Natural Biota’s Contribution to Cultured Aquatic Animals’ Growth in Aquaculture Cannot Be Ignored

Jin, Shiyu; Kong, Qingling; John, Chibuike Kemdi; Wang, Zhaoyu; Zhang, Tanglin; Li, Xiangqian; Zhu, Xiaoyan; Li, Jing; Luo, Yan; Qian, Mengyu; Chen, Feifei; Kong, Xiaolong; Gu, Dangen; Luo, Si

doi:https://doi.org/10.1155/2023/2646607

Aquaculture Research

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Review Article | Open Access

Volume 2023 | Article ID 2646607 | https://doi.org/10.1155/2023/2646607

Natural Biota’s Contribution to Cultured Aquatic Animals’ Growth in Aquaculture Cannot Be Ignored

Shiyu Jin,¹Qingling Kong,¹Chibuike Kemdi John,¹Zhaoyu Wang,¹Tanglin Zhang,²Xiangqian Li,¹Xiaoyan Zhu,¹Jing Li,¹Yan Luo,¹Mengyu Qian,¹Feifei Chen,¹and Xiaolong Kong¹ et al.

Academic Editor: Daniel L. Merrifield

Received02 Sept 2022

Revised05 Dec 2022

Accepted24 Dec 2022

Published02 Feb 2023

Abstract

The rapid expansion of the aquaculture industry is accompanied by high organic and nutrient loadings from formulated feeds. This leads to water deterioration and pathogenic microorganisms. Natural biota (e.g., bacteria, phytoplankton, zooplankton, and zoobenthos) in ponds form important parts of cultured aquatic animals’ diets. They contain essential proteins, lipids, carbohydrates, amino acids, and fatty acids and are considered promising supplementary nutrition sources for cultured aquatic animals. Particularly, they are available to aquatic animals throughout the day, and an adequate supply of them as starter foods during the larvae stage ensures high survival. Since formulated feeds constitute more than 50% of aquaculture production costs, optimizing the utilization of natural biota and reducing dietary nutrient input without compromising animals’ growth should be a priority to improve the economic success and sustainability of aquaculture. From this scenario, the present review offers an updated view of the natural biota category in aquaculture systems, their nutritional components, and their contributions to the growth of cultured aquatic animals. Taken together, this review emphasizes the significant roles of natural biota playing in the growth of aquatic animals and encourages maximizing utilization of natural biota to improve feed conversion efficiency and aquaculture sustainability.

1. Introduction

Aquaculture supplies more than two-thirds of fishery products consumed worldwide, contributing significantly to global food security and poverty alleviation [1]. Nevertheless, the industry faces numerous challenges regarding its sustainability, especially for nutrient pollution originating from the overuse of feeds, leading to high amounts of organic and nutrient loadings in water environments [2, 3]. The situation is particularly true for semi-intensive or intensive aquaculture production, which mainly depends on high-cost dietary inputs via “formulated artificial diets” [4–6]. The nutrient loadings result in water deterioration, which in turn causes the thriving of pathogenic microorganisms and eventually the death of cultured aquatic animals [7]. This causes more than $9.5 billion economical loss per year in aquaculture [8]. It is, therefore, of supreme importance for aquaculture management to be optimized by improving feeding strategies for aquaculture suitability [7].

