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Review

The Effectiveness of Biofloc Technology and Its Application Prospects in Sea Cucumber (Apostichopus japonicus) Aquaculture: A Review

by
Haoran Xiao
1,2,
Shufeng Li
1,2,
Zitong Wang
1,
Ye Tian
1,2,
Qiwei Zuo
1,2,
Fenglin Tian
1,2,
Yongjie Wang
1,2,
Chong Zhao
1,2,3 and
Jun Ding
1,2,3,*
1
Key Laboratory of Mariculture & Stock Enhancement in North China’s Sea Ministry of Agriculture and Rural Affairs, Dalian Ocean University, Dalian 116023, China
2
Liaoning Provincial Key Laboratory of Northern Aquatic Germplasm Resources and Genetics and Breeding, Dalian Ocean University, Dalian 116023, China
3
Dalian Jinshiwan Laboratory, Dalian 116034, China
*
Author to whom correspondence should be addressed.
Fishes 2024, 9(11), 457; https://doi.org/10.3390/fishes9110457
Submission received: 9 September 2024 / Revised: 2 November 2024 / Accepted: 8 November 2024 / Published: 10 November 2024
(This article belongs to the Special Issue Biofloc Technology in Aquaculture)
Versions Notes

Abstract

:
This review aims to advance the development of biofloc technology (BFT), providing more sustainable and efficient practices for the farming of the Japanese sea cucumber (Apostichopus japonicus). BFT is a sustainable aquaculture method that promotes nutrient recycling and effective carbon source management, offering significant advantages such as improving water quality, enhancing growth performance, and boosting the physiological activity and disease resistance of cultured animals. In A. japonicus farming, the optimal carbon source is glucose, and the ideal carbon-to-nitrogen (C/N) ratio ranges between 15 and 20. Microbial additives, such as the Bacillus species, have been shown to enhance biofloc formation and growth, as well as the immune responses in A. japonicus. However, the technology also faces limitations, including finding suitable biofloc culture protocols that match the physiological habits of A. japonicus and potential challenges with biofloc stability under varying environmental conditions. Based on existing research, this review discusses these limitations in the farming of A. japonicus. Additionally, it compares biofloc farming models for other economically important aquatic species. By addressing these key aspects, this review offers insights to enhance BFT performance, ultimately contributing to more efficient and sustainable A. japonicus aquaculture practices.
Keywords:
biofloc technology; water quality parameters; Apostichopus japonicus; growth performance; physiological indicators
Key Contribution: The main contribution of this review lies in systematically exploring the application prospects of biofloc technology (BFT) in A. japonicus farming, particularly its role in improving water quality, enhancing growth performance, and boosting immune capacity. This article also addresses the specific physiological needs of A. japonicus, proposing recommendations for optimizing carbon source selection and controlling biofloc protein levels, providing essential theoretical support and technical guidance for A. japonicus aquaculture.

1. Introduction

Since the 1990s, bioflick technology (BFT), first introduced to aquaculture by Yoram Avnimelech, has been widely adopted in the field [1]. In recent years, BFT has gained increasing attention due to its advantages in energy efficiency and emissions reduction. BFT enhances the carbon-to-nitrogen ratio in water by adding additional carbon sources, thereby promoting microbial growth [2,3,4]. This method processes the nitrogenous waste produced during aquaculture through microbial metabolism, maintaining low levels of harmful nitrogen in the system [5,6,7]. Additionally, BFT promotes water recycling. It reduces the chances of polluted water entering the system, thereby lowering the risk of disease. Moreover, BFT decreases the discharge of pollutants such as uneaten feed, feces, total ammonia nitrogen (TAN), and urea, mitigating eutrophication problems [8]. Bioflocs are rich in various nutrients and microbial metabolites, such as lipopolysaccharides, peptidoglycans, and glucans, which can modulate the gut microbiota of cultured organisms. This modulation enhances growth performance and induces nonspecific immune responses, strengthening the immune system and improving the resistance to pathogens, overall health, and productivity [9,10].
The Japanese sea cucumber (Apostichopus japonicus), an important commercially farmed species worldwide, has seen rapid expansion in aquaculture over the past few decades, becoming a highly demanded aquatic product in the market [11,12]. According to the 2023 China Fisheries Statistical Yearbook, China’s A. japonicus production in mariculture reached 248,509 tons in 2022, an increase of 11.59% compared to 2021 [13]. During this period, the use of intensive farming practices in juvenile A. japonicus farming gradually increased. While this model improves productivity by increasing feed inputs, it also results in more waste, environmental degradation, and higher farming costs [14]. Statistics show that only 20−30% of feed is effectively utilized by the farmed organisms, with the remainder becoming water pollutants, releasing toxic substances such as ammonia nitrogen and nitrite nitrogen [8], which not only pollute the water but also increase treatment costs. However, intensive farming practices also pose challenges, such as reducing the living space for animals, worsening environmental conditions, and leading to frequent disease outbreaks [15]. To prevent and treat diseases, antibiotics and chemical disinfectants are often used extensively, which may lead to increased bacterial resistance and even the emergence of superbugs [16,17,18,19,20]. Therefore, stricter regulation and supervision are essential to prevent these issues [21]. Additionally, promoting sustainable ecological farming practices in A. japonicus aquaculture has become increasingly urgent.
Currently, BFT has achieved significant results in the farming of economically important aquatic species such as Oreochromis niloticus and Litopenaeus vannameil, but its application in A. japonicus farming systems remains relatively limited [22,23]. This paper reviews the mechanisms and effects of BFT on water purification and A. japonicus farming and discusses biofloc farming models in other economically important aquatic species. It aims to explore the application prospects of BFT in A. japonicus farming, providing theoretical support and technical guidance for the sustainable development of aquaculture in China.

