001, 73, 4145–4153. [Google Scholar] [CrossRef]
  31. Casciotti, K.L.; Sigman, D.M.; Hastings, M.G.; Böhlke, J.K.; Hilkert, A. Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method. Anal. Chem. 2002, 74, 4905–4912. [Google Scholar] [CrossRef]
  32. Koba, K.; Inagaki, K.; Sasaki, Y.; Takebayashi, Y.; Yoh, M. Nitrogen isotopic analysis of dissolved inorganic and organic nitrogen in soil extracts. In Earth, Life and Isotopes; Ohkouchi, N., Tayasu, I., Koba, K., Eds.; Kyoto University Press: Kyoto, Japan, 2010; pp. 17–36. [Google Scholar]
  33. Holmes, R.M.; McClelland, J.W.; Sigman, D.M.; Fry, B.; Peterson, B.J. Measuring 15N-NH4/+ in marine, estuarine and fresh waters: An adaptation of the ammonia diffusion method for samples with low ammonium concentrations. Mar. Chem. 1998, 60, 235–243. [Google Scholar] [CrossRef]
  34. Tsunogai, U.; Kido, T.; Hirota, A.; Ohkubo, S.B.; Komatsu, D.D.; Nakagawa, F. Sensitive determinations of stable nitrogen isotopic composition of organic nitrogen through chemical conversion into N2O. Rapid Commun. Mass Spectrom. 2008, 22, 345–354. [Google Scholar] [CrossRef] [PubMed]
  35. Lachouani, P.; Frank, A.H.; Wanek, W. A suite of sensitive chemical methods to determine the δ15N of ammonium, nitrate and total dissolved N in soil extracts. Rapid Commun. Mass Spectrom. 2010, 24, 3615–3623. [Google Scholar] [CrossRef] [PubMed]
  36. Li, H. The distribution characteristics of nutritive salt in Dongshan Bay and its interrelation with Chlorophyll. Environ. Dev. 2019, 11, 119–122, (In Chinese with English Abstract). [Google Scholar] [CrossRef]
  37. Page, H.M.; Lastra, M. Diet of intertidal bivalves in the Ria de Arosa (NW Spain): Evidence from Stable C and N isotope analysis. Mar. Biol. 2003, 143, 519–532. [Google Scholar] [CrossRef]
  38. Xu, Q.; Yang, H.S. Food sources of three bivalves living in two habitats of Jiaozhou Bay (Qingdao, China): Indicated by lipid biomarkers and stable isotope analysis. J. Shellfish Res. 2007, 26, 561–567. [Google Scholar] [CrossRef]
  39. Seitzinger, S. Out of reach. Nature 2008, 452, 162–163. [Google Scholar] [CrossRef] [PubMed]
  40. Lin, L.; Xu, W.; Liu, L.; Wang, F.; Yang, S.; Cao, W. Assessment of impacts of river nutrient input and structural changes on estuarine eutrophication potential. J. Lake Sci. 2023, 35, 1990–1999, (In Chinese with English Abstract). [Google Scholar]
  41. Denk, T.R.A.; Mohn, J.; Decock, C.; Lewicka-Szczebak, D.; Harris, E.; Butterbach-Bahl, K.; Kiese, R.; Wolf, B. The nitrogen cycle: A review of isotope effects and isotope modeling approaches. Soil Biol. Biochem. 2017, 105, 121–137. [Google Scholar] [CrossRef]
  42. McLaughlin, K.; Nezlin, N.P.; Howard, M.; Beck, C.D.; Kudela, R.M.; Mengel, M.J.; Robertson, G.L. Rapid nitrification of wastewater ammonium near coastal ocean outfalls, Southern California, USA. Estuar. Coast. Shelf Sci. 2017, 186, 263–275. [Google Scholar] [CrossRef]
  43. Archana, A.; Thibodeau, B.; Geeraert, N.; Xu, M.N.; Kao, S.; Baker, D.M. Nitrogen sources and cycling revealed by dual isotopes of nitrate in a complex urbanized environment. Water Res. 2018, 142, 459–470. [Google Scholar] [CrossRef] [PubMed]