Natural biota, composed of internally correlated ecological communities of biological species, are the foundation of the food chains in ecosystems and important natural food items for aquaculture targets. At the broadest level, the natural biota in the aquatic system underlies adaptive diversification of species belonging to bacteria, phytoplankton, periphyton (algae attached to stream substrates), macrophytes (visible plants that are either rooted in the substrate in the case of emergent and floating-leaved macrophytes, floating beneath the surface in the case of submerged macrophytes, or floating on the surface in the case of free-floating macrophytes), zooplankton (suspended in the water column), and zoobenthos (inhabit around the stream bed) [9]. In aquaculture ponds, the production process is based on the conversion of solar energy into chemical energy stored in glucose during photosynthesis by phytoplankton (Chrysophyceae, Cyanophyta, Bacillariophyceae (diatoms), Euglenophyceae, and Chlorophyceae (green algae)), algae, and other submerged plants, which constitute essential nutritional sources for aquatic life. Zooplankton (Protozoa, Rotifera, Copepoda, Cladocera, and Ostracoda), zoobenthos (Chironomidae, Oligochaeta, Ceratoponogonidae, and Mollusca), fish, shrimp, crayfish, and crabs dominate the consumption process, and they derive nutrition from autochthonous and added organic matters (e.g., formulated feeds) [10]. In the decomposition process, microorganisms such as bacteria (Escherichia, Thermotoga, Cyanobacteria, Streptomyces, Methanobacterium, Rhodospirillum, Nitrobacter, and Azotobacter) play significant roles in the decomposition of organic detritus and the recycling of essential nutrients, acting as a sink for carbon [11]. The decomposed detritus and inorganic nutrients are consumed by cultured aquatic animals, which finally build blocks for biomass. These natural biota (rich in proteins, lipids, amino acids, fatty acids, vitamins, trace elements, and bioactive compounds) improve the growth and nutritional values of numerous cultured aquatic animals (herbivorous/omnivorous species) [7, 12–23]. They can also replicate some of their effects with nonliving cells or components of the cell wall, particularly those involving the digestive and metabolic processes, intestinal balance, and immune system [20]. Their accessibility, palatability, reproducibility, and better nutritional levels make them valuable foods, especially for larvae. Supplying adequate natural biota during population recruitment of fish, shellfish, crayfish, shrimp, and crabs ensures maximum aquaculture production and profitability [12, 17, 24–27]. Furthermore, the utilization of these natural biota in aquaculture is cost-effective, which can hopefully reduce formulated feed inputs and increase the productivity and efficiency of aquaculture production systems [10, 28].

It is, therefore, possible to improve feeding strategies that maximize the utilization of natural biota as an alternative way to reduce formulated feed input for sustainable and environmentally friendly aquaculture. A comprehensive understanding of the categories of natural biota in aquaculture ponds, their nutritional components, and their contributions to the growth of cultured aquatic animals’ is a top priority. This review detailed the category, discussed their general properties as promising candidates for aquatic animals’ foods, discussed their contributions to animals’ growth, and highlighted the benefits of utilizing them in aquaculture.

2. Natural Biota Category in the Aquaculture System

In freshwater aquaculture systems, natural biota are normally classified into autotrophs, heterotrophs, and detritus. Autotrophic natural biota include phytoplankton (algae, Chrysophyceae, Cyanophyta, Bacillariophyceae, Euglenophyceae, and Chlorophyceae), periphyton (attached algae), and aquatic macrophytes (very low biomass) [10, 29]. Heterotrophic natural biota comprised bacteria, zooplankton (Protozoa, Rotifera, Copepoda, Cladocera, and Ostracoda), and zoobenthos (Chironomidae, Oligochaeta, Ceratoponogonidae, and Mollusca). Detritus is characterized by organic particles from dead organisms. They interact and contribute to the formation and stability of ecosystems.