2. The Impact of Biological Flocs on Water Quality

Bioflocs consist of bacterial communities, protozoa, metazoans, microalgae, and organic particles. These components aggregate into active flocculated substances through the adhesion of bacterial extracellular polymeric substances (EPSs) or surface charge attraction [10,24,25]. As the carbon-to-nitrogen ratio increases and time progresses, bioflocs accumulate in the aquaculture water. The quantity of bioflocs is typically evaluated using the biofloc volume (BFV) and total suspended solids (TSS) [26]. In aquaculture systems, bioflocs form complex food chain structures; their mechanisms for processing nitrogenous pollutants include ammonification, nitrification, denitrification, and microbial assimilation [27,28].

2.1. Nitrogen Removal Mechanism

In aquaculture systems, nitrogen transformation processes are influenced by microbial functionality, environmental conditions, and management practices. Understanding and optimizing these factors are essential for enhancing the environmental sustainability and economic efficiency of aquaculture operations [29].
In most environments, heterotrophic microorganisms can decompose proteins and release ammonia [30,31]. Studies indicate that in intensive indoor aquaculture systems for Pacific white shrimp, the predominant ammonifying bacteria include Aeromonas, Alcaligenes, and Enterobacter [29]. Another study isolated a strain of Bacillus megaterium from shrimp aquaculture water that can perform both ammonification and ammonia oxidation, further confirming the presence of ammonifying bacteria in aquaculture environments [32]. Microbial assimilation can convert harmful nitrogen into microbial biomass protein, promoting growth and reproduction, with the resulting bioflocs serving as supplemental feed for cultured organisms [33]. Research by Schneider et al. demonstrated that the growth of heterotrophic bacteria in aquaculture systems can convert 7% of feed nitrogen into bioflocs, thereby reducing nitrogen loss [34]. Other studies have shown that BFT significantly enhances nitrogen utilization in tilapia aquaculture systems. Consequently, recent research has focused on enhancing the assimilation capabilities of bioflocs [35]. Assimilation occurs in three scenarios: (1) When heterotrophic microorganisms use ammonia nitrogen as a nitrogen source and organic carbon as a carbon source, 1 g of ammonia nitrogen consumption requires 15.17 g of carbohydrates, 3.57 g of total alkalinity, and 4.17 g of oxygen, producing 8.07 g of volatile suspended solids (VSSs) [36]. (2) When the organic carbon is insufficient, autotrophic nitrifying bacteria use ammonia nitrogen and HCO3− as nitrogen and carbon sources. Under these conditions, assimilating 1 g of ammonia nitrogen produces 0.2 g of volatile suspended solids (VSSs), 0.98 g of nitrate nitrogen, and 5.85 g of carbon dioxide [36,37]. (3) Denitrifying bacteria, using nitrate nitrogen as a nitrogen source and organic carbon as a carbon source, reduce 96% of nitrate nitrogen to nitrogen gas through denitrification, with the remaining 4% converted into microbial protein [38]. In biofloc aquaculture systems, the gradual accumulation of nitrate nitrogen indicates that ammonia nitrogen undergoes nitrification, eventually completing full nitrification. Studies have shown that using BFT technology in Pacific white shrimp farming can increase the nitrate nitrogen concentration in the water from 0 mg/L at the start of the experiment to 6 mg/L after 11 weeks. Denitrification requires specific environmental conditions, including sufficient organic carbon sources, to effectively reduce nitrate and nitrite nitrogen, converting them to nitrogen gas [39,40].

