Impact of Rice-Catfish/Shrimp Co-culture on Nutrients Fluxes Across Sediment-Water Interface in Intensive Aquaculture Ponds

Liu Yaobin, Qin Lin, Li Fengbo, Zhou Xiyue, Xu Chunchun, Ji Long, Chen Zhongdu, Feng Jinfei, Fang Fuping

Research Paper

Impact of Rice-Catfish/Shrimp Co-culture on Nutrients Fluxes Across Sediment-Water Interface in Intensive Aquaculture Ponds

Liu Yaobin1, #, Qin Lin3, #, Li Fengbo1, 2, Zhou Xiyue1, Xu Chunchun1, Ji Long1, Chen Zhongdu1, Feng Jinfei1, Fang Fuping1

(China National Rice Research Institute, Hangzhou 310006, China; Integrated and Urban Plant Pathology Laboratory, Université de Liège, Gembloux B-5030, Belgium; Analysis and Determination Center, Sichuan Academy of Agricultural Sciences, Chengdu 610000, China; These authors contributed equally to this work)

Exchange of nitrogen and phosphorus across sediment-water interface plays an important role in the management of nutrient recycling in the aquaculture pond. In this study, a plot experiment was conducted to study the effect of rice-catfish/shrimp co-culture on the micro-profile of oxygen (O2), pH and nutrient exchange across sediment-water interface in the intensive culture ponds. The results showed that rice-catfish co-culture increased the concentration and penetrating depth of O2, but decreased the pH value across the sediment-water interface, compared with catfish monoculture. Additional rice cultivation significantly reduced the flux rates of ammonium (NH4+) and nitrate (NO3-) across sediment-water interface in the catfish and shrimp ponds. The flux rates of NO2-and soluble phosphorus (PO43-) showed no significant difference between rice-catfish/shrimp co-culture ponds and catfish/shrimp monoculture ponds. Rice only affected the dissolved inorganic nitrogen and phosphorus fractions in the sediment. The concentrations of NH4+were significantly lower in the sediment of co-culture ponds than in the monoculture ponds. Additional rice cultivation also significantly reduced the content and percentage of dissolved inorganic phosphorus in the sediment of catfish ponds.

sediment-water interface; rice-fish co-culture; eutrophication; nitrogen and phosphorus recycling; aquaculture

Pond aquaculture plays an important role in the inland fish production. The area of pond aquaculture was estimated to be 16.7 × 106hm2in 2011 around the world (Jescovitch, 2014). As in China, the largest fishery nation, pond aquaculture accounted for 71.9% of the total production of freshwater fish. Intensive culture, characterized by high stocking density of fish with high input of pelleted feed, has been widely adopted in pond aquaculture to achieve high yield and benefit in the last three decades (Bosma and Verdegem, 2011; Li et al, 2011). However, intensive culture in ponds has induced serious environmental concerns, such as eutrophication and salinization (Martinezporchas and Martinezcordova, 2012; Sun et al, 2018). Nutrient budgets showed that only 23.0%–46.5% of the nitrogen and phosphorus in the feed is utilized by aquatic animals (Briggs and Fvnge-Smith, 1994; Jackson et al, 2003; Zhang et al, 2018). The remainder is retained in the pond or discharged to surrounding water bodies.

A large portion (48.0%–86.3%) of un-utilized nitrogen (N) and phosphorus (P) and in residual feeds and fish excretes is deposited to the bottom soil (Hargreaves, 1998; Zhang et al, 2018). The amount of nutrients accumulated in surface bottom soil is usually several times higher than that in the water column (Avnimelech and Ritvo, 2003). The transformation and release of N and P in the bottom soil are key issues of nutrient recycling in pond aquaculture system (Avnimelech and Ritvo, 2003).

