Effect of rice cultivar on greenhouse-gas emissions from rice–fish co-culture

Abstract

In aquaculture, co-culturing rice with fish may mitigate greenhouse-gas emissions. In this study, coculture of four rice cultivars in a laboratory-scale rice–fish system reduced CH4 and N2O emissions relative to fish monoculture. Differences in CH4 and N2O emissions among rice cultivars primarily stem from the differential effects of rice plants on plant-mediated CH4 transport, CH4 oxidation and nitrogen absorption.

Headnote

ABSTRACT

In aquaculture, co-culturing rice with fish may mitigate greenhouse-gas emissions. In this study, coculture of four rice cultivars in a laboratory-scale rice–fish system reduced CH4 and N2O emissions relative to fish monoculture. Differences in CH4 and N2O emissions among rice cultivars primarily stem from the differential effects of rice plants on plant-mediated CH4 transport, CH4 oxidation and nitrogen absorption.

Keywords:

Greenhouse gas emissions

Aquaculture

Rice-fish system

Rice cultivar

1. Introduction

Aquaculture, though producing an increasing share of the world's food fish relative to capture fisheries [1], is a major anthropogenic source of greenhouse gas (GHG) emissions [2]. Carbon (C) and nitrogen (N) unused in intensive aquaculture systems are transformed to CH4 and N2O [3,4] and released annually in megaton quantities [2,5].

Integration of aquaculture with crop culture is a measure recommended for limiting the environmental pollution induced by residual nutrients accumulating in aquaculture systems [6]. Vegetables or cereal crops can be integrated with aquaculture using several co-culture systems (aquaponics, co-culture in ponds, floating bed) to reuse the unused nutrients [7–9], which are the primary substrate for the production of CH4 and N2O.

Studies of the effect of integrated culture on CH4 and N2O emissions from aquaculture are scarce. Culturing with vegetables in aquaponic systems mitigated N2O emission to the atmosphere because of the uptake of N in the aquaculture water by vegetables [10,11]. Co-culturing with rice in shrimp or catfish ponds reduced N2O emission by reducing residual N in the water and sediment [12]. CH4 contributes more than N2O to total global warming potential (GWP) in the aquaculture system [13]. Unlike the substrate N, the substrate C for CH4 production cannot be directly absorbed by plants. The effects of various crops on GHG emissions were highly dependent on biological characteristics such as morphological traits, rhizospheric effect, and N uptake ability [1416]. The linkage between the morphological and physiological traits of plants and their efficiency in mitigating GHG emissions from aquaculture is poorly understood.

Rice is a typical cereal crop used in the integration of aquaculture and agriculture systems. Rice plants affect the CH4 production and oxidation processes through their rhizospheric effect (e.g., root-secreted substrate C or O2) or facilitate CH4 transport through their aerenchyma [17]. Thus, the net effect of rice on CH4 emission was highly dependent on the biological characteristics of different rice cultivars and the culture environment. Rice cultivars with higher N uptake ability and biomass might more strongly reduce N2O emission but increase CH4 production and transport. It is not known whether cultivars with high efficiency in reducing N2O emission were also efficient in reducing CH4 emission. Previous studies [18–20] focused on comparing the effect of rice cultivar on the CH4 and N2O emissions from rice fields. Aquaculture systems usually have longer flooding time and greater water depth when co-cultured with rice than conventional rice production in paddy fields. But the effect of rice cultivar on CH4 and N2O emissions from aquaculture is still unknown.

Pond aquaculture, widely adopted worldwide, is a main source of GHG emissions from water bodies [5]. Rice plants can be integrated into a culture with fish by direct planting in the sediment in shallow ponds or using floating beds in deep ponds. To our knowledge, no experiment has been conducted to compare rice cultivars with respect to their efficiency of mitigation of GHG emissions from shallow-pond aquaculture.

The objectives of this study, conducted in a laboratory-scale rice–fish culture system, were to identify 1) the effect of rice cultivar on GHG emissions from aquaculture ponds, 2) the main factors influencing the efficiency of GHG emission reduction, and 3) the effect of rice cultivar on yield and GWP.