2.2. The Effects of Different Conditions on the Total Suspended Solids (TSS) and Biofloc Volume (BFV) in the Biofloc Culture System of A. japonicus

The effects of different conditions on the TSS and BFV in the biofloc culture system of A. japonicus are shown in Table 1. Research has shown that in ex situ cultured A. japonicus biofloc systems, inoculating bacterial solution at concentrations of 0, 40, 70, 100, and 120 mL/L increased the BFV and improved the ammonia nitrogen removal as the inoculum concentrations increased. The survival rate of A. japonicus increased with the inoculum concentration up to 100 mL/L but decreased at 120 mL/L, likely due to the stress caused by an excessively high BFV [36]. Another study, using different bacterial additives to culture bioflocs, including photosynthetic bacteria, Saccharomycetes, and Bacillus, showed that the TSS reached 50, 125, and 200 mL/L, respectively, with the Bacillus group having a significantly higher TSS and the highest A. japonicus weight gain. This may be due to Bacillus’ efficient organic matter degradation capabilities and its ability to form stable flocs [28,41,42]. These characteristics allow Bacillus to rapidly decompose feed residues and excreta, increase the organic matter concentration, and form stable flocs that capture and accumulate suspended solids, thereby providing rich nutrients and a good water quality environment for cultured organisms [41]. Another study found that different carbon sources (glucose, sucrose, and starch) had varying effects on bioflocs in A. japonicus farming. Over a 60-day experiment, the BFV reached 22, 17, and 9 mL/L, and the TSS was 225, 190, and 160 mg/L, respectively [43]. As a simple monosaccharide, glucose can be quickly and efficiently utilized by microorganisms, promoting rapid growth and stable biofloc formation, thereby increasing the BFV and TSS [28,44]. Although sucrose is less efficient than glucose, it still effectively supports microbial growth and floc formation [45]. In contrast, starch, due to its complex polysaccharide structure, requires more time and additional enzymatic activity for effective decomposition, resulting in the lowest BFV and less microbial growth and floc formation [46,47]. Thus, different types of carbon sources significantly affect microbial growth efficiency, biofloc stability, and the accumulation of suspended solids [48].
In biofloc systems, the TSS and BFV are significantly influenced by the carbon source type, carbon-to-nitrogen ratio, and bacterial additives [49]. Appropriate levels of TSS and BFV can effectively improve water quality, provide nutrients, manage waste, support higher stocking densities, and promote the health and growth of cultured organisms [50,51]. However, an excessively high TSS can cause water turbidity and biological stress, thus requiring careful control. Studies have shown that simple carbon sources like glucose can rapidly increase the BFV and TSS [49]. Bacillus, with its efficient organic matter degradation capabilities, significantly increases the TSS and weight gain; in contrast, complex starch, due to its lower utilization efficiency, results in a lower BFV and TSS [44]. For nitrogen removal, heterotrophic, nitrifying, and denitrifying bacteria effectively convert ammonia nitrogen, nitrate nitrogen, and nitrite nitrogen through different assimilation mechanisms. Based on the current water quality, optimizing the carbon source types, carbon-to-nitrogen ratio, and bacterial additives can specifically enhance the water quality and nitrogen utilization efficiency. Future research should focus on optimizing the operational conditions of biofloc systems and exploring efficient microbial formulations to improve water quality stability and aquaculture yield [44,52].

3. Effects of BFT on A. japonicus and Common Species

3.1. Growth Performance

The effects of BFT on the growth of A. japonicus and other common aquatic species are shown in Table 2. In BFT, the targeted addition of beneficial bacterial strains is a key factor in establishing an effective biofloc system [53]. Studies have shown that in the bioflocs cultured with sucrose as the carbon source, the groups treated with beneficial bacteria (such as Bacillus subtilis and nitrifying bacteria) exhibited a higher growth performance. In contrast, the natural seawater group without beneficial bacteria showed a lower growth performance [54]. This could be related to the probiotics or the bioflocs they form, which can improve water quality by reducing ammonia and nitrite concentrations and increasing digestive enzyme activity [54]. Research also indicates that A. japonicus cultured in BFT with different carbon sources (glucose, starch, and sucrose) showed a higher growth performance than the control group. Notably, the group using glucose as the carbon source achieved a weight gain of 47.32%, demonstrating a significant advantage, consistent with the findings in tilapia biofloc culture [55]. Some researchers suggest that, as a monosaccharide, glucose has a high utilization efficiency, allowing microorganisms to rapidly proliferate, thereby significantly increasing the BFV and producing more protein and fat. Conversely, starch showed the lowest weight gain, likely due to a lower microbial utilization efficiency, which affects biofloc formation [48]. The effects of different ratios of biofloc substitute feed on the physiological growth of A. japonicus are shown in Table 3. Further studies have shown that, when collected bioflocs were used to replace part of the feed (a 15% to 20% replacement rate) for A. japonicus, these groups demonstrated significant growth advantages [56]. The nutrients in bioflocs significantly increased the activity of trypsin, lipase, and amylase in A. japonicus, enhancing feed digestion and nutrient absorption, such as extracellular enzymes. However, excessively high levels of biofloc addition (30%, 45%, and 60%) inhibited A. japonicus growth, possibly due to high microbial protein levels affecting feed palatability and digestibility [57]. Additionally, this aquaculture model has shown significant advantages in other species, further demonstrating the broad applicability and potential benefits of biofloc technology in aquaculture [22,55,58,59].