  44. Xing, M.; Liu, W.G. Nitrate source proportional contributions in the Chanhe and Bahe rivers—Using its isotopic ratios in combination with a Bayesian isotope mixing mode. Earth Sci.-China 2016, 7, 27–36, (In Chinese with English Abstract). [Google Scholar] [CrossRef]
  45. Wu, W.H.; He, X.J.; Su, Y.L.; Wang, X.Z. Review on identifying nitrogen pollution sources in water based on the nitrogen and oxygen stable isotope. Environ. Sci. Technol. 2016, 39, 77–84, (In Chinese with English Abstract). [Google Scholar]
  46. Zeng, H.A.; Wu, J.L. A method to extract ammonium and nitrate from freshwater for nitrogen isotope analysis. Mar. Geol. Quat. Geol. 2013, 33, 173–177. [Google Scholar] [CrossRef]
  47. Green, P.A.; Vörösmarty, C.J.; Meybeck, M.; Galloway, J.N.; Peterson, B.J.; Boyer, E.W. Preindustrial and contemporary fluxes of nitrogen through rivers: A global assessment based on typology. Biogeochemistry 2004, 68, 71–105. [Google Scholar] [CrossRef]
  48. Neumann, B.; Vafeidis, A.T.; Zimmermann, J.; Nicholls, R.J. Future coastal population growth and exposure to sea level rise and coastal flooding: A global assessment. PLoS ONE 2015, 10, e0131375. [Google Scholar] [CrossRef]
  49. DiFiore, P.J.; Sigman, D.M.; Karsh, K.L.; Trull, T.W.; Dunbar, R.B.; Robinson, R.S. Poleward decrease in the isotope effect of nitrate assimilation across the Southern Ocean. Geophys. Res. Lett. 2010, 37, L17601. [Google Scholar] [CrossRef]
  50. Emerson, S.; Hedges, J. Chemical Oceanography and the Marine Carbon Cycle; Cambridge University Press: Cambridge, UK, 2008; pp. 134–172. [Google Scholar] [CrossRef]
  51. Tucker, J.; Sheats, N.; Giblin, A.E.; Hopkinson, C.; Montoya, J.P. Using stable isotopes to trace sewage derived material through Boston harbor and Massachusetts bay. Mar. Environ. Res. 1999, 48, 353–375. [Google Scholar] [CrossRef]
  52. Ostrom, N.E.; Macko, S.A.; Deibel, D.; Thompson, R.J. Seasonal variation in the stable carbon and nitrogen isotope biogeochemistry of a coastal cold ocean environment. Geochim. Cosmochim. Acta 1997, 61, 2929–2942. [Google Scholar] [CrossRef]
  53. Mcclelland, J.W.; Valiela, I. Linking nitrogen in estuarine producers to land derived sources. Limnol. Oceanogr. 1998, 43, 577–585. [Google Scholar] [CrossRef]
  54. Lehmann, M.F.; Bernasconi, S.M.; Barbieri, A.; McKenzie, J.A. Preservation of organic Matter and alteration of its carbon and nitrogen isotope composition during simulated and in Situ early sedimentary diagenesis. Geochim. Cosmochim. Acta 2002, 66, 3573–3584. [Google Scholar] [CrossRef]
  55. Wang, X.C.; Ma, H.Q.; Li, R.H.; Song, Z.S.; Wu, J.P. Seasonal fluxes and source variation of organic carbon transported by two major Chinese rivers: The Yellow river and Changjiang (Yangtze) river. Glob. Biogeochem. Cycles 2012, 26, 1–10. [Google Scholar] [CrossRef]
  56. Yu, F.L.; Zong, Y.Q.; Lloyd, J.M.; Huang, G.Q.; Leng, M.J.; Kendrick, C.; Lamb, A.L.; Yim, W.W. Bulk organic δ13C and C/N as indicators for sediment sources in the Pearl river delta and estuary, Southern China. Estuar. Coast. Shelf Sci. 2010, 87, 618–630. [Google Scholar] [CrossRef]
  57. Cai, D.L.; Tan, F.C.; Edmond, J.M. Sources and transport of particulate organic carbon in the Amazon river and estuary. Estuar. Coast. Shelf Sci. 1988, 26, 1–14. [Google Scholar] [CrossRef]