Exchange of N and P across the sediment-water interface is a primary pathway regulating the nutrients fluxed from bottom soil to the water. Many previous studies have investigated the characteristics of nutrient fluxes across the sediment-water interface of lake, reservoir, river, estuarine and coastal systems (Nowlin et al, 2005; Helali et al, 2016; Qiu et al, 2016; Mu et al, 2017; Yang et al, 2017; Boynton et al, 2018). The nutrient flux rates are affected by many environmental factors, such as the pH and hypoxia of sediment, bioturbation and hydrodynamic condition, and show great spatial and temporal variations among different aquatic systems (Boynton et al, 2018; Lei et al, 2018). In recent years, increasing attentions have been paid to the impact of aquaculture on the nutrient exchange across sediment- water interface. For example, Petranich et al (2018) measured the seasonal changes of nutrient fluxes across the sediment-water interface in a coastal shrimp farm. Cheng et al (2014) monitored the nutrient release from the sediment at the floating cage aquaculture areas of Daya Bay. However, most of these studies focus on coastal or seawater culture areas. The study on inland freshwater aquaculture is still limited.

Co-culturing with aquatic plants, including natural macrophytes, rice and vegetables, is a recommend measure to re-use the residual nutrients and to reduce the eutrophication in aquaculture ponds. Many previous studies have examined the effects of these aquatic plants on the restoration of water quality in the intensive aquaculture pond (Henry-Silva and Camargo, 2006; Ferdoushi et al, 2008; Akinbile and Yusoff, 2011; Lin et al, 2013; Feng et al, 2016). These studies primarily focused on the direct absorption of N and P in the water or bottom soil. The effect of aquatic plants on the nutrient exchange across sediment-water interface has rarely been studied. Rice is the only cereal crop that can be planted in aquaculture ponds and has the inherent advantage in the co-culture with aquatic animals. Therefore, in this study, we selected two rice-fish co-culture systems (yellow catfish-rice and freshwater shrimp-rice) to investigate the effect of rice-fish co-culture on the micro-profile of pH and dissolved oxygen (DO) across sediment-water interface in the intensive aquaculture ponds, the flux rates of inorganic N and P across sediment-water interface, and the fractions of N and P in the sediment.

Materials and Methods

Experiment design

This experiment was carried out in the experimental farm of China National Rice Research Institute (30o05′ N, 119o95′ E) in Zhejiang Province, China. Four treatments, including yellow catfish monoculture (YC), yellow catfish-rice co-culture (YC-R), freshwater shrimp monoculture (FS), and freshwater shrimp-rice co-culture (FS-R), with three replications were arranged in 12 experiment plots. The size of each plot was 10 m long and 8 m wide. Rice was planted in the central region of the co-culture plots, accounting for about 60% of the total area. The images of monoculture and co-culture plots are showed in Fig. 1.

A new high-stalk rice variety Yudao 1, specially developed for aquaculture pond, was used. The rice variety can grow up to 1.85 m,and can be planted into pond with the water depth below 1.5 m. Rice seeds were sown on a nursery bed on 29 May in 2015, and transplanted to co-culture plots at a spacing of 0.6 m × 0.6 m on 30 June in 2015. The water level was 0.1 m when rice seedlings were transplanted and rose gradually with the height of rice increasing. The maximum water level was 1.0 m for all the plots. The rice was harvested on 5 November in 2015. The rice yields were 457.7 and 392.9 g/m2for YC-R and FS-R, respectively. No fertilizer and pesticide were used for rice cultivation. The fingerlings of yellow catfish and freshwater shrimp were stocked into plots with a density of 15 and 45 fingerlings/m2on 12 August in 2015, respectively. Commercial pelleted feeds were fed two times per day for yellow catfish and one time per day for freshwater shrimp, respectively. The management practices for yellow catfish and freshwater shrimp were similar in the co-culture and monoculture ponds. The fish or shrimp yields were 344.9, 345.8, 29.1 and 35.9 g/m2for YC-R, YC, FS-R and FS, respectively.

Fig. 1. Images of rice-catfish/shrimp co-culture (A) and monoculture (B) ponds.