3.2. Antioxidant Reaction

The effects of BFT on the antioxidant enzyme activity of Apostichopus japonicus and other common aquatic species are shown in Table 4. Biofloc technology can effectively enhance the antioxidant capacity of cultured organisms by improving the aquaculture environment, as demonstrated in several studies. Superoxide dismutase (SOD) is one of the major antioxidant enzymes in A. japonicus, primarily functioning to convert a superoxide anion (O2−) into hydrogen peroxide, thereby protecting A. japonicus from oxidative damage. SOD helps maintain the metabolic balance of reactive oxygen species (ROS) and is a primary defense mechanism against oxidative stress [63]. Catalase (CAT), mainly present in peroxisomes and mitochondria, forms part of the antioxidant defense mechanism by converting hydrogen peroxide into water and oxygen [64]. Studies have shown that in the coelomic fluid of A. japonicus cultured in bioflocs, the activities of SOD and CAT increased significantly, especially in the glucose group, where the SOD activity was notably higher than in the sucrose and starch groups [48]. The glycogen content in the biofloc system with glucose as the carbon source was also significantly higher than in the other treatment groups, consistent with the findings in tilapia biofloc culture [65]. This may be due to the increased production of glucose under stress conditions through gluconeogenesis and glycogenolysis, stimulated by cortisol, to meet the energy demands related to stress and to activate anti-stress responses [48]. Other studies observed that, when collected bioflocs were used to replace feed at 5%, 10%, 15%, and 20% replacement rates, the higher replacement levels resulted in increased SOD activity (Table 3) [56]. The results indicated that bioflocs, rich in various antioxidants such as vitamins, can effectively neutralize free radicals and reduce oxidative stress damage in A. japonicus [43]. The ability of bioflocs to enhance the SOD activity in the body wall of A. japonicus may be due to increased antioxidant enzymes preventing lipid peroxidation and boosting antioxidant capacity. Similar results have been observed in related studies on other species [66].

3.3. Immunoreaction

The effects of BFT on the immune enzyme activity of Apostichopus japonicus and other common aquatic species are shown in Table 5. In A. japonicus farming, A. japonicus cultured with biofloc technology exhibit significant nonspecific immune responses. Lysozyme (LZM) is a key nonspecific immune enzyme in invertebrates that plays a crucial role in defending against invading pathogens, particularly effective in removing Gram-positive and Gram-negative bacteria [70]. LZM hydrolyzes the β−1,4−glycosidic bonds in the bacterial cell walls, leading to bacterial lysis and preventing bacterial infections [71]. Additionally, LZM has a defense mechanism against oxidative stress, enhancing phagocytic activity as blood cell counts and bactericidal activity increase, thereby boosting the overall immunity and antioxidant capacity [72]. Studies have shown that both A. japonicus cultured with biofloc technology and those fed with collected bioflocs exhibit significantly increased LZM activity. This is because bioflocs act as immunostimulants, enhancing the innate immune response in A. japonicus [43,48]. Another study showed that A. japonicus cultured in bioflocs with sucrose, glucose, and starch as the carbon sources exhibited a high LZM activity; however, the LZM activity in the starch group was significantly lower than in the other two groups. This may be due to the lower utilization efficiency of starch as a carbon source, affecting microbial growth rates [73,74]. Additionally, the higher proportion of Vibrio and the lower proportion of Bacillus in the A. japonicus gut may have limited the antibacterial effect. However, in BFT applied to tilapia farming, even with less efficient carbon sources like rice bran and wheat by-products, tilapia’s LZM activity significantly increased. This could be because tilapia’s target organ is the liver, which can significantly enhance LZM activity by optimizing metabolic processes and boosting the immune function [75,76]. In contrast, A. japonicus lack a liver, have simpler metabolic processes, and cannot effectively utilize complex carbon sources, resulting in a lower LZM activity [77,78]. In invertebrates, alkaline phosphatase (ALP) and acid phosphatase (ACP) are involved in various immune mechanisms. ALP neutralizes the bacterial endotoxins in the digestive tract, protecting the gut from infection. It also plays a role in the growth and repair of bones and exoskeletons. ACP is crucial in regulating exoskeletal mineralization and the signaling in the immune cells, helping invertebrates adapt to various environmental stresses [79,80]. Studies have shown that, in A. japonicus cultured with BFT, ACP and ALP activities are significantly increased, possibly due to the immune responses and physiological adaptations to environmental stress in the biofloc environment [48,54,56]. In biofloc-cultured A. japonicus, LZM activity is significantly enhanced and ALP and ACP activities increase to cope with immune responses under high-density farming conditions. Similar results have been observed in the biofloc farming of other species [70].