  58. Mortillaro, J.M.; Abril, G.; Moreira-Turcq, P.; Sobrinho, R.L.; Perez, M.; Meziane, T. Fatty acid and stable isotope (δ13C, δ15N) signatures of particulate organic matter in the lower Amazon river: Seasonal contrasts and connectivity between Floodplain lakes and the mainstem. Org. Geochem. 2011, 42, 1159–1168. [Google Scholar] [CrossRef]
  59. Li, S.L. Carbon and Nitrogen Isotope Geochemistry of Karst Groundwater in City: Implications for Contamination Transportation and Transformation; University of Chinese Academy of Sciences: Beijing, China, 2005; (In Chinese with English Abstract). [Google Scholar]
  60. Wang, C.Y.; Guo, Q.J.; Zhu, G.X.; Peters, M.; Yang, J.X.; Zhang, H.Z.; Wei, R.F.; Tian, L.Y.; Wan, Y.X. Applying stable carbon isotope techniques to detect different sources of organic matters in lake sediments from Beijing parks. Chin. J. Ecol. 2014, 33, 778–785, (In Chinese with English Abstract). [Google Scholar] [CrossRef]
  61. Wang, Z.L.; Li, J.; Liu, C.Q.; Zhu, Z.Z.; Li, Y. Using Stable Carbon Isotopes to Identify the Sources of Organic Carbon in Surface Waters of the Tianjin District. Earth Environ. 2011, 39, 1–8, (In Chinese with English Abstract). [Google Scholar]
  62. Zhen, S.; Zhu, W. Analysis of isotope tracing of domestic sewage sources in Taihu Lake—A case study of Meiliang Bay and Gonghu Bay. Ecol. Indic. 2016, 66, 113–120. [Google Scholar] [CrossRef]
  63. Currin, C.A.; Newell, S.; Paerl, H. The role of standing dead Spartina alterniflora and benthic microalgae in salt marsh food webs: Considerations based on multiple stable isotope analysis. Mar. Ecol. Prog. Ser. 1995, 121, 99–116. [Google Scholar] [CrossRef]
  64. Shang, X.; Zhang, G.S.; Zhang, J. Relative importance of vascular plants and algal production in the food web of a Spartina-invaded salt marsh in the Yangtze River estuary. Mar. Ecol. Prog. Ser. 2008, 367, 93–107. [Google Scholar] [CrossRef]
  65. Gaston, T.F.; Suthers, I.M. Spatial variation in δ13C and δ15N of liver, muscle and bone in a rocky reef planktivorous fish: The relative contribution of sewage. J. Exp. Mar. Biol. Ecol. 2004, 304, 17–33. [Google Scholar] [CrossRef]
  66. Goering, J.; Alexander, V.; Haubenstock, N. Seasonal variability of stable carbon and nitrogen isotope ratios of organisms in a North Pacific Bay. Estuar. Coast. Shelf Sci. 1990, 30, 239–260. [Google Scholar] [CrossRef]
  67. Ji, N.N.; Liu, Y.; Wang, S.R. The sources characteristics of stable isotope organic carbon and nitrogen in suspended particles and surface sediments in Lake Erhai and their water quality implications. J. Lake Sci. 2022, 34, 118–133, (In Chinese with English Abstract). [Google Scholar] [CrossRef]
  68. Kang, C.; Kim, J.B.; Lee, K.; Kim, J.B.; Lee, P.Y.; Hong, J. Trophic importance of benthic microalgae to macrozoobenthos in coastal bay systems in Korea: Dual stable C and N isotope analyses. Mar. Ecol. Prog. Ser. 2003, 259, 79–92. [Google Scholar] [CrossRef]
  69. Middelburg, J.J.; Nieuwenhuize, J. Carbon and nitrogen stable isotopes in suspended matter and sediments from the Schelde Estuary. Mar. Chem. 1998, 60, 217–225. [Google Scholar] [CrossRef]
  70. Ogrinc, N.; Markovics, R.; Kanduč, T.; Walter, L.M.; Hamilton, S.K. Sources and transport of carbon and nitrogen in the River Sava watershed, a major tributary of the River Danube. Appl. Geochem. 2008, 23, 3685–3698. [Google Scholar] [CrossRef]