Sampling and chemical analysis methods

Nutrient flux rates across the sediment-water interface were measuredusing benthic chambers (Niencheski and Jahnke, 2002), which was constructed from a cylindrical plastic pipe with an inside diameter of 40 cm and a height of 30 cm. The bottom water samples were collected before the chambers were deployed. The chambers were manually placed at the central region of each plot, and the total incubation time was 6 h. Water samples were taken from inside the chambers every 2 h using 100-mL plastic syringes through a silicone tube connected to the chambers. NH4+, NO3-, NO2-and PO43-in these water samples were analyzed. Nutrient flux rates were calculated by the following formula:

=/× (/)

Where,is the flux rates of nutrients [mmol/(m2·h)],/is the slope of nutrient content changing with time in the chamber [mmol/(L·h)],is the volume of incubated water (L), andis the bottom area of chamber (m2). The flux rates of inorganic N and P were measured every two weeks from the fish stocking to rice harvest. The surface water samples and bottom sediment samples were collected at the same day as benthic incubation.

Micro-profile of pH and O2across sediment-water interface was measured using microelectrode (Unisense, pH-50, O2-50, Denmark) (Andersen et al, 2006). Sediment cores (inner diameter: 7 cm, height: 15 cm) were collected from YC-R and YC plots at the middle stage of rice-fish co-culture season. The height of the sediment in the cores was approximately 10 cm with a water column of 2 cm. O2and pH values were measured in the profiles from the water phase and down to a depth of 3 cm. The microelectrode was controlled by a micro manipulator and advanced in 1 mm steps from water phase down to sediment. Three replicated profiles were measured for each core.

The concentrations of N and P in water samples, including total N (TN), total P (TP), NH4+, NO3-, NO2-and PO43-, and inorganic N and P in sediment (NH4+, NO3-and PO43-) were measured using an AA3 Auto Analyzer (Bran-lube, GmbH Co., Germany) according to the classical colorimetric methods. The contents of turbidity, total suspended solid (TSS), biological oxygen demand (BOD) and chemical oxygen demand (COD) of water samples were analyzed using standard methods (SEPA, 2002). The pH and DO in the water were measured by portable apparatus (Mettler Toledo, Seven2Go Pro S9; Mettler Toledo, SG2). The contents of TN and TP in the sediment were determined by the Kjeldahl and H2SO4-H2O2methods, respectively (Lu, 2000). P fractions [(residual P (Res-P), Fe- and Al-bound organic P (Fe/Al-OP), Fe- and Al-bound inorganic P (Fe/Al-IP), Ca-bound P (Ca-P) and dissolved inorganic phosphorus (DIP)] in the sediment were determined by the chemical sequential extraction method (Kapanen, 2008).

Statistical analysis

The statistical analysis was conducted using the software SPSS 19.0. The difference between rice-fish co-culture and fish monoculture was tested using the ANOVA procedure.

Results

Water properties

Rice-fish/shrimp co-culture significantly affected the water parameters (Table 1). The pH value was significantly lower in the co-culture ponds than monoculture ponds. The contents of BOD, COD, turbidity and TSS in the water were significantly reduced by additional rice cultivation, especially in the catfish pond. Rice-fish co-culture also reduced the eutrophication in pond water. The concentrations of TN, NH4+-N, NO3--N, NO2--N, TP and PO43-were significantly mitigated by 39.2%, 48.3%, 15.3%, 46.0%, 30.8% and 24.1% in YC-R compared to YC, and mitigated by 23.4%, 38.9%, 15.9%, 64.8%, 46.7% and 38.5% in FS-R compared to FS, respectively.

Micro-profiles of pH and O2 values across the sediment-water interface

Fig. 2 illustrated the micro-profiles of O2and pH values across the sediment-water interface. The concentration of O2was decreased sharply across the sediment-water interface both in YC-R and YC. The concentration of O2were higher in YC-R than YC across the sediment-water interface (Fig. 2). Additionally, O2penetrated deeper in the sediment of YC-R than YC. The pH value across the sediment-water interface was lower in YC-R than YC. These results indicated that rice-catfish co-culture increased the concentration and penetrating depth of O2, but decreased the pH across the sediment-water interface, compared with catfish monoculture.