3.4. Disease Resistance

The effects of BFT on the disease resistance of A. japonicus and other common aquatic species are shown in Table 6. A study demonstrated that when A. japonicus was challenged with Vibrio splendidus (108 cfu/L), those in the biofloc system using glucose as the carbon source had a cumulative mortality rate of 50%; in the starch-based system, it was 55%; and in the sucrose-based system, it was 62%. In contrast, the control group had a cumulative mortality rate of 90% [48]. This might be because the A. japonicus in the glucose-based biofloc system exhibited significantly increased total coelomic cell counts, phagocytic activity, and respiratory burst activity, leading to the stronger inhibition of pathogens. Complement components bind to pathogens, forming membrane attack complexes that cause pathogen cell lysis, effectively preventing infection [48]. Additionally, similar results have been observed in studies involving other species. For example, Gustilatov’s study found that when Vibrio parahaemolyticus was used to challenge Litopenaeus vannamei at different concentrations, the shrimp in the biofloc system had significantly lower cumulative mortality rates than the control group. This indicates that bioflocs can significantly enhance the nonspecific immune responses of shrimp, increasing their disease resistance [84]. Bioflocs not only inhibit bacterial infections but also have significant effects on viral inhibition. Ekasari’s research indicated that in a biofloc system using rice bran as the carbon source, the survival rate of Litopenaeus vannamei significantly improved following artificial infection with the IMNV (infectious myonecrosis virus). This effect is believed to be due to the bioflocs enhancing the activity or efficiency of the shrimp’s immune system [85]. Haridas et al. found that in a biofloc system using wheat flour, when Aeromonas hydrophila (106 CFU/L) was used to challenge Oreochromis niloticus, the survival rates were 83.3% at a density of 200 fish/m³, 75% at 300 fish/m³, and 62.5% at 350 fish/m³, all significantly higher than the control group. This suggests that bioflocs positively influence disease resistance in tilapia. However, as the stocking density increases, the survival rates decrease, possibly due to faster disease spread in high-density environments, an increased immune system burden, and decreased animal health, making them more susceptible to disease [66].
Overall, BFT shows significant advantages in A. japonicus farming. The targeted addition of beneficial bacterial strains and the selection of suitable carbon sources (such as glucose) can significantly improve the growth performance, antioxidant capacity, and immune responses in A. japonicus. Research indicates that adding beneficial bacterial strains can improve the water quality, increase the biofloc production, and enhance the digestive enzyme activity in A. japonicus. Additionally, biofloc systems using glucose as the carbon source show the best weight gain and increase the antioxidant enzyme activity in the coelomic fluid of A. japonicus. Moreover, bioflocs can enhance lysozyme (LZM) activity and alkaline phosphatase (ALP) and acid phosphatase (ACP) levels, boosting immune responses and the resistance to pathogens. However, excessive biofloc addition may inhibit A. japonicus growth and affect feed palatability and digestibility. Furthermore, in high-density farming environments, the disease resistance effect of bioflocs may be compromised, leading to lower survival rates [66].

4. Application Prospect of Bioflocs in the Culture of A. japonicus

In recent years, research on the impact of biofloc technology (BFT) on water quality and the physiological growth of common species like shrimp and fish has matured significantly. However, there is still a lack of studies on different aquaculture species, particularly regarding the effects of bioflocs on water quality and the physiological growth of A. japonicus. In both theoretical and practical applications, the use of BFT in A. japonicus farming requires further in-depth research, especially in optimizing farming conditions and improving production efficiency. This section briefly outlines the effects of BFT on water quality and the growth physiology of aquatic organisms and, based on previous studies, proposes several areas for further exploration regarding the application of BFT in A. japonicus farming.

4.1. Study on the Tolerance of A. japonicus to the BFV and TSS and Water Quality Management

As a marine organism, the A. japonicus has specific requirements for water turbidity [41]. Studies have shown that excessive turbidity can adversely affect the survival and growth of A. japonicus [36]. Currently, systematic research on the tolerance of A. japonicus to the biofloc volume (BFV) and total suspended solids (TSS) is lacking. Therefore, exploring the survival and growth of A. japonicus under different BFV and TSS conditions is crucial for optimizing the aquaculture environment. This could help improve survival rates and growth speeds, providing scientific evidence for future A. japonicus farming. It is recommended to control the water quality parameters and systematically observe the growth, survival rate, and physiological responses of A. japonicus to determine their tolerance thresholds for the BFV and TSS. Effective water quality management measures, such as regular water replacement, the use of filtration systems, controlled feeding, and adjusting stocking densities, should be implemented to maintain the BFV and TSS within the tolerable range for A. japonicus.