2. Materials and methods

2.1. Experimental setup and design

The laboratory-scale rice–fish system was constructed in a greenhouse under controlled conditions in China National Rice Research Institute, Hangzhou, Zhejiang, China. This region is a typical aquaculture region in South China. Two inbred rice cultivars (Jia 67 and Xiushui 121) with low biomass and two hybrid rice cultivars (Yongyou 1540 and Zhongzheyou 8) with high biomass, all commonly used in local rice–fish systems, were selected for comparison of their efficiencies in mitigating GHG emissions. The fish animal used in this study was yellow catfish (Pelteobagrus fulvidraco).

This experiment consisted of five treatments: (I) fish cocultured with Jia 67 (F-J67); (II) fish co-cultured with Xiushui 121 (F-XS121); (III) fish co-cultured with Yongyou 1540 (FYY1540); (IV) fish co-cultured with Zhongzheyou 8 (F-ZZY8); and (V) fish monoculture (F) as control. All treatments had four replicates and were arranged in 20 plastic tanks of 1.75 1.25 1 m height. Bottom soil to a depth of 0–20 cm was collected from a nearby aquaculture pond used for more than ten years. A blender was used to homogenize the collected soil and each tank was filled with a 20 cm-thick layer of the homogenate. The main soil properties were as follows: pH (1:2.5 H2O) 6.72, soil organic carbon (SOC) 21.4 mg g1 , total nitrogen (TN) 2.44 mg g1 , ammonium nitrogen (NH4 + ) 136 mg kg1 , and nitrate nitrogen (NO3 ) 22.4 mg kg1 .

Rice seedlings were transplanted into the tanks at a spacing of 0.5 m 0.5 m (four hills per tank) on June 12, 2022 for all cultivars. The water level was raised as the rice plants grew, reaching a maximum depth of 0.7 m. The water depth in each tank was the same. The fish fingerlings were stocked in the tank on July 21, 2022. The stocking density was 80 individuals per tank; and the average size of the fish fingerlings was 4.5 g. Fish were fed twice daily, at 07:00 with 40% and at 18:00 PM. with 60% of the daily feed. The feed amount was increased with fish growth. The density of feed applied in each tank was 708.6 g m2 . The total C and N in the feed were 242.9 g m2 and 43.1 g m2 , respectively. Rice and fish were harvested on October 26, 2022.

2.2. Flux rates of CH4 and N2O

The static chamber method was used to quantify the flux rates of CH4 and N2O [21]. The static chamber was cubic, 0.5 m on a side. The chamber in each tank was equipped with steel supports as the foundation before rice planting, and the height of the supports could be adjusted as the water depth increased. Gas samples were collected from each chamber using an automated gas sampler at 0, 10, 20, and 30 min after closing the chambers between 8:00–10:00 AM. Gas samples were collected once a week during the rice growing stage and twice a week during drying stage after rice and fish were harvested. To investigate the change of CH4 and N2O flux rates induced by water drainage, a more frequent sampling was conducted at intervals of 3 h over 2 d (48 h) after the water was drained. The contents of CH4 and N2O in the gas samples were measured by gas chromatography (GC2010, Shimadzu, Kyoto, Japan). The flux rates of CH4 and N2O were calculated based on the linear increases of gas concentration during the sampling time [22].

2.3. Contents of CH4 and N2O in the pore solution of bottom soil

The pore solution in the bottom soil of each tank was collected with a Rhizon soil solution sampler (Rhizon SMS, Eijkelkamp Agrisearch Equipment, the Netherlands). The samplers were placed in the bottom soil close to the rice roots in the rice-fish co-culture tanks, or in the central part in the fish monoculture tanks. Pore solution was sampled simultaneously with gas sampling. About 10 mL pore solution was collected and immediately injected into a 20 mL headspace bottles with a syringe. The contents of CH4 and N2O in the pore solution were determined by a headspaceequilibration method [23].

2.4. Flux rate of CH4 through plant-mediated transport

CH4 transport through the rice plant was measured at the middle growth stage. First, the static chamber method was used to measure the full emission of CH4 via plant transport, diffusion, and bubbling (A). The plants were then covered with a 0.15 1.5 m flat plastic bag to prevent the transport of CH4 through the rice aerenchyma (Fig. S1). The bag mouth was submerged 5 cm below the water surface and tied tightly around the rice stems to prevent gas leakage, and the flux rate of CH4 without plant transport was measured by the static chamber method. The CH4 flux rate via plant-mediated transport was calculated as the difference between the first and second rates.