  71. Redfield, A.C.; Ketchum, B.H.; Richards, F.A. The influence of organisms on the composition of sea-water. Sea 1963, 2, 26–77. [Google Scholar]
  72. Zeng, H.A.; Wu, J.L. Isotopic tracing of terrestrial contribution to organic matter of sediments in the estuary of TaiHu Lake basin. Mar. Geol. Quat. Geol. 2009, 29, 109–114, (In Chinese with English Abstract). [Google Scholar] [CrossRef]
  73. Wu, G. Organic Carbon Sources and Microbial Carbon Assimilation in Mangrove Ecosystems. Ph.D. Thesis, Xiamen University, Fujian, China, 2018. (In Chinese with English Abstract). [Google Scholar]
  74. Choy, E.J.; Richard, P.; Kim, K.R.; Kang, C.K. Quantifying the trophic base for benthic secondary production in the Nakdong River estuary of Korea using stable C and N isotopes. J. Exp. Mar. Biol. Ecol. 2009, 382, 18–26. [Google Scholar] [CrossRef]
  75. Hillebr, H.; Sommer, U. The nutrient stoichiometry of benthic microalgal growth: Redfield proportions are optimal. Limnol. Oceanogr. 1999, 44, 440–446. [Google Scholar] [CrossRef]
  76. Kanaya, G.; Takagi, S.; Kikuchi, E. Spatial dietary variations in Laternula marilina (Bivalva) and Hediste spp.(Polychaeta) along environmental gradients in two brackish lagoons. Mar. Ecol. Prog. Ser. 2008, 359, 133–144. [Google Scholar] [CrossRef]
  77. Ning, J.J.; Liu, H.; Gu, B.H.; Liu, Z.W. Carbon and nitrogen stable isotope characteristics of particulate organic matter and zooplankton in Liuxihe Reservoir. Acta Ecol. Sin. 2012, 32, 1502–1509, (In Chinese with English Abstract). [Google Scholar] [CrossRef]
  78. Yokoyama, H.; Sakami, T.; Ishihi, Y. Food sources of benthic animals on intertidal and subtidal bottoms in inner Ariake Sound, southern Japan, determined by stable isotopes. Estuar. Coast. Shelf Sci. 2009, 82, 243–253. [Google Scholar] [CrossRef]
  79. Zhang, N.X.; Song, J.M.; He, Z.P. Biogeochemical mechanism of particulate organic carbon(POC) variations in seawaters. Acta Ecol. Sin. 2006, 26, 2328–2339, (In Chinese with English Abstract). [Google Scholar]
Water 16 02054 g001
Figure 1. The sampling stations in Zhangjiang Estuary in May 2023.
Figure 1. The sampling stations in Zhangjiang Estuary in May 2023.
Water 16 02054 g001
Water 16 02054 g002
Figure 2. Comparison of physicochemical parameters observed in May 2023 and December 2021.
Figure 2. Comparison of physicochemical parameters observed in May 2023 and December 2021.
Water 16 02054 g002
Water 16 02054 g003
Figure 3. The contents and isotopic values of nitrate and ammonium.
Figure 3. The contents and isotopic values of nitrate and ammonium.
Water 16 02054 g003
Water 16 02054 g004
Figure 4. The contents and isotopic values of particulate organic matter: (a) the results in May 2023; (b) the comparison of POM content in December 2021 and May 2023.
Figure 4. The contents and isotopic values of particulate organic matter: (a) the results in May 2023; (b) the comparison of POM content in December 2021 and May 2023.
Water 16 02054 g004
Water 16 02054 g005
Figure 5. The content correlation and isotopic values of nitrate and ammonium in May 2023: (a) the correlation matrix of the observed parameters in May 2023; (b) the correlation between nitrate and ammonium contents; (c) the isotopic characteristics of nitrate observed in May 2023, which was shown by the blue dot.
