The Asian swamp eel, Monopterus albus (Zuiew, 1793), is one of the most economically important freshwater fish species in China and other Asian countries (Zhou et al., 2002), namely, Cambodia, Singapore, Thailand, and Vietnam (Pedersen et al., 2014). Its production were close to 334, 215 tons, and the annual output value was nearly 23 billion yuan in 2022 (The Fisheries Bureau of Ministry of Agriculture, 2023). In China, three major farming regions with large-scale culture of M. albus are Hubei, Jiangxi, and Anhui, which account for 154, 279 tons, 89, 943 tons, and 32, 880 tons (The Fisheries Bureau of Ministry of Agriculture, 2023). Currently, pond cage culture is the main method for M. albus culture, and other methods are paddy field culture and soil pond culture.

Since the 21st century, recirculating aquaculture, as a new type of aquaculture mode, has addressed the drawbacks of traditional aquaculture methods, reduced the dependence of the aquaculture process on the surrounding water environment, reduced sewage discharge during the aquaculture process, increased yield and quality, and achieved green aquaculture. The application scale of recirculating aquaculture in freshwater fish and shrimp aquaculture is continuously expanding (Ahmed and Turchini, 2021). M. albus likes to live in groups and can adapt to high-density farming (Luo et al., 2014). In the aquaponics system, the survival rate of M. albus can be more than 79% (Portalia et al., 2019). Currently, M. albus is cultured at different scales in Hubei and Jiangxi, China, but there is a lack of studies on recirculating aquaculture technology for this species.

Because of the lack of substantial breakthroughs in the artificial reproduction of M. albus, the current production of seedlings is mainly relies on wild fishing. Generally, wild seedlings require 2–3 weeks of open domestication after being stocked, and the mortality rate of seedlings is relatively high at this stage (Yuan et al., 2020). Poor nutrition and water quality and parasitic, bacterial, and viral infections can cause serious losses in M. albus juveniles under intensive culture conditions (Gao et al., 2016; Shao et al., 2016; Liu et al., 2019; Xia et al., 2019). Therefore, it is important to improve the survival rate and initial feeding success of M. albus juveniles during the stocking stage.

In nature, M. albus is a nocturnal predator that devours fish, worms, crustaceans, and other small aquatic animals (Zhou et al., 2011; Ma et al., 2014). In traditional practices, M. albus is usually fed a commercial formula feed mixed with trash fish or earthworms. However, trash fish can pose serious sanitary risks such as transfer of pathogens or parasites to the eels and water pollution (Morais et al., 2014). Moreover, trash fish have been facing a sharp decline, leading to an unreliable supply and high cost (Tacon and Metian, 2008). Recently, insects have yielded tremendous results as potential replacers of fishmeal in aquafeed, with the black soldier fly (Hermetia illucens) and mealworm (T. molitor) being the most studied and promising insects (Maulu et al., 2022). In aquaculture, many studies have revealed positive results when black soldier fly meal was used as a substitute for fish meal for many species such as whiteleg shrimp (Litopenaeus vannamei) (Richardson et al., 2021) and Nile tilapia (Oreochromis niloticus) (Were et al., 2021). Tenebrio molitor has shown positive results when utilized in the diets of many aquatic species, such as yellow catfish (Pelteobagrus fulvidraco) (Su et al., 2017). Furthermore, T. molitor has a relatively high nutritional value, and it is a rich source of essential amino acids (such as methionine), lipids, and fatty acids that vary depending on the developmental stage of the larvae (Shafique et al., 2021).

The aim of this study was to comprehensively evaluate the effects of four types of bait, namely, trash fish, earthworms, fly maggots, and yellow mealworms (T. molitor), on the survival rate, feeding, antioxidant enzymes activity, body composition, and aquaculture water quality of M. albus juveniles under recirculating aquaculture conditions. The results will provide theoretical support for improving open-mouth domestication technology in the juvenile stage of M. albus and important guidance for recirculating aquaculture of M. albus.

Recently, there has been a widespread increase in research on the applications of insect protein, especially from house flies and yellow mealworms, as a substitute for fish meal in aquaculture. Most of the studies have reported processes by which insects were converted into powder and added to feed, and few studies analyzed the effects of feeding live insect bait to fish (Maulu et al., 2022). M. albus prefers to eat live bait, and studying the effects of different insect larvae on their feeding and growth is of great significance for practical production.

The ANOVA results showed that recirculating aquaculture with four different bait types had significant effects on the survival rate of M. albus. The highest survival rate was found in the YMW group and the lowest in the TF group, presumably because the water quality was suitable or at least in the feasible range to support the maintenance of M. albus. This can be observed from the changes in TAN and NO₂ ⁻-N indicators. TAN and NO₂ ⁻-N are environmental factors that are more likely than other environmental factors such as NO₃ ⁻-N to exert stress on fish (Portalia et al., 2019). In this study, the DO content in the TF and EW groups was significantly lower than that in the FM and YMW groups, and the pH levels were also lower than those in the FM and YMW groups, consistent with the general trend of a positive correlation between DO and pH levels. The pH level primarily fluctuates due to CO₂ dynamics, influenced by factors such as algae photosynthesis, aquatic organisms’ respiration, and the oxidation and decomposition of organic matter, as CO₂ is a byproduct of organic decay. It is widely acknowledged that aquatic plants absorb CO₂ during photosynthesis, leading to a rise in pH levels, the production of oxygen, and an increase in DO concentrations (Yuan et al., 2023). The TN, TP, and NO₃ ⁻-N content in the recirculating aquaculture water remained within normal ranges overall. Between July 4th and 11th, the water temperature rapidly increased from 33°C to 37°C, whereas TAN content fluctuated less in the YMW group and rapidly increased in the other groups, exceeding 1.5 mg/L. This may be because YMW is a live bait, and, even if it was available in surplus, it decomposes slowly in the water, while the other bait types were all frozen. Although TAN content in the YMW group increased significantly in the last week of the experiment, this may be related to the continuous cultivation of high-stock fish, whereas TAN content in the other groups decreased because of more M. albus deaths, resulting in a decrease in feeding volume and TAN content in the last week. The toxicity of ammonia nitrogen to cultured animals is closely related to temperature and pH values. With higher pH and temperature, the proportion of free ammonia (NH₃) increases, leading to a significant increase in toxicity. In this study, the average pH values of the four treatment groups ranged from 7.0 to 7.5, with most of the rearing period experiencing water temperatures exceeding 30°C. Under these conditions, the proportion of free ammonia accounted for approximately 1% of the total ammonia concentration (Zhu et al., 2021). The Asian swamp eel is normally considered an air-breathing fish capable of lowering the toxicity of ammonia in their environment and body via unique strategies of ammonia detoxification (Ip et al., 2004; Chew et al., 2005; Chen et al., 2013); hence, the ammonia nitrogen content in present study should not exert direct stress on the M. albus. In addition, NO₂ ⁻-N content in the YMW group decreased continuously; the significant increase after 1 week of aquaculture may be related to the recirculating water treatment system, as biological filters require some time for membrane formation. However, simultaneous occurrences of elevated concentrations of ammonia nitrogen, high water temperatures, and insufficient DO indicate deteriorating water quality, which can easily lead to infections by opportunistic pathogenic bacteria, ultimately resulting in fish morbidity and mortality (Zaheen et al., 2022). This observation aligns with the phenomena we observed during the experimental process, where dead Asian swamp eels exhibited symptoms of bacterial infections such as external hemorrhaging or anal bleeding.

Another important reason for the high survival rate of M. albus may be the presence of antimicrobial peptide activity in YMW, which in turn enhances the immune system of M. albus. According to Xiang et al. (2019), insect meal contains bioactive peptides that may prevent diseases. Therefore, insect meal presents the potential prevention of intestinal inflammation in aquaculture. Incorporation of YMW in yellow croaker (Larimichthys crocea) diets in which fishmeal was replaced by 426.2–568.3 g/kg (75%–100% fishmeal replacement) led to increased muscle hardness and significantly lower shear force in fillets (Yuan et al., 2022). Replacing fishmeal with YMW in the diets of L. vannamei juveniles improved the survival rates of the shrimp after being challenged with the pathogenic bacterium Vibrio parahaemolyticus (Motte et al., 2019). In P. fulvidraco, 18% dietary YMW improved the immune response and disease resistance of the fish against the bacterium Edwardsiella ictaluri (Su et al., 2017). In juvenile mandarin fish (Siniperca scherzeri), the inclusion of YMW in the diets enhanced the immune system of the fish (Sankian et al., 2018). According to Motte et al. (2019), replacing fishmeal with 50% defatted YMW improved the disease resistance of L. vannamei against early mortality syndrome. In red seabream (Pargus major), feeding the fish with diets containing YMW after challenge with a bacterial pathogen (Edwardsiella tarda) improved survival (Ido et al., 2019). Henry et al. (2018) used YMW to feed the rainbow trout (Oncorhynchus mykiss) for 6 weeks. The fish showed a significant enhancement in anti-inflammatory responses, lysozyme antibacterial activity, and serum trypsin inhibition, which are usually related to anti-parasitic activity. These findings show that insect meal may help to improve disease resistance in fish farming.

No significant differences in SGR of M. albus were detected among the bait groups, but the YMW group had the lowest SGR. Because the YMW group showed the highest survival rate, a decrease in SGR may have been caused by the relatively high-density recirculating aquaculture. This is in accordance with the findings of Yuan et al. (2018), who stated that stocking density will affect the competition for space. Limited space for movement will cause M. albus to become more easily stressed, which will then affect growth. The causes for the slowed growth of fish are a large level of competition between individuals for food, space for movement, oxygen consumption, and the amount of waste material, including carbohydrates, ammonia and nitrite, in the water that can interfere with the fish (Portalia et al., 2019). In addition, growth rate and nutrient quality of M. albus in freshwater aquaculture are influenced by natural feed (Herawati et al., 2018). Different natural feed intakes may also affect the SGR of M. albus, but this needs to be studied further by conducting longer culture experiments.

For M. albus, multiple low-dose feedings were performed, so the feeding amount was closer to the food intake amount. In this study, significant differences in feeding amount were found among the different groups, with the YMW group having the highest feeding amount, followed by the EW group. The EW group had the highest feeding percentage; the YMW group had a higher feeding percentage in the first week, but it decreased with time. This indicates that M. albus prefers to eat yellow mealworms and earthworms more than fly maggots and trash fish. M. albus are responsive to live baits such as aquatic invertebrates, small fish, and crustaceans with nocturnal foraging behavior prevailing (Hill and Watson, 2007). Live baits can elicit a strong feeding response due to their natural movement and scent, making them effective for angling and aquaculture purposes. This indicates that live bait such as yellow mealworms is more conducive to training Asian swamp eels to accept feeding compared to frozen baits.

After 40 days of feeding with different natural bait types, the crude protein and fat contents of the whole body of M. albus significantly increased. The TF group showed the highest rate of increase in crude protein content, followed by the YMW group. This indicates that the utilization efficiency of M. albus for trash fish protein is higher than that for insect protein, but the specific reasons need to be evaluated. At the end of the experiment, the crude protein content of M. albus was higher than that of M. albus cultivated with a formulated diet (Ma et al., 2014; Yue et al., 2021). Ma et al. (2014) found that, after 10 weeks of mixed feed cultivation, the highest crude protein content of M. albus was 16.78%. The moisture content of M. albus in this study was significantly lower than that of M. albus cultured with a formulated diet (more than 70%) (Ma et al., 2014; Yue et al., 2021).

Aerobic metabolism has the potential to generate reactive oxygen species (free radicals), whose elevated levels can induce oxidative damage, leading to oxidative stress (Kakade et al., 2020). SOD, CAT, GSH-Px, T-AOC, and MDA serve as crucial markers of antioxidant activity. SOD and CAT function by scavenging free radicals, mitigating oxidative stress-induced damage to the intestinal mucosa, thereby playing a pivotal role in intestinal defense and repair. GSH-Px reflects the organism’s capability to neutralize free radicals, safeguarding against lipid peroxide-induced harm. T-AOC serves as a comprehensive indicator of antioxidant capacity, illustrating the organism’s ability to counteract external stressors and the status of free radical metabolism. MDA content indicates the extent of lipid peroxidation and indirectly reflects cellular damage severity (Wang et al., 2022). In this study, the MDA content in the liver of the TF group was significantly higher than that of the other bait groups, which implies that insect bait can reduce lipid peroxidation and oxidative stress. Numerous studies have shown that housefly maggots have positive effects on the growth performance of various farmed animals (Yi et al., 2014; Xiang et al., 2019). Among the insect feed groups, liver GSH-Px activities was significantly higher in the EW group than in the YMW group, with no significant differences when compared with the FM group. Many studies have reported the feeding and growth of fish with earthworms (Parolini et al., 2020). Earthworm dry matter (16%–20% of fresh matter) contains from 55% to 70% proteins (Mohanta et al., 2016) and earthworms are easy to cultivate, making them a promising alternative protein in fish farming (Parolini et al., 2020). This study shows that earthworms may be beneficial for enhancing the antioxidant stress capacity of M. albus.

Currently, the unit price of yellow mealworm larvae available in the Chinese market ranges from 12 to 16 RMB/kg, frozen earthworms are priced at 8 to 10 RMB/kg, frozen fly maggots at 4 RMB/kg, and frozen trash fish at 5 to 6 RMB/kg. Yellow mealworms are insects with a fast growth cycle and are easy to rear. They can be raised on balconies or in old buildings, making them a cost-effective option for bait production, with bait costs potentially controlled below 8 RMB/kg through supplementary breeding. Considering the high survival rate of Asian swamp eels trained to accept yellow mealworms as indicated in present study, and with the continuous decrease in natural resources of trash fish (Tacon and Metian, 2008), using yellow mealworms as an alternative bait option demonstrates significant economic feasibility. However, natural insect baits, particularly yellow mealworms, due to their high lipid content, may pose adverse health effects on cultured animals with prolonged and extensive usage. Therefore, further research is needed to develop feeding strategies that not only does it domesticate Asian swamp eels with natural baits for feeding, but also promote their long-term health and growth.

According to the results of this study, aquaculture of M. albus with natural insect bait rather than trash fish has significant advantages in terms of survival rate, water quality. The YMW group exhibited the highest survival rate during recirculating aquaculture, relatively good water quality. Therefore, T. molitor could potentially serve as one of the alternative feeds during the initial stages of M. albus juveniles stocking. The second-best natural bait is earthworms, which has significant advantages with respect to feeding rate and antioxidant enzyme activity of M. albus.