2.5. Water and bottom soil sampling and analysis

Composite water samples were collected simultaneously with the gas sampling at a depth of 10 cm in each tank. The contents of N forms (total N, NH4 + , NO3 , and NO2 ) in the water were measured using standard water chemistry methods [24]. The content of total organic carbon (TOC) in the water was measured with a 3100 TOC Analyzer (Yena, Germany). The soil samples were collected monthly after rice planting, by using a soil-drilling sampler at 0–10 cm depth. The composite soil samples were divided into two equal parts. One part of the samples was stored for soil chemical analysis, the other part was stored at a temperature of 80 C for subsequent soil microbial analysis. The contents of total and inorganic N, SOC, and dissolved organic carbon (DOC) in the soil were determined using standard soil chemistry methods [25]. The abundance of specific functional groups of microorganisms involved in CH4 and N2O emissions in the bottom soil, including methanogenic functional gene (mcrA), methanotrophic functional gene (pmoA), nitrifier functional genes (AOA and AOB), and denitrifier functional genes (nirS, nirK, and nosZ) were measured by qPCR (Bio-Rad CFX96, USA). The primers are listed in Table S1.

2.6. Rice and fish sampling and analysis

Rice roots were sampled for the measurement of morphological traits at the middle growth stage. The roots were scanned (Epson Perfection V800 Photo, Japan) and their length, mean diameter, volume, and number were determined with a WinRhizo Root Analysis System (Regent Instruments Inc., Quebec, Canada). The roots were then dried at 70 C to constant weight. Root slices from each cultivar were cut with a razor blade 15–20 mm from the root tip and photographed under a scanning electron microscope (S3400 N, Hitachi, Japan). The area of aerenchyma was measured with ImageJ software and the proportion of aerenchyma was calculated as pore space area divided by total space area. Plant height, tiller number, aboveground biomass, and grain yields of each rice cultivar were recorded at maturity stage for each cultivar. Fish were weighed before stocking and after harvesting to calculate yield. N content in the rice and fish was determined using the Kjeldahl method [25].

2.7. Calculation of GWP

The overall GWP of CH4 and N2O was calculated using the 100year radiative forcing potential coefficients to CO2 (34 was used for CH4 and 298 for N2O) [26]. Yield-scaled GWP was calculated as GWP per unit yield of rice and fish.

3. Results

3.1. CH4 and N2O emissions

The flux peaks of CH4 presented both during flooding and drying stages (Fig. 1A). Co-culturing with J67, XS121, and YY1540 significantly reduced cumulative CH4 emission during the flooding stage, as compared with fish monoculture treatment (Fig. 1C). There was no difference in cumulative CH4 emission between FZZY8 and F during the flooding stage. The content of CH4 in the pore solution of the bottom soil was inconsistent with the cumulative CH4 emission among the four cultivars. Co-culturing with YY1540 and ZZY8 showed lower CH4 content in the pore solution than co-culturing with J67 and XS121 (Fig. 2A). However, Coculturing with YY1540 and ZZY8 did not reduced more CH4 emission during the flooding stage than co-culturing with J67 and XS121. As for the drying stage, the cumulative CH4 emission for all four co-culture treatments were lower than that of fish monoculture treatment (Fig. 1C). Compared with two inbred cultivars (J67 and XS121), co-culturing with two hybrid cultivars (YY1540 and ZZY8) showed higher efficiency in the mitigation of CH4 emission during the drying stage. The total CH4 emission of the whole experiment duration was reduced 40.1% by YY1540, 40.7% by XS121, 33.6% by J67, and 18.2% by ZZY8, as compared with fish monoculture (Fig. 1C). ZZY8 showed lower efficiency in the mitigation of CH4 emission than that of the other three cultivars.