2.1. Phytoplankton

Phytoplankton is capable of oxygenic photosynthesis and normally contains chlorophyll a. They convert solar energy into chemical energy, which forms the base of food webs in aquatic ecosystems. In freshwater aquaculture ponds, Chrysophyceae, Cyanophyta, Bacillariophyceae (diatoms), Euglenophyceae, and Chlorophyceae (green algae) mainly constitute phytoplankton [29], with over 20 genera found (summarized in Table 1). The biomass of phytoplankton was highly variable among aquaculture ponds. For example, their biomass ranged between 7.85 × 10⁵–10.24 × 10⁵ cells/L, 29.39 × 10⁵–32.90 × 10⁵ cells/L, and 15.8 × 10⁵–21.10 × 10⁵ cells/L for pond bottom with sandy loam, loam, and clay loam [35]. The biomass was higher in the fish culture ponds (Subarno Agro-Based Initiative and Bismillah Agro Production), which was 36 × 10⁵–94.92 × 10⁵ cells/L, with Euglena sp., Microcystis sp., and Eurolena sp. dominant [37]. The high phytoplankton biomass was also observed in crayfish Cherax cainii culture ponds, which ranged from 500,000 to 14500,000 cells/L [38]. Normally, the highest phytoplankton biomass occurred in spring, followed by early autumn and summer, with the lowest abundance in winter [30]. In spring, Chlorophyceae (green algae) had the highest abundance and constituted 49%–76.6% of the total observed phytoplankton population, followed by Bacillariophyceae (diatoms, 18.9%–40.4%) [39]. In early autumn, Cyanophyceae dominated in aquaculture ponds (main genera: Microcystis, Anabaena, and Planktolymbya), while Chlorophyceae (Chlorella vulgaris, Pediastrum sp., and Scenedesmus denticulatus) were dominant in rainy seasons, and Bacillariophyceae (Navicula angusta and Cyclotella meneghiniana) were dominant in winter [30]. Overall, the biomass of Bacillariophyta, Chlorophyta, Cyanobacteria, Euglenophyta, and Pyrrophyta was 0.07–25.1 × 10⁶ ind./L, 1.63–73.2 ind./L, 6.78–54.9 × 10⁶ ind./L, 1.53–11.8 × 10⁶ ind./L, and 0.09–0.72 × 10⁶ ind./L across seasons, with the relative contributions of 12.5%, 22.5%, 12.5%, 10%, and 2.5%, respectively [33, 40].

Chrysophyceae, the golden algae, produce siliceous cysts called stomatocysts or statospores and get energy and nutrients by photosynthesis and/or heterotrophy (ingesting bacteria or complex organic molecules) [41]. Species Hydrurus foetidus, the genera Mallomonas, and Synura are widely distributed and are considered a valuable food source for cultured aquatic animals [31, 32, 36]. Furthermore, Dinobryon sp. and Synura sp. are also common species belonging to Chrysophyceae in aquaculture ponds.

Cyanophyceae, Gram-negative oxygenic photosynthetic prokaryotes, are ideal candidates for food supplements in aquaculture, and they also have huge potential as biofertilizers and have been applied in wastewater treatment because of their ability to produce exopolysaccharides and flocculants [42]. In ponds, Anabaena sp., Aphanocapsa sp., Arthrospira sp., Chroococcus sp., Coelosphaerium sp., Cylindrospermopsis sp., Gomphosphaeria sp., Lyngbya sp., Merismopedia sp., Microcystis sp., Nostoc sp., Oscillatoria sp., Phormidium sp., and Spirulina sp. are commonly dominate and serve as foods for numerous fish species [34].

Bacillariophyceae, the diatoms, play significant roles in the primary production of ecosystems and purifying water. They are rich in sterols, polyunsaturated fatty acids, calcium, magnesium, iron, and vitamins and are considered important natural foods for aquatic animals [34, 43]. Normally, in aquaculture ponds, Synedra sp. is dominant, with other genera such as Achnanthidium, Amphipleura, Aulacoseira, Craticula, Cyclotella, Cymbella, Diatoms, Epithemia, Eunotia, Melosira, Navicula, Nitzschia, Pinnularia, Pleurosigma, and Synedra also being frequently observed.

The dinoflagellates have normally high biomass (1,200–61,140 cells/L) and are widely used as feed additives for cultured aquatic animals. In aquaculture ponds, there are primary producers, predators, preys, and symbiotic partners. Particularly, several species such as Heterocapsa rotundata, Ansanella granifera, Alexandrium sp., Takayama sp., and Gymnodinium smaydae dominate, with biomass of 49.37–77.24 μg·C·l⁻¹, 2.16 × 10⁸ cells/L, 1000–1200 cells/L, and 18500 cells/L, respectively [44–49].

For Euglenophyceae (unicellular flagellates), they normally dominate in late autumn, and the most frequently occurring taxa were Euglena sp. and Phacus sp. [30, 34]. They play crucial roles in larvae surviving through the winter. The properties of efficient nutrient uptake and high biomass productivity make them a suitable source of lipids [50].