4.2. Study on the Optimal Culture Density of A. japonicus in Biological Floc Systems

Stocking density is a key factor affecting the effectiveness of biofloc systems [86]. High stocking densities can increase the system load, leading to deteriorated water quality and heightened disease risks. Studies have shown that, when Aeromonas hydrophila was used to challenge tilapia in biofloc systems, survival rates decreased with increasing stocking density [66]. Similarly, high stocking densities in A. japonicus farming can lead to increased feeding and carbon sources, which subsequently raise BFV and TSS levels, adversely affecting A. japonicus growth. Conversely, low stocking densities can increase farming costs, resulting in insufficient biofloc formation to meet the nutritional needs of the animals [87]. Determining the optimal stocking density is crucial for maximizing the efficiency of biofloc systems in A. japonicus farming. The appropriate density should enhance growth rates and feed conversion efficiency while effectively reducing farming costs and improving economic returns. It is suggested that, when determining the optimal stocking density of A. japonicus in biofloc systems, factors such as the growth rate, survival rate, feed conversion ratio, and water quality changes under different densities are considered. By optimizing the stocking density, better farming outcomes can be achieved. Any adjustments to feeding rates and carbon source additions should be made based on the stocking density to avoid excessive feeding that may increase the BFV and TSS, thus maintaining a stable and healthy water quality.

4.3. Optimization of Feeding Habits and the Floc Sedimentation of A. japonicus

Compared to other marine organisms, A. japonicus have a higher tolerance to ammonia nitrogen and nitrite nitrogen, allowing them to survive in harsher environments. However, their low efficiency in food particle intake may limit the utilization of the nutrients in bioflocs [88]. The A. japonicus is a deposit feeder that primarily uses its tentacle crown to capture organic particles from the sediment for food. Studies have shown that A. japonicus have a high feeding efficiency for particles in the 20-50 µm range. However, due to their slow movement and the structural limitations of their oral apparatus, they cannot directly capture suspended bioflocs, resulting in a low utilization rate of bioflocs. [89]. Most bioflocs remain suspended in the water due to water flow and aeration devices, while A. japonicus can only consume floc particles that settle at the bottom of the pond. This characteristic limits the direct application of BFT in A. japonicus farming. To improve BFT and make it more suitable for A. japonicus feeding habits, thereby enhancing farming outcomes, this study suggests exploring methods such as changing the water flow direction, improve the bottom aeration devices, and optimizing the floc composition to facilitate the settlement of bioflocs on the pond bottom, thus improving the feeding efficiency of A. japonicus.

4.4. Protein Requirements of A. japonicus and the Optimization of Floc Nutrients

Bioflocs may contain high protein levels, which is an important consideration. A. japonicus have relatively low protein requirements, and a high protein content may burden their digestive systems, potentially inhibiting normal growth [90]. Therefore, in designing biofloc systems, particular attention must be paid to controlling the protein content to avoid adverse effects on the health of A. japonicus. This can be achieved by adjusting feed formulations and optimizing floc composition to ensure that protein levels in bioflocs remain within acceptable ranges for A. japonicus, thereby promoting healthy growth. It is suggested that, when designing biofloc systems, selecting the appropriate feed and carbon sources to control the protein levels in bioflocs is essential to avoid excessive protein burdens on the A. japonicus digestive system. Research should focus on adjusting feed formulations to ensure moderate protein levels, meeting the growth needs of A. japonicus without exceeding them. These adjustments are crucial for preventing potential digestive burdens due to excessive protein intake and optimizing the farming outcomes for A. japonicus.

5. Conclusions

This review summarized the potential and challenges of applying biofloc technology (BFT) in A. japonicus farming. BFT improved water quality, reduced nitrogenous waste, and enhanced the immune responses and antioxidant capacity in A. japonicus by adjusting the carbon-to-nitrogen ratio and optimizing microbial metabolism. Systems using glucose as the carbon source significantly improved the A. japonicus’s growth performance and nonspecific immune enzyme activity. However, research also indicated that an excessive biofloc volume (BFV) and total suspended solids (TSS) could place stress on A. japonicus, affecting their health. Given the specific physiological needs of A. japonicus, it was recommended to optimize the carbon source selection, control the protein levels, and adjust the biofloc sedimentation to improve the farming efficiency. Future studies were encouraged to further explore optimized BFT applications for sustainable A. japonicus aquaculture.

Author Contributions

H.X.: writing—original draft, investigation, data curation, and formal analysis; S.L.: data curation, writing—review, supervision, and funding acquisition; Z.W.: review and editing, and data curation; Y.T.: investigation and data curation; Q.Z.: investigation and data curation; F.T.: methodology and resources; Y.W.: methodology and resources; C.Z.: writing—review and supervision; and J.D.: supervision and funding acquisition. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Dalian Jinshitanwan Laboratory Demonstration Project (Dljswsf202401), the Major Agricultural Project of the Liaoning Provincial Science and Technology Department (Project No.: 2023JH1/10200007), and the Scientific Research Project of Dalian Bangchuidao Marine Products Co., Ltd. (Ding Jun, 2023).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All the relevant data are presented within this paper.

Conflicts of Interest

The authors declare that this study received funding from the Scientific Research Project of Dalian Bangchuidao Marine Products Co., Ltd. (the corresponding author, Jun Ding, has a collaborative relationship through a horizontal project). The funder had the following involvement with the study: data collection.

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Table 1. The effects of different conditions on total suspended solids (TSS) and biofloc volume (BFV) in the biofloc culture system of A. japonicus.
Table 1. The effects of different conditions on total suspended solids (TSS) and biofloc volume (BFV) in the biofloc culture system of A. japonicus.
CarbonC/NCultureAmount of InoculumPeriodBFV
mL/L		TSS
mg/L		Reference
**Bacillus Fermentation Liquid0 mg/L31 d2.5*[36]
40 mg/L4
70 mg/L5
100 mg/L12.5
120 mg/L17.5
Sucrose20:1Photosynthetic Bacteria104 cfu/L20 d*50[41]
Saccharomycetes125
Bacillus200
Glucose15:1**60 d22225[43]
Sucrose17190
Starch9160
Note: “*” indicates anything not mentioned in the original text.
Table 2. Effects of BFT on growth of A. japonicus and other common aquaculture species.
Table 2. Effects of BFT on growth of A. japonicus and other common aquaculture species.
SpeciesCarbonC/NPeriodGrowthReference
Apostichopus japonicus**60 d−[60]
+
+
+
×
×
×
Glucose15:160 d+[43]
Starch×
Sucrose+
Sucrose (0% Feed Replacement)20:130 d+[56]
Sucrose (10% Feed Replacement)+
Sucrose (15% Feed Replacement)−
Sucrose (20% Feed Replacement)×
Sucrose (No Bacteria)7:10
Sucrose/Fodder		60 d−[54]
Sucrose (Bacteria Addition)+
100% Sucrose20: 120 d+[41]
6.7:3.3 (Sucrose/Corn Starch)−
5:5 (Sucrose/Corn Starch)−
3.3:6.7 (Sucrose/Corn Starch)−
**60 d−[48]
+
+
−
Oreochromis niloticusMolasses8.4:174 d+[22]
Glycerinum15:174 d+[58]
Mannooligosaccharides+
Glucose15:1120 d+[55]
Starch15:130 d+[59]
Litopenaeus vannameiMolasses17:190 d+[23]
Tapioca10:1
Wheat Flour9:1
Millfeed12:136 d+[61]
Amaranth Seed
Oat Bran
Sucrose15:130 d+[62]
Note: “*” indicates anything not mentioned in the original text; “+” means significantly higher than the control group; “−” means significantly lower than the control group; and an “×” indicates no significant difference. The significant difference was (p < 0.05).
Table 3. Effects of different proportions of biological floc instead of feed on physiological growth of A. japonicus.
Table 3. Effects of different proportions of biological floc instead of feed on physiological growth of A. japonicus.
Replacement of Feed with BioflocsPeriodGrowthSOD ActivityLZM ActivityACP ActivityALP ActivityReference
5%60 d×****[60]
10%+
15%+
20%+
30%×
45%×
60%×
5%60 d×××××[48]
10%+++++
15%+++++
20%×++++
Note: “*” indicates anything not mentioned in the original text; “+” means significantly higher than the control group; and an “×” indicates no significant difference. The significant difference was (p < 0.05). Superoxide dismutase, SOD; lysozyme, LZM; acid phosphatase, ACP; and alkaline phosphatase, ALP.
Table 4. Effect of BFT on antioxidant enzyme activity of A. japonicus and other common aquaculture species.
Table 4. Effect of BFT on antioxidant enzyme activity of A. japonicus and other common aquaculture species.
SpeciesCarbonC/NEnzyme Activity TypePeriodTarget OrganResponseReference
Apostichopus japonicusGlucose15:1SOD60 dBody Fluid+[48]
Starch+
Sucrose+
Sucrose (0% Feed Replacement)20:1SOD30 dBody Wall+[56]
Sucrose (10% Feed Replacement)+
Sucrose (15% Feed Replacement)+
Sucrose (20% Feed Replacement)+
Glucose20:1SOD60 dBody Wall−[67]
Sucrose+
Corn Starch+
Sweet Potato Flour−
Oreochromis niloticusGlycerinum15:1SOD98 dSerum+[68]
Molasses+
Starch×
Glucose10:1SOD120 dLiver+[65]
15:1+
20:1−
Wheatmeal15:1SOD90 dLiver−[66]
Litopenaeus vannameiSucrose15:1SOD30 dPlasma+[62]
20:1
Bagasse*SOD60 dHepatopancreas+[69]
Rice Bran+
Straw−
Apostichopus japonicusGlucose15:1CAT60 dBody Fluid+[48]
Starch+
Sucrose+
Oreochromis niloticusGlycerinum15:1CAT98 dSerum+[68]
Molasses+
Starch+
Litopenaeus vannameiBagasse*CAT60 dHepatopancreas+[69]
Rice Bran+
Straw−
Note: “*” indicates anything not mentioned in the original text; “+” means significantly higher than the control group; “−” means significantly lower than the control group; and an “×” indicates no significant difference. The significant difference was (p < 0.05). Superoxide dismutase, SOD; and catalase, CAT.
Table 5. Effects of BFT on immunoenzyme activity of A. japonicus and other common aquaculture species.
Table 5. Effects of BFT on immunoenzyme activity of A. japonicus and other common aquaculture species.
SpeciesCarbonC/NEnzyme Activity TypePeriodTarget OrganResponseReference
Apostichopus japonicusGlucose15:1LZM60 dBody Fluid+[48]
Starch+
Sucrose+
Oreochromis niloticusSucrose10:1LZM98 dSerum×[81]
Glucose15:1LZM56 dSerum+[82]
Glycerinum15:1LZM84 dSerum+[58]
Glucose10:1LZM120 dLiver+[65]
15:1+
20:1+
Molasses15:1LZM53 dSkin−[83]
Wheat By-Product15:1LZM70 dLiver+[77]
Rice Bran+
Litopenaeus vannameiSucrose15:1LZM30 dPlasma×[62]
20:1
Bagasse−LZM90 dHepatopancreas+[69]
Rice Bran+
Straw−
Apostichopus japonicusGlucose15:1ACP60 dBody Fluid+[48]
Starch+
Sucrose+
Apostichopus japonicusSucrose (0% Feed Replacement)20:1ALP30 dBody Wall−[56]
Sucrose (10% Feed Replacement)+
Sucrose (15% Feed Replacement)+
Sucrose (20% Feed Replacement)−
Glucose20:1ALP60 dBody Wall+[67]
Sucrose+
Corn Starch+
Sweet Potato Flour×
Note: “+” means significantly higher than the control group; “−” means significantly lower than the control group; and an “×” indicates no significant difference. The significant difference was (p < 0.05). Lysozyme, LZM; acid phosphatase, ACP; and alkaline phosphatase, ALP.
Table 6. Effects of BFT on disease resistance of A. japonicus and other common aquaculture species.
Table 6. Effects of BFT on disease resistance of A. japonicus and other common aquaculture species.
SpeciesPathogenConcentrationCarbonC:NPeriodRate of SurvivalResponseReference
Apostichopus japonicusVibrio splendidus108 cfu/LGlucose15:114 d50%+[48]
Starch45%+
Sucrose38%+
Litopenaeus vannameiVibrio parahaemolyticus103 cfu/LMolasses10:121 d*+[84]
105 cfu/L×
107 cfu/L+
IMNV
(Infectious Myonecrosis Virus)		100 MLMolasses15:16 d*×[85]
Cassava×
Rice Bran+
Oreochromis niloticusAeromonas hydrophila106 cfu/LWheat Flour, 200 Fish/m315:13 d83.33%+[66]
Wheat Flour, 250 Fish/m383.33%+
Wheat Flour, 300 Fish/m375%+
Wheat Flour, 350 Fish/m362.5%+
Note: “*” indicates anything not mentioned in the original text; “+” means significantly higher than the control group; and an “×” indicates no significant difference. The significant difference was (p < 0.05).
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Xiao, H.; Li, S.; Wang, Z.; Tian, Y.; Zuo, Q.; Tian, F.; Wang, Y.; Zhao, C.; Ding, J. The Effectiveness of Biofloc Technology and Its Application Prospects in Sea Cucumber (Apostichopus japonicus) Aquaculture: A Review. Fishes 2024, 9, 457. https://doi.org/10.3390/fishes9110457

AMA Style

Xiao H, Li S, Wang Z, Tian Y, Zuo Q, Tian F, Wang Y, Zhao C, Ding J. The Effectiveness of Biofloc Technology and Its Application Prospects in Sea Cucumber (Apostichopus japonicus) Aquaculture: A Review. Fishes. 2024; 9(11):457. https://doi.org/10.3390/fishes9110457

Chicago/Turabian Style

Xiao, Haoran, Shufeng Li, Zitong Wang, Ye Tian, Qiwei Zuo, Fenglin Tian, Yongjie Wang, Chong Zhao, and Jun Ding. 2024. "The Effectiveness of Biofloc Technology and Its Application Prospects in Sea Cucumber (Apostichopus japonicus) Aquaculture: A Review" Fishes 9, no. 11: 457. https://doi.org/10.3390/fishes9110457

APA Style

Xiao, H., Li, S., Wang, Z., Tian, Y., Zuo, Q., Tian, F., Wang, Y., Zhao, C., & Ding, J. (2024). The Effectiveness of Biofloc Technology and Its Application Prospects in Sea Cucumber (Apostichopus japonicus) Aquaculture: A Review. Fishes, 9(11), 457. https://doi.org/10.3390/fishes9110457

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