Co-cultured with four rice cultivars significantly reduced cumulative N2O emission during the flooding stage (Fig. 1D). Though the content of N2O in the pore solution (Fig. 2B) were lower for two hybrid cultivars (YY1540 and ZZY8) than two inbred cultivars (J67 and XS121), the cumulative N2O emission did not differ between four cultivars during the flooding stage. As for the drying stage, two hybrid cultivars reduced more N2O emission than two inbred cultivars. The total N2O emission of the whole experiment duration was respectively reduced 92.8% by ZZY8, 90.1% by YY1540, 66.4% by XS121, and 60.3% by J67, as compared with catfish monoculture (Fig. 1D). Two hybrid cultivars showed higher efficiency in the mitigation of N2O emission than that of two inbred cultivars.

3.2. Substrate C and N and the functional genes

Co-culturing with four rice cultivars did not affect the contents of SOC and TN in the bottom soil over the experiment (Fig. 3A, C). Co-culturing with XS121, YY1540, and ZZY8 showed lower content of DOC in the bottom soil than fish monoculture treatment during the drying stage (Fig. 3B). Co-culturing with four rice cultivars significantly reduced the content of inorganic N (NH4 + , NO3 , and NO2 ) in the bottom soil during the flooding and drying stages (Fig. 3DF). Co-culturing with two hybrid rice cultivars (YY1540 and ZZY8) resulted in a greater reduction of inorganic N (NH4 + and NO3 ) content than two inbred rice cultivars (J67 and XS121).

Co-culturing with four rice cultivars showed an effect on the abundances of only pmoA and AOB in the bottom soil (Fig. 4). The abundance of pmoA in the bottom soil was higher for four co-culture treatments than fish monoculture treatment during the flooding stage (Fig. 4B). Co-culturing with two hybrid rice cultivars increased more pmoA than two inbred rice cultivars. Coculturing with four rice cultivars significantly reduced the abundance of AOB in the bottom soil (Fig. 4G) during the flooding stage. As in the drying stage, only co-culturing with two hybrid rice cultivars showed significantly lower AOB in the bottom soil.

3.3. Root morphological traits and plant-mediated transport

The root number, root length, root volume, and root dry weight of four rice cultivars were in the order ZZY8 > YY1540 > J67 > XS121 (Fig. 5A–D). Two hybrid cultivars showed stronger root system than two inbred cultivars. ZZY8 showed the highest root aerenchyma area of the four cultivars (Fig. 5F).

The flux rates of CH4 measured with rice plants were higher than that without rice plants for all four cultivars (Fig. 6A). ZZY8 showed higher plant-mediated CH4 flux rate than the other three cultivars. The flux rate of N2O did not differ when measured with and without the plant. The plant-mediated N2O flux rate did not differ among the four cultivars.

3.4. Yields and yield-scaled GWP

Co-culturing with four rice cultivars all significantly increased the N use efficiency, compared with F (Table 1). Two hybrid cultivars (YY1540 and ZZY8) absorbed nearly 3 times N than two inbred cultivars (J67 and XS121). The overall GWP of CH4 and N2O was significantly lower for four co-culture treatments than monoculture treatment. CH4 contributes 84.6%–98.0% to the overall GWP, which was far more than the contribution of N2O. The rice yields were significantly higher for two hybrid cultivars (YY1540 and ZZY8) than two inbred cultivars (J67 and XS121). The yieldscaled GWP was respectively reduced 56.0% by F-J67, 53.2% by F-XS121, 72.6% by F-YY1540, and 57.7% by F-ZZY8, compared with F. Co-culturing with YY1540 showed the highest efficiency in the mitigation of yield-scaled GWP

4. Discussion

4.1. Effect of rice cultivar on CH4 emission

The effect of cultivar on the CH4 emission from aquaculture in this study was inconsistent with the results of rice cultivars in the paddy fields. Hybrid rice cultivars showed less CH4 emission than inbred cultivars in paddy fields [27,28]. However, coculturing with hybrid rice cultivars showed similar or higher CH4 emission than co-culturing with inbred rice cultivars in this study, especially during the flooding stage (Fig. 1C). CH4 emission from aquaculture was determined by three processes: production, oxidation, and transport [29]. Co-culturing with four rice cultivars did not affect CH4 production in the bottom soil, given that there were no differences in the content of available C and the abundance of metagenesis in the bottom soil between co-culture and monoculture treatments (Figs. 3 and 4). The difference among the four cultivars may be attributed primarily to their effect on CH4 oxidation and transport in the aquaculture system. Coculturing with two hybrid cultivars showed higher abundance of methanotrophs in the bottom soil than two inbred cultivars in the flooding stage (Fig. 4B). However, they did not present higher efficiency on the mitigation of CH4 emission in this stage and ZZY8, one of the hybrid cultivars, even showed higher CH4 emission than the two inbred cultivars (Fig. 1C). This may be attributed to their stronger root system and aerenchyma tissue, which promote the plant-mediated transport of CH4 from the flooded bottom soil to the atmosphere [30,31]. In previous studies [32,33], CH4 transport in paddy fields was not limited by the transport capacity, and rice plants served as conduits for CH4 transport rather than limiting it. However, continuous flooding with deep water may limit the transport of CH4 from the bottom soil to the atmosphere in the aquaculture system [34]. The CH4 flux rate was higher with the rice plant conduit than without the rice plant conduit (Fig. 6A). ZZY8 showed higher CH4 flux rate through plant transport. Thus, higher plant-mediated transport may weaken their inhibition of CH4 emission during the flooding stage.

The inconsistency between the content of CH4 in the pore solution of bottom soil and the cumulative CH4 emission in the flooding stage (Figs. 1C, 2A) may also be attributed mainly to plantmediated transport. The content of CH4 in the pore solution of bottom soil is determined by not only CH4 oxidation but CH4 transport [35]. Co-culturing with ZZY8 showed higher abundance of the methanotrophic functional genes (Fig. 4B), and promoted the CH4 oxidation in the bottom soil, resulting in reduced CH4 in the pore solution. ZZY8 also had higher plant-mediated transport of CH4 (Fig. 6B), which could promote the transport of CH4 from bottom soil to the atmosphere and reduce the CH4 in the pore solution. Thus, less CH4 in the pore solution did not indicate less CH4 emission to the atmosphere.

Previous studies [18,19,36] focused on evaluating the influence of rice cultivar on CH4 emissions during the rice growing stage. In the present study, co-culturing with rice continued to affect CH4 emission during the drying stage after rice harvest. Co-culturing with four rice cultivars all showed lower CH4 emission than fish monoculture treatment (Fig. 1C). The CH4 emission during the drying stage was emitted primarily from the pore solution of exposed soil [34,37]. The content of CH4 in the pore solution of bottom soil before water draining and the CH4 flux rate during 48 h after water draining were lower for four co-culture treatments than fish monoculture treatment (Figs. S2, S3), thus resulting in reduced CH4 emission during drying stage. Co-culturing with two hybrid rice cultivars showed higher efficiency on the mitigation of CH4 emission during the drying stage. This was attributed to their higher CH4 oxidation and plant-mediated transport ability (Figs. 4 and 6), which induced lower CH4 left over in the pore solution (Fig. S2), and then reduced more CH4 emission during the drying stage than two inbred cultivars. Thus the loss through plantmediated CH4 transport during the flooding stage could be partly compensated during the drying stage. In assessing the effectiveness of a rice cultivar in mitigating CH4 emissions from an aquaculture pond, both the growth stage and the post-harvest stage should be considered.

4.2. Impact of different rice cultivars on N2O emission

Co-culturing with four rice cultivars reduced the N2O emission from a catfish aquaculture system (Fig. 1D). Rice plants have the capacity to absorb inorganic N from bottom soil, thereby reducing the availability of N for N2O production [12]. Two hybrid rice cultivars showed higher N uptake ability than two inbred cultivars (Table 1), but they did not show higher efficiency in the mitigation of N2O emission during the flooding stage (Fig. 1D). The N2O emission from aquaculture was usually produced in the bottom soil or water [38]. Co-culture with rice plants may provide the other source for N2O emission. Many plants produce N2O in cells and emit it to the atmosphere [39,40]. Two hybrid cultivars with higher N uptake may directly emit the N2O produced in the rice plants [41], and weaken their inhibition on the N2O emission during the flooded rice growing stage.

Draining the water stimulated the N2O emission from aquaculture system (Fig. 1D), as also observed in paddy fields [42]. Coculturing with four rice cultivars also reduced the N2O emission during the drying stage after rice harvested. Different from that in the flooding stage, two hybrid rice cultivars showed higher efficiency on the mitigation of N2O emission than two inbred cultivars in this stage. Co-culturing with two hybrid cultivars reduced more inorganic N in the bottom soil than with two inbred cultivars, which may continuously affect the N2O production during the drying stage after rice harvest. Decomposition of rice residues with high C/N ratio (> 30) could deplete available N in bottom soil [43]. Two hybrid cultivars left more root residue in the bottom soil than two inbred cultivars, which may intensify the reduction of available N for N2O production, thus further reducing N2O emission.

4.3. Effect of cultivar on yields and GHG mitigation

Constructing an integrated rice-fish system to mitigate GHG emissions from aquaculture should consider the comprehensive effect on the yields of rice and fish and GHG mitigation. Coculturing with rice plants could improve water quality and may promote the growth of fish [44,45]. In this study, only coculturing with YY1540 resulted in higher fish yield than monoculture treatment (Table 1). This was attributed to its highest efficiency in the mitigation of NH4 + and NO2 – in the water (Fig. S4), which may weaken the negative effect of these two inorganic N forms on fish growth and increase fish yield [46].

Cultivars with higher yield and N uptake ability showed higher efficiency in inhibiting N2O emission, as also observed in paddy fields [14,47]. CH4 contribute far more than N2O to GWP (Table 1). Reducing CH4 emission was more important than N2O in mitigating overall GWP in the aquaculture ponds. However, the rice yields of four cultivars were correlated with their efficiency in mitigating of CH4 emission from aquaculture, primarily because rice plants had both positive and negative effects on CH4 emission from aquaculture [17]. The key processes governing the efficiency of highyield rice cultivars in inhibiting CH4 emission were their effect on belowground CH4 oxidation and production in the paddy fields [33]. The distinctive characteristics of high-yield cultivar with less CH4 emission were high yield potential, high root oxidation ability, and less photosynthate allocated to belowground parts [18,48,49]. In the present study, the difference in CH4 emission among two high-yield hybrid cultivars stemmed primarily from their differential effects on plant-mediated CH4 transport. A high-yield cultivar with less aerenchyma for CH4 transport could show higher efficiency in mitigating CH4 emission from aquaculture. The optimal morphological and physiological traits of rice plants for the mitigation of CH4 emission from aquaculture may be different from that for paddy fields.

5. Conclusions

Co-culturing with rice cultivars reduced CH4 and N2O emissions relative to fish monoculture, during the rice growth period and after harvest. The differences in CH4 and N2O emissions among rice cultivars were attributed to their differential effects on CH4 oxidation in the bottom soil, plant-mediated CH4 transport, and substrate N for N2O production. Co-culturing with hybrid rice cultivars produced higher yields and lower yield-scaled GWP than with inbred cultivars. High yield with low plant-mediated CH4 transport and high N uptake ability are recommended characteristics for selecting or breeding rice cultivars to reduce GHG emissions from aquaculture.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

CRediT authorship contribution statement

Kexin Xie: Conceptualization, Data curation, Writing - original draft, Writing - review & editing. Mengjie Wang: Data curation, Methodology, Visualization, Writing - original draft. Xiaodan Wang: Data curation; Formal analysis. Fengbo Li: Methodology, Investigation, Funding acquisition. Chunchun Xu: Investigation, Funding acquisition. Jinfei Feng: Project administration, Supervision. Fuping Fang: Conceptualization, Methodology, Writing - review & editing, Funding acquisition

Acknowledgments

This work was supported by the National Natural Science Foundation of China (42177455), "Pioneer" and "Leading Goose" R&D Program of Zhejiang (2022C02008 and 2022C02058), Central Public-interest Scientific Institution Basal Research Fund (CPSIBRF-CNRRI-202305), and the Agricultural Science and Technology Innovation Program (ASTIP).

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ARTICLE INFO

Article history:

Received 22 January 2024

Revised 16 April 2024

Accepted 25 April 2024

Available online 29 May 2024

Footnote

* Corresponding author.

E-mail address: [email protected] (F. Fang).

1 These authors contributed equally to this work.

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Appendix A. Supplementary data

Supplementary data for this article can be found online at https://doi.org/10.1016/j.cj.2024.04.011.