Table 1. Water properties of monoculture and co-culture ponds.

YC, Yellow catfish monoculture; YC-R, Yellow catfish-rice co-culture; FS, Freshwater shrimp monoculture; FS-R, Freshwater shrimp-rice co-culture; BOD, Biological oxygen demand; COD, Chemical oxygen demand; TP, Total phosphorus; OP, Organic phosphorus.

Different letters indicate significant difference between different cultures for the same parameter at the 0.05 level.

Flux rates of inorganic N and P across the sediment-water interface

As shown in Fig. 3, the flux rate of NH4+across the sediment-water interface was negative on 21 August and 4 September in YC-R, indicating that NH4+in the water column was consumed by the sediment in YC-R in these two sampling days. NH4+fluxes were generally positive in YC, indicating the release of NH4+from sediment to water column. NO3-fluxes only showed significant difference on 19 September. It was negative in YC-R but positive in YC at this day. The seasonal mean flux rate of NH4+was -0.002 mmol/(m2·h) in YC-R, which was significantly reduced by 100.5% compared with that in YC. The mean flux rates of NO3-, NO2-and PO43-showed no significant difference between YC-R and YC.

As in the shrimp ponds (Fig. 4), the flux rates of NH4+and NO3-across the sediment-water interface were negative in most sampling days in FS-R, while almost positive in FS. The seasonal mean flux rates of NH4+and NO3-were -0.107 and 0.0002 mmol/(m2·h)in FS-R, respectively, which were respectively reduced by 150.4% and 99.8%, compared with that in FS. The mean flux rates of NO2-and PO43-showed no significant difference between FS-R and FS.

Fractions of N and P in the sediment

The fractions of N in the sediment are shown in Fig. 5. The concentrations of NH4+were significantly lower in the sediment of co-culture ponds than monoculture ponds at most sampling days. The mean contents of NH4+were significantly reduced by 51.2% and 58.9% in the sediment of YC-R and FS-R than YC and FS, respectively. Additional rice cultivation did not affect the contents of NO3-and NO2-in the sediment. No significant difference was observed between co-culture and monoculture ponds.

The fractions of P in the sediment were in the order of Res-P (47.0%–49.9%) > Fe/Al-OP (25.5%–28.9%) > Fe/Al-IP (20.3%–27.8%) > Ca-P (2.4%–3.6%) > DIP (0.21%–0.33%) (Fig. 6). Additional rice cultivation significantly reduced the content and percentage of DIP in the sediment of catfish ponds, but increased DIP in shrimp ponds (Table 2). Significantly reduction of Fe/Al-OP was observed in the sediment of YC-R compared to YC, but was not found in FS-R. The concentrations and ratios of Fe/Al-IP, Ca-P and Res-P showed no significant difference between the co-culture and monoculture ponds.

Fig.2. Micro-profiles of oxygen (O2) and pH value across sediment-water interface in rice-catfish co-culture and catfish monoculture ponds.

YC1 to YC3, Three profiles of yellow catfish monoculture; YC-R1 to YC-R3, Three profiles of yellow catfish-rice co-culture.

Discussion

Micro-profiles of O2 and pH across sediment-water interface

Micro-environment is an important factor affecting the transformation of N and P across the sediment-water interface. Previous studies focused on investigating the micro-environment of sediment-water interface in natural water bodies (Bryant et al, 2011; Mügler et al, 2012; Wang et al, 2013b). Aquaculture ponds have rarely been studied. In this study, we measured the micro- profiles of O2and pH values across the sediment- water interface in the rice-catfish co-culture and catfish monoculture ponds. The O2penetration depth in this study is close to the results measured in Taihu Lake and Xiangxi River (Tian et al, 2013), but higher than in Carvins Cove Reservoir (Bryant et al, 2011), and lower than in Milling Lake (Koschorreck et al, 2003), Palaeochori Bay (Wenzh?fer et al, 2000), and Dazong Lake (Wang et al, 2013a). This is possibly attributed to the difference in the water depth, sediment texture and benthic bioturbation among different water bodies (Santschi et al, 1990; Li et al, 2019).