Figure 5. The content correlation and isotopic values of nitrate and ammonium in May 2023: (a) the correlation matrix of the observed parameters in May 2023; (b) the correlation between nitrate and ammonium contents; (c) the isotopic characteristics of nitrate observed in May 2023, which was shown by the blue dot.
Water 16 02054 g005
Water 16 02054 g006
Figure 6. The significant contribution of aquaculture sewage to the total (a) nitrate and (b) ammonium in May 2023.
Figure 6. The significant contribution of aquaculture sewage to the total (a) nitrate and (b) ammonium in May 2023.
Water 16 02054 g006
Water 16 02054 g007
Figure 7. The δ13C and C:N ratio of particulate organic matter in May 2023.
Figure 7. The δ13C and C:N ratio of particulate organic matter in May 2023.
Water 16 02054 g007
Water 16 02054 g008
Figure 8. The contribution ratio of the possible sources to particulate organic matter in Zhangjiang Estuary.
Figure 8. The contribution ratio of the possible sources to particulate organic matter in Zhangjiang Estuary.
Water 16 02054 g008
Water 16 02054 g009
Figure 9. The correlation matrix of particulate organic matter and dissolved inorganic nitrogen derived from aquaculture water and phytoplankton in May 2023.
Figure 9. The correlation matrix of particulate organic matter and dissolved inorganic nitrogen derived from aquaculture water and phytoplankton in May 2023.
Water 16 02054 g009
Table 1. The physicochemical parameters in Zhangjiang Estuary in May 2023.
Table 1. The physicochemical parameters in Zhangjiang Estuary in May 2023.
StationT (°C)S (‰)DO (mg L−1)Phycoerythrin (μg L−1)Chl a (μg L−1)
S225.5 12.7 7.4010.1 4.30
S325.1 15.3 6.973.43 3.69
S424.7 19.0 6.583.42 6.37
S524.0 20.5 6.980.72 3.39
S624.2 24.5 6.751.29 2.77
S723.7 27.6 6.930.75 1.99
S823.7 30.1 6.65 0.58 2.14
Table 2. δ15N and δ18O of nitrate derived from different sources.
Table 2. δ15N and δ18O of nitrate derived from different sources.
Sourceδ15N (‰)δ18O (‰)References
Seawater7.158.97This study
Freshwater10.406.13This study
Aquaculture sewage20.755.24This study
Agriculture sewage0.300.88[24,44]
Domestic sewage8.018.74[45,46]
Table 3. δ13C and C:N ratio of particulate organic matter derived from different sources.
Table 3. δ13C and C:N ratio of particulate organic matter derived from different sources.
Sourceδ13C (‰)C:N RatioReferences
Mangrove soil−25.2412.34This study
Aquaculture sewage−27.684.05This study, [59,60,61,62]
Phytoplankton−21.107.77[63,64,65,66,67,68,69,70,71,72]
Freshwater−25.384.49This study, [73]
Seawater−23.174.05This study, [73]
Zooplankton−28.903.45[64,67,68,74,75,76,77,78,79]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

He, S.; Chu, T.-J.; Lu, Z.; Li, D. Coupling Imports of Dissolved Inorganic Nitrogen and Particulate Organic Matter by Aquaculture Sewage to Zhangjiang Estuary, Southeastern China. Water 2024, 16, 2054. https://doi.org/10.3390/w16142054

AMA Style

He S, Chu T-J, Lu Z, Li D. Coupling Imports of Dissolved Inorganic Nitrogen and Particulate Organic Matter by Aquaculture Sewage to Zhangjiang Estuary, Southeastern China. Water. 2024; 16(14):2054. https://doi.org/10.3390/w16142054

Chicago/Turabian Style

He, Shuang, Ta-Jen Chu, Zhiqiang Lu, and Danyang Li. 2024. "Coupling Imports of Dissolved Inorganic Nitrogen and Particulate Organic Matter by Aquaculture Sewage to Zhangjiang Estuary, Southeastern China" Water 16, no. 14: 2054. https://doi.org/10.3390/w16142054

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop