Introduction
In the early 1990s, researchers initiated pilot studies on the integrated rice-crab farming system in Panjin City, Liaoning Province, thereby accumulating nearly three decades of experiential data [1-3]. Currently, this integrated farming system covers approximately 10% of the total rice field area in Liaoning Province, with primary concentrations in regions such as Panjin and Yingkou in the Liaohe River Delta and Dandong in the Yellow Sea rice-producing area [4]. By 2010, over 10,000 farmers nationwide had adopted the rice-crab farming model, leading to the establishment of a “company + farmers + base” business framework, which facilitated the rapid expansion of the rice-crab industry. This innovative ecologically integrated farming model, characterized by “one water serving two purposes, dual benefits from one place, and coexistence of rice and crabs,” optimizes the utilization of agricultural resources. Remarkably, it not only yields significant economic value from crab production but also markedly enhances the quality of rice, thereby resulting in a substantial increase in income for rice farmers [5, 6].
Ensuring the long-term and sustainable development of the rice-crab farming model, as well as safeguarding the production capacity of the system, requires comprehensive research into the interaction mechanisms within the rice-crab symbiotic system. Previous studies have indicated that various fertilization methods significantly influence the growth and reproduction of Chinese mitten crabs [7]. Excessive application of ammonium-nitrogen fertilizer can induce crab toxicity, thereby impeding their growth and development [8, 9]. Following ammonium-nitrogen toxicity, crabs exhibit noticeable disruptions in their physiological and biochemical processes, leading to metabolic disorders in organs such as the liver and pancreas, as well as a reduction in immune system functionality [9]. To ensure safe fertilization for crabs without compromising rice yield and quality, research suggests that the optimal nitrogen fertilizer application should not exceed 270 kg per hectare [10]. Furthermore, adopting a judicious fertilization approach can significantly mitigate nitrogen leaching losses in rice-crab farming fields and augment nitrogen utilization efficiency [11].
As the rice-crab model continues to mature, various ecological farming models have emerged across different regions of southern China, including rice-fish, rice-duck, and rice-shrimp farming, gaining popularity among local farmers [12, 13]. Compared to single rice cultivation, these multi-species models exhibit notable efficiency in resource utilization and have demonstrated robust developmental trends [12, 14, 15]. It has been reported that the rice-crab farming model contributes to increased soil organic matter, beneficial soil biota populations, and soil nutrient levels, ultimately enhancing soil fertility. However, despite its significant economic benefits, research on the impact of the rice-crab farming model on soil ecosystems remains limited, particularly regarding the long-term evolution of soil fertility under multi-year rice-crab farming systems. A comprehensive understanding of the long-term evolution of soil fertility within the rice-crab farming system holds paramount significance for its sustainable development [5, 16]. To address this research gap, this study focuses on the following scientific questions: First, the long-term application of the rice-crab ecological farming system can significantly improve the physical structure of the soil, such as by reducing soil bulk density and increasing soil porosity, thereby enhancing soil aeration and water infiltration. Second, whether this model can significantly increase the content of soil organic matter and total nitrogen and improve soil nutrient status, including the levels of available nitrogen, phosphorus, and potassium, thus providing more sufficient nutrients for crops. Additionally, this study evaluates whether the long-term application of the rice-crab farming model can enhance the quality and market price of rice and provide additional economic benefits through crab production, achieving both economic and ecological benefits.
Our study presents several innovations: Firstly, unlike previous short-term studies, this research involves 16 years of continuous monitoring of the rice-crab ecological farming model, systematically analyzing its long-term effects on soil physical and chemical properties, filling the gap in long-term dynamic studies. Secondly, this research not only focuses on changes in soil physical and chemical properties but also systematically evaluates soil biological properties, such as enzyme activity, and the impact of these changes on crop growth and yield, providing a comprehensive soil health assessment. Additionally, through detailed economic benefit analysis, the study assesses the economic feasibility and advantages of the rice-crab farming model in improving rice quality, market price, and crab production, offering theoretical support for its promotion. Lastly, the research delves into the specific mechanisms of soil improvement under the rice-crab farming model, such as the impact of crab activities on soil structure and the application of organic-inorganic fertilizers on soil nutrient accumulation, providing scientific explanations for the ecological effects of the rice-crab farming model. Through these innovative studies, this paper not only validates the environmental and economic benefits of the rice-crab ecological farming model but also provides a scientific basis and practical guidance for its broader application. These findings are of significant importance for promoting sustainable agricultural development.
Experimental Procedures
Overview of the Test Area
The experiment was conducted within the rice field area situated in Jiangjia Village, Bawangzi Town, Panshan County, Panjin City, Liaoning Province, China (latitude N 40°45’ to 41°27’, longitude E 121°27’ to 122°29’). This locale is typified by a single-season rice cultivation zone prevalent in Northern China, characterized by a warm temperate continental semi-humid monsoonal climate. It registers an annual average temperature of 8.3ºC, an annual average precipitation of 623.6 mm, and an annual average sunshine duration of 2787 h. Irrigation for the experiment was facilitated utilizing water sourced from the Liao River, conforming to the stipulated criteria for irrigation in green food production and freshwater aquaculture.
Table 1.
Physical-chemical characteristics of tested soil (2006).
| pH | Bulk density/ (g·cm-3) | Porosity/% | Organic matter/% | Total N/% | Total P/% | Total K/% | Hydrolysable N/ (mg·kg-1) | Ava. P/ (mg·kg-1) | Ava. K/ (mg·kg-1) |
|---|---|---|---|---|---|---|---|---|---|
| 7.9 | 1.36 | 48.87 | 2.54 | 0.14 | 0.05 | 0.18 | 95.1 | 10.0 | 198 |
The experimental site is situated within the core trial and demonstration area designated for rice-crab ecologically integrated farming. Historically, prior to 2006, the area was conventionally utilized for rice cultivation. Subsequently, in 2006, the experimental setup commenced. The treatment plots allocated for rice-crab ecologically integrated farming spanned an area of 667 m2, with three replications implemented. Correspondingly, adjacent plots of equivalent size, where crab farming was absent and conventional rice farming prevailed, served as control plots (referred to as FP treatment), and also replicated thrice. The soil composition in the vicinity is categorized as saline-alkali paddy soil, and the fundamental physical and chemical attributes of the topsoil (0~20 cm) are detailed in Table 1.
Experimental Design
Between 2007 and 2022, a continuous monitoring and tracking study was undertaken, comparing conventional rice fields (referred to as the FP treatment) with rice-crab ecologically integrated farming fields (designated as the CR treatment). Throughout the 16-year duration, the experimental treatments and locations remained consistent, with fixed monitoring sites established each year. The rice variety selected for the experiments was ‘Yanfeng 47’.
In the FP treatment, conventional fertilization practices indigenous to the locality were adhered to, comprising a basal application of 750 kg·hm-2 of a ternary compound fertilizer (composed of N-P2O5-K2O at percentages of 26%-15%-18%), along with 150 kg·hm-2 of urea for tillering and 75 kg·hm-2 of urea for panicle development. This corresponded to a total nutrient application of N 298.5 kg·hm-2, P2O5 112.5 kg·hm-2, and K2O 135 kg·hm-2. Field management procedures followed traditional rice cultivation practices typical of the area.
In the context of the Controlled Release (CR) treatment, a singular application of organic-inorganic fertilizer tailored specifically for rice-crab cultivation was uniformly administered prior to the transplantation of rice seedlings. This application was executed at a rate of 1200 kg·hm-2, comprising nutrients with a composition of N-P2O5-K2O at 22.5%-8.75%-7.5%, maintaining an inorganic-to-organic nitrogen ratio of 7:3. Consequently, the total nutrient dosage amounted to N 270 kg·hm-2, P2O5 105 kg·hm-2, and K2O 90 kg·hm-2. The cultivation methodology employed in these fields adhered to the “Panshan rice-crab integrated farming” model, characterized by the implementation of parallel ditches and ridges, interspersed planting of rice and fallow spaces, cultivation of beans on the ridges, and the early introduction of crab juveniles. Chinese mitten crabs were introduced into the fields precisely one week following the transplantation of rice seedlings, with a stocking density of 9000 crabs·hm-2. Additionally, 1050 kg·hm-2 of crab feed was supplied concurrently. Notably, no supplementary fertilizer was administered throughout the subsequent growth stages of the rice plants.
Indicator Measurements
Annually, spanning from mid to late May, soil samples were systematically collected prior to land preparation utilizing the S-shaped five-point sampling technique. These samples, sourced from the surface layer spanning 0-20 cm depth, underwent meticulous mixing, air-drying at ambient temperature, and subsequent analysis through diverse methodologies.
Soil Physical Properties
The physical properties of the soil were mainly determined by the bulk density and porosity, which were determined by the ring knife method [17, 18]. The volume of 200 mL ring knife with a bottom cover was selected, and the mass of the ring knife was weighed and recorded as M0; fresh soil samples were uniformly loaded into the ring knife, and the mass of the ring knife and soil was weighed and recorded as M1; the ring knife and soil were dried at 105℃ for 4 h, and then naturally cooled in the desiccator for 4 h, and the mass of the ring knife and soil was weighed and recorded as M2, and then the calculation of the bulk density was carried out by the following Equations:
Soil samples were loaded into the ring cutter in a field-tight condition, fastened to the perforated top cover, and weighed as M3; the ring cutter was soaked in water for 24 h and weighed as M4. The Equation for the determination of soil porosity is given below:
Soil Chemical Properties
The determination of soil organic matter content utilized the potassium dichromate-sulfuric acid oxidation method [19]. pH levels were assessed employing a potentiometric technique. Total nitrogen content was quantified employing the Kjeldahl nitrogen determination method [20]. Total phosphorus concentration was determined via the molybdenum antimony anti-colorimetric method [21]. Total potassium content was measured through a mixed acid digestion method followed by atomic absorption spectroscopy [22]. Water-soluble nitrogen was assessed utilizing sodium hydroxide alkali diffusion [23]. Available phosphorus was quantified employing the molybdenum antimony anti-colorimetric method [24], while available potassium levels were determined through ammonium acetate extraction followed by atomic absorption spectroscopy as per NY/T 889-2004 standard protocol [25]. Soil redox potential was determined using an automatic redox potential meter (FJA-6) with undisturbed 0-20 cm topsoil samples collected from the rice fields within 3 h of extraction. Measurements were taken each year on May 20th for 16 consecutive years. In addition, in 2022, the exchangeable base ion content was determined with ammonium acetate and analyzed using ICP.
Soil Enzyme Activities
Soil phosphatase activity was measured using the disodium phenyl phosphate method [26]. Urease content was determined using the indophenol blue colorimetric method [27].
Crab and Rice Yields
The mass of Chinese mitten crabs was weighed using an electronic balance. The crab survival rate was calculated as the number of crabs recaptured divided by the number released, multiplied by 100% [28]. Rice yield was determined based on actual field measurements, but data for yield measurements were only available for 2021-2022.
Data Statistics and Analysis
Using DPS 18.1 software [29], the trial’s raw data were submitted to a one-way ANOVA after being tallied using Excel 2019.
Results
Soil Physical Properties
Continuous monitoring of soil physical properties from 2007 to 2022 revealed that the rice-crab ecological farming system (CR) significantly improved soil bulk density and porosity compared to the conventional single-crop paddy field (FP). In 2007, there were no significant differences between the two systems in terms of soil bulk density and porosity. However, starting in 2011, the CR treatment showed a notable decrease in soil bulk density and a significant increase in soil porosity, a trend that continued in subsequent years and stabilized after 2013. Specifically, the soil bulk density under the CR system gradually decreased to approximately 1.28 g·cm-3, while soil porosity increased to 52.64%. Compared to the FP treatment, the soil bulk density in the CR treatment decreased by 4.41% in 2011, 5.19% in 2013, and 5.88% in 2022. Concurrently, soil porosity in the CR treatment increased by 3.06% in 2011, 5.28% in 2013, and 6.55% in 2022. These results indicate that the rice-crab ecological farming system significantly enhances soil structure, improving aeration and water infiltration, thereby creating a more favorable environment for crop growth (Table 2).
General Chemical Properties of Soil
Throughout the study period, there were no significant differences in soil pH and redox potential (Eh) between the two treatments. However, the rice-crab ecological farming system (CR) showed significant advantages in terms of organic matter content and total nitrogen content. Specifically, during the early years of the study (2007-2008), there were no significant differences in organic matter and total nitrogen content between the CR and FP treatments. However, from 2009 onwards, the CR treatment significantly outperformed the FP treatment in both parameters (p<0.05). For instance, in 2009, the organic matter content in the CR treatment reached 28.2 g·kg-1, which was 12.8% higher than in the FP treatment. The total nitrogen content in the CR treatment was 1.55 g·kg-1, 8.4% higher than in the FP treatment. This trend continued and further strengthened in subsequent years. By 2022, the organic matter content in the CR treatment increased to 29.1 g·kg-1, a 14.9% increase compared to the FP treatment. Similarly, the total nitrogen content in the CR treatment increased to 1.63 g·kg-1, a 14.5% increase compared to the FP treatment (Table 3).
Table 2.
Physical properties of soil.
Table 3.
Effect of perennial rice-crab system on soil general chemical properties.
Soil Available Nutrient Contents
The soil in the experimental area demonstrated an abundance of hydrolysable nitrogen, an excess of available potassium, and a moderately lower level of available phosphorus. Available nutrient indicators serve as metrics for the soil’s capacity to provide nutrients readily accessible to plants during the growing season. As illustrated in Fig. 1, over the 16-year period, all available nutrient indicators for the FP treatment exhibited non-significant variations, with mean values of 99.3 mg·kg-1 for hydrolysable nitrogen, 10.11 mg·kg-1 for available phosphorus, and 198 mg·kg-1 for available potassium. In contrast to FP, the CR treatment demonstrated significant alterations in all indicators from 2007 to 2010, but insignificant changes from 2011 to 2022. Notably, the hydrolysable nitrogen, available phosphorus, and available potassium indicators for the CR treatment experienced substantial changes from 2007 to 2010, increasing from 102 mg·kg-1 to 123 mg·kg-1, 10.8 mg·kg-1 to 13.0 mg·kg-1, and 209 mg·kg-1 to 228 mg·kg-1, respectively. Subsequent to 2010, the interannual variations in these indicators for the CR treatment were statistically non-significant, maintaining mean values of 122 mg·kg-1 for hydrolysable nitrogen, 12.6 mg·kg-1 for available phosphorus, and 230 mg·kg-1 for available potassium. Throughout the 16-year duration, the CR treatment witnessed a notable increase in all available nutrient indicators, with percentage increments as follows: 20.1% for hydrolysable nitrogen, 22.2% for available phosphorus, and 14.7% for available potassium, in comparison to the FP treatment.
Soil Exchangeable Base Ions Contents
As additional testing for soil exchangeable salt base ion content was conducted only in 2022, our study presents the results for that specific year. From Table 4, it is evident that, in comparison to the FP treatment, the CR mode demonstrates a consistent trend of decreasing ion content. Notably, the levels of exchangeable Na+ and Ca2+ ions exhibit a significant reduction. Given that the experimental area is characterized by coastal saline-alkali soil, the exchangeable Na+ ion content in the soil is considerably higher than that found in conventional soils. Through the field practices implemented under the rice-crab farming model, there is a significant decrease in the levels of Na+ and Ca2+ ions within the plots.
Enzyme Activities in Soils
As depicted in Fig. 2, the URE activity in the CR treatment significantly lags behind that of the FP treatment, suggesting diminished urease activity within the rice-crab farming system compared to conventional rice cultivation. Typically, urease activity shows a significant positive correlation with soil organic matter content, total nitrogen, available nitrogen content, and total porosity. However, in this study, all indicators of the CR treatment surpass those of the FP treatment, except for urease content, which displays an inverse trend. This deviation may stem from the FP treatment incorporating a higher amount of inorganic ammonium nitrogen in the base fertilizer, totaling 300 kg·hm-2. This heightened urease activity induced by the substrate promotes the conversion of ammonium nitrogen to nitrate nitrogen, facilitating rice growth and development. Conversely, in the CR treatment, the total nitrogen application in the soil is 270 kg·hm-2, significantly lower than that in the FP treatment, with 30% of the nitrogen being organic nitrogen, resulting in relatively low urease activity. Furthermore, urease activity correlates with the timing of exogenous nitrogen application in the soil.
Fig. 1.
Soil available nutrient contents in different cropping systems. Note: Significant differences between treatments are indicated by different letters (p<0.05).
Alkaline phosphatase (AKP) plays a crucial role in converting organic phosphorus in the soil into inorganic phosphorus, thus enhancing its availability for crops. The activity of alkaline phosphatase exhibits a significant negative correlation with soil phosphorus levels. In the context of AKP, the FP treatment demonstrates markedly higher activity compared to the CR treatment, indicating lower effective phosphorus content in the FP treatment soil than in the CR treatment soil. This observation aligns with the available phosphorus content values in this study. Specifically, the FP treatment soil exhibits moderately low available phosphorus levels, averaging 10.0 mg·kg-1 over 16 years, while the CR treatment soil presents moderately higher available phosphorus levels, averaging 12.3 mg·kg-1 over the same period (Fig. 1). This discrepancy could be attributed to the enhanced AKP activity in the FP treatment, facilitating the release of organic phosphorus and its subsequent absorption by rice. Conversely, the significant increase in available phosphorus content in the CR treatment adequately meets the requirements for rice growth, resulting in reduced alkaline phosphatase activity.
Economic Benefits
The findings, as summarized in Table 5, reveal that during the years 2021 and 2022, the CR treatment exhibited a marginal increase in rice yield compared to the FP treatment, albeit without achieving statistical significance. Notably, the CR treatment, characterized by distinct fertilization patterns, featured a reduced proportion of inorganic nitrogen coupled with a higher proportion of organic nitrogen. Consequently, the rice quality within the CR treatment surpassed that of the FP treatment, precipitating a 13.8% escalation in the price of CR-treated rice. Additionally, the CR treatment demonstrated elevated crab output, averaging approximately 20,000 RMB per hectare. When scrutinizing the net income implications, it becomes apparent that the CR treatment yielded a noteworthy average increment of 18,269 RMB per hectare in economic benefits across 2021 and 2022.
Moreover, the nitrogen utilization efficiency within paddy fields operating under the rice-crab farming system witnessed a commendable rise of 10.3%. This enhancement in efficiency is particularly notable when juxtaposed against the FP treatment’s nitrogen fertilizer application, which amounted to 300 kg N·hm- 2 in contrast to the CR treatment’s lower total nitrogen application of 270 kg N·hm-2, with 30% being organic nitrogen. The discernible improvement in nitrogen utilization efficiency within the rice-crab farming system in comparison to the FP treatment signifies a substantial boon.
Discussion
Changes in soil physical properties generally occur at a much slower pace compared to changes in chemical properties [30]. Experimental monitoring conducted over a span of 16 years in rice-crab farming fields reveals a decrease in soil bulk density and an increase in total porosity, indicative of improved soil structure. The bulk density of the soil under the CR system gradually decreased to approximately 1.28 g·cm-3, while soil porosity increased to 52.64% by 2022. These changes are primarily attributed to the field activities of river crabs, which disrupt the soil plow layer, enhancing soil aeration and improving soil pore structure [31]. Additionally, enhancements in fertilizer composition and residual river crab bait significantly elevate soil organic matter content, consequently reducing soil bulk density and enhancing soil structure [32]. Throughout the study period, soil pH and redox potential (Eh) showed no significant differences between the two treatments. However, the CR system exhibited significant advantages in terms of organic matter content and total nitrogen content. From 2009 onwards, the organic matter content in the CR treatment significantly surpassed that in the FP treatment, reaching 29.1 g·kg-1 by 2022, a 14.9% increase compared to the FP treatment. Similarly, the total nitrogen content in the CR treatment increased to 1.63 g·kg-1, a 14.5% increase compared to the FP treatment. This trend may be ascribed to the disturbance of water and soil by river crabs, leading to heightened dissolved oxygen content in water and improved soil redox conditions [33].
Fig. 2.
Enzyme activities in soils with different cropping systems (in 2022). Note: Significant differences between treatments are indicated by different letters (p<0.05).
The augmentation in nutrient and organic matter content within rice-crab farming fields is partially attributed to the annual application of organic-inorganic compound fertilizers, containing 30% organic nitrogen. This organic nitrogen, not entirely decomposed and utilized within the same year, accumulates over time, thereby augmenting the soil’s nutrient reservoir capacity [34-36]. Additionally, to foster high-quality river crabs, bait is continuously introduced into rice fields during their growth [37]. With an annual input of 1050 kg·hm-2, a portion of the crab feed remains unconsumed in the rice fields, consequently increasing soil organic matter, total nitrogen, and total potassium content. Furthermore, weeds and aquatic organisms within the fields are consumed by river crabs and subsequently converted into feces, contributing to an increase in organic fertilizer within the rice fields [38]. Our study denotes that while the change in soil total phosphorus content in the rice-crab farming system is insignificant, available phosphorus content has markedly increased. This phenomenon may be attributed to the increased exogenous phosphorus being readily absorbed and utilized by plants, consequently resulting in a significant rise in active phosphorus content. Additionally, river crab excreta harbors abundant microorganisms and undigested protein from feed [39]. Partially digested feed components undergo breakdown and oxidation in water, elevating the available nutrient content and total microbial population within the rice fields [2]. Moreover, the foraging behavior of river crabs, wherein they consume weeds and floating organisms in field water, diminishes the absorption of available nutrients in the soil by other organisms, thereby furnishing adequate nutrients for rice growth [40]. The CR system also demonstrated notable improvements in soil enzyme activities, particularly alkaline phosphatase (AKP), which plays a crucial role in converting organic phosphorus into inorganic phosphorus, enhancing its availability for crops. The activity of AKP was significantly higher in the CR system, reflecting the increased available phosphorus content and meeting the nutrient requirements for rice growth. Economically, the CR system provided substantial benefits over the FP system. While rice yield differences between the two systems were not statistically significant, the quality of rice in the CR system was superior, resulting in a 13.8% increase in rice prices. Moreover, crab production within the CR system yielded a net economic advantage of approximately 18,269 RMB per hectare, demonstrating the dual benefits of rice and crab production. The nitrogen utilization efficiency in the CR system also witnessed a commendable rise of 10.3%, indicating a more efficient use of nitrogen fertilizers.
Table 5.
Economic benefits of different cropping systems.
In the rice-crab farming ecological system, rice and crabs coexist synergistically, with rice fields serving as a conducive habitat and a source of feed for river crabs. The crabs, in turn, consume weeds and supplementary feed, the remnants of which return to the fields as organic manure. Organic nutrients supplant some of the roles of chemical nutrients, thereby reducing the overall input of chemical nutrients and curbing excessive fertilizer usage, consequently enhancing nutrient utilization efficiency and mitigating chemical fertilizer emissions into the environment. The foraging behavior of river crabs, characterized by their consumption of weeds, aquatic plants, and waterborne insects, optimizes the growth environment for rice, creating conditions unfavorable for the proliferation of diseases and pests. Consequently, this diminishes the frequency and quantity of chemical pesticide applications, fostering the sustainable advancement of rice cultivation. Furthermore, the ecological farming model substantially bolsters rice growth and quality, coupled with the production of high-value aquatic products, thereby augmenting farmers’ income and fortifying their resilience to market vicissitudes. Additionally, it enriches market supply. Therefore, the rice-crab ecological farming model epitomizes a win-win scenario, ensuring both economic prosperity and ecological sustainability in rice cultivation.
Conclusions
The results of a 16-year field experiment in the rice-crab farming plots demonstrate that the long-term rice-crab farming model significantly improves soil physical, chemical, and biological properties. Especially in the initial 3 to 4 years, the soil bulk density significantly decreases, while soil porosity markedly increases. Soil organic matter, total nitrogen content, and available nitrogen, phosphorus, and potassium contents all show significant increases. Over the subsequent 13 years, these indicators exhibit no significant changes and reach a stable state. In terms of economic performance, the improvement in rice quality and the output of river crabs in the rice-crab farming system significantly boost farmers’ income, with an increase in income exceeding 18,000 RMB per hectare. In conclusion, the rice-crab farming model is highly recommendable for widespread adoption, both from an economic and ecological perspective.