Fig. 3. Flux rates of NH4+(A), NO3-(B), NO2-(C) and PO43-(D) across the sediment-water interface in the rice-catfish co-culture and catfish monoculture ponds.

YC, Yellow catfish monoculture; YC-R, Yellow catfish-rice co-culture.

Values are Mean ± SE (= 3). * indicates significant differences at the 0.05 level.

Fig. 4. Flux rates of NH4+(A), NO3-(B), NO2-(C) and PO43-(D) across the sediment-water interface in the rice-shrimp co-culture and shrimp monoculture ponds.

FS, Freshwater shrimp monoculture; FS-R, Freshwater shrimp-rice co-culture.

Values are Mean ± SE (= 3). * indicates significant differences at the 0.05 level.

Fig. 5. Fractions of N in the sediment of co-culture and monoculture ponds.

YC, Yellow catfish monoculture; YC-R, Yellow catfish-rice co-culture; FS, Freshwater shrimp monoculture; FS-R, Freshwater shrimp-rice co-culture.

Data are Mean ± SE (= 3).

Table 2.Mean contents of differentphosphorus (P) fractions in the sediment of co-culture and monoculture ponds.

YC, Yellow catfish monoculture; YC-R, Yellow catfish-rice co-culture; FS, Freshwater shrimp monoculture; FS-R, Freshwater shrimp-rice co-culture; DIP, Dissolved inorganic phosphorus; Fe/Al-IP, Fe- and Al-bound inorganic phosphorus; Fe/Al-OP, Fe- and Al-bound organic phosphorus; Res-P, Residual phosphorus; Ca-P, Ca-bound phosphorus.

Different lowercase letters indicate significant differences at the 0.05 level among the treatments for the same phosphorus fraction.

Rice-catfish co-culture increased the concentration and penetration depth across the sediment-water interface compared with catfish monoculture (Fig. 2). This can be explained by the root aeration of rice plants. Rice can transfer the O2from the atmosphere through its aerenchyma to roots and secrete to the rhizosphere in flooding water bodies (Colmer et al, 2006). Thus, additional rice cultivation improved the O2level across the sediment-water interface. Rice- catfish co-culture also decreased the pH of sediment- water interface (Fig. 2). This is because rice root can secret organic acids to the rhizosphere, thus reducing the pH in the sediment and water column in the aquaculture pond (Liu et al, 2007). The reduction of pH induced by rice in this study is higher than that induced by(Tian et al, 2013).

Fluxes of N and P across water-sediment interface

We measured the flux rates of N and P across the water-sediment interface in the co-culture and monoculture ponds (Figs. 3 and 4). The flux rates of inorganic N and P were in the order: NH4+> NO3-> NO2-> PO43-, which consists with the results measured in the cage aquaculture zone or aquaculture ponds in previous studies (Nicholaus and Zheng, 2014; Zhong et al, 2015). The N and P accumulated in the sediment surface primarily originated from the excretion of aquatic animals and residual feed, which contain more N than P due to the widely use of high-protein feed in intensive aquaculture to meet the requirement of aquatic animals (Dien et al, 2018; Zhang et al, 2018). The flux rates of N and P in this study are close to the results measured in the costal cage culture zone of fish and scallop (Jiang et al, 2007; Liao et al, 2016; Hu et al, 2017), but lower than that in the aquaculture pond of grass carp and(Guo et al, 2013; Zhong et al, 2015). The stocking density ofis higher than that of the yellow catfish and freshwater shrimp and the body size of grass carp is larger than that of yellow catfish and freshwater shrimp in this study. Higher stocking density and larger body size induced serve bioturbation in the sediment, which may stimulate the release of nutrients from the sediment to the water column (Adámek and Mar?álek, 2013).

Fig. 6. Fractions of P in the sediment of co-culture and monoculture ponds.

YC, Yellow catfish monoculture; YC-R, Yellow catfish-rice co-culture; FS, Freshwater shrimp monoculture; FS-R, Freshwater shrimp-rice co-culture; DIP, Dissolved inorganic phosphorus; Fe/Al-IP, Fe- and Al-bound inorganic phosphorus; Fe/Al-OP, Fe- and Al-bound organic phosphorus; Res-P, Residual phosphorus; Ca-P, Ca-bound phosphorus.

Additional rice cultivation significantly reduced the flux rate of NH4+across the sediment-water interface both in the catfish and shrimp ponds (Figs. 3 and 4). This can be attributed to three possible reasons. Firstly, rice directly uptakes NH4+in the sediment, thus reduces the release of inorganic N from the sediment (Feng et al, 2016). Secondly, rice root can stabilize the sediment and weaken the bioturbation of aquatic animals on sediment surface, thus reduce the inorganic N release induced by bioturbation (Yahel et al, 2008). Thirdly, the shading of rice leaf reduced the water and sediment temperature, which may reduce the flux of nitrogen from sediment (Arandia-Gorostidi et al, 2016). Rice only significantly reduced the release of NO3-from sediment in shrimp ponds. The amount of feed applied in shrimp ponds was far lower than that in catfish ponds. The residual N accumulated in the sediment of shrimp ponds may not provide sufficient NH4+for rice. Thus, rice absorbed more NO3-in the sediment of shrimp ponds and significantly reduced the release of NO3-from the sediment.

Rice did not affect the flux rate of PO43-across the sediment-water interface both in the catfish and shrimp ponds (Figs. 3 and 4). The effects of rice on PO43-exchange across sediment-water interface was complicated. Both positive and negative effects of rice on the release of PO43-from sediment may exist (Dai et al, 2015). Moreover, rice can absorb the PO43-in the sediment, thus reduced the release of PO43-from the sediment. Rice can increase the redox potential, cationic exchange capacity and exchangeable Ca, Fe and Al in the sediment through excreting oxygen and organic acids to the rhizosphere (Wang et al, 2007), which may increase the sorption of PO43-in the sediment. The excretion of organic acids by rice may also decrease the pH value of sediment and increase the chemical desorption of P in the sediment (Bolan, 1991). These effects may balance each other.

Conclusions

Rice-catfish/shrimp co-culture significantly reduced the contents of N and P in the water of intensive aquaculture ponds. Additional rice cultivation also affected the micro-environment and nutrient exchange across the sediment-water interface. Rice-catfish co-culture increased the concentration and penetrating depth of O2, but decreased the pH value across the sediment- water interface, compared with catfish monoculture. The flux rate of NH4+across sediment-water interface was significantly lower in the rice-catfish/shrimp co-culture ponds than catfish/shrimp monoculture ponds. The flux rates of NO2-and PO43-showed no significant difference between the co-culture and monoculture ponds. Rice only affected the dissolved inorganic N and P fractions in the sediment.

Acknowledgements

This work was supported by the Natural Science Foundation of China (Grant Nos. 41877548 and 31400379), Natural Science Foundation of Zhejiang Province of China (Grant No. LY15C030002) and Innovation Program of Chinese Academy of Agricultural Sciences.

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3 April 2019;

24 June 2019

FENG Jinfei (fengjinfei@caas.cn); FANG Fuping (fangfuping@caas.cn)

Copyright ? 2019, China National Rice Research Institute. Hosting by Elsevier B V

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Peer review under responsibility of China National Rice Research Institute

http://dx.doi.org/10.1016/j.rsci.2019.06.001

(Managing Editor: Li Guan)