Chlorophyceae, single-celled or multicellular assemblages, are a large group of freshwater algae, which habitats from damp soil, and wetlands to the benthic zones of ponds. The common Chlorophyceae in aquaculture ponds include Botryococcus sp., Chaetophora sp., Chlamydomonas sp., Chlorella sp., Chlorococcum sp., Dictyosphaerium sp., Scenedesmus sp., Pediastrum sp., Ankistrodesmus sp., Closterium sp., Coelastrum sp., Cosmarium sp., Spirogyra sp., Zygnema sp., and Ulothrix sp. [29, 34]. They mainly serve in six parts: (1) nutritional supplement [51]; (2) wastewater treatment by removed nitrogen, phosphorus, chemical oxygen demand, and improving water quality [50, 52–55]; (3) disease control [56]; (4) developing and producing of biodiesel and/or bioethanol biodiesel) [57, 58]; (5) bioremoval of metals [59]; and (6) enhancing animals’ health and resistance to the adverse environment [60].

2.2. Bacteria

Bacteria (mostly 1-2 μm in diameter) are unicellular, autotrophic, or mixotrophic, regulating the cycle of nutrients and energy flows in aquatic ecosystems. The biomass of bacteria in aquaculture systems can be up to 10¹⁰ cells·m/L, ranging from 0.5 × 10³ cells·mL⁻¹ to 1.2 × 10¹⁰ mL⁻¹ across seasons [61, 62], which is almost similar to phytoplankton biomass [63]. They play significant roles in aquatic animals’ gut microbiota, which mediate the absorption and utilization of nutrients, physiological and immune activities, etc. The common bacteria found in aquaculture systems are (1) Escherichia and Thermotoga (intestinal microorganisms, improving digestive and immune process and protecting cultured aquatic animals from other harmful microbes); (2) Cyanobacteria (photosynthetic and fixing nitrogen, major contributors to carbon and nitrogen fluxes of aquaculture systems); (3) Streptomyces (producing bioactive secondary metabolites, such as antifungals, antivirals, immunosuppressants, and especially antibiotics, and improving metabolic and immune functions of animals); (4) Methanobacterium (generating methane as a metabolic by-product, and converting organic wastes into clean energy by reducing chemical and biological oxygen demand in the wastes); (5) Rhodospirillum (using sulfide as the electron donor for photosynthesis); (6) Nitrobacter (oxidizing nitrite into nitrate); and (7) Azotobacter (aerobic nitrogen fixation) [29, 64].

2.3. Zooplankton

Zooplankton, which transfer organic matter from phytoplankton and detritus to higher trophic levels, constitute the major part of cultured aquatic animals’ nutrition and have significant implications for the recycling of nutrients and flow of energy in ecosystems [65]. Zooplankton in the aquaculture ponds mainly include Rotifera, Copepoda, and Cladocera, with more than 20 genera or species frequently observed (Table 2). Among them, rotifers (Brachionus sp. and Keratella sp.) are the most frequently observed, followed by cladocerans (Chydorus sp. and Daphnia galeata) and copepods (Mesocyclops australiensis) [66]. They are the most important food items in aquaculture ponds [67], which are crucial to larvae survival.

Rotifers are major foods for many cultured aquatic animals, especially juveniles and larvae [68]. Normally, Asplanchna sp., Brachionus sp., Euchlanis sp., Filinia sp., Keratella sp., Lecane sp., Monostyla sp., Notholca sp., Polyarthra sp., and Rotaria sp. are highly abundant in aquaculture ponds, which provide essential nutrition for aquatic animals’ growth [34]. Although numerous research studies have focused on alternatives (e.g., improving the formulation of microdiets) [69–71] to rotifers as natural foods for cultured aquatic animals, a perfect substitute is still not found. In hatcheries of many cultured species, rotifers are suitable starter feed due to their smaller sizes (50–110 μm), constant availability, easy digestibility, and high reproductive rates, which are particularly essential for larval growth and development [26]. Brachionus sp. are frequently observed in aquaculture ponds, and the freshwater species Brachionus rotundiformis is recognized as an excellent live feed in aquaculture industries and has been widely cultured through different nutrition-enriched technologies.

Copepoda, especially their nauplii, are valuable foods for commercially important species such as P. clarkii. Some Copepoda genera (Acanthocyclops sp., Aglaodiaptomus sp., Cyclops sp., Diacyclops sp., and Leptodiaptomus sp.) are commonly found in aquaculture ponds [34]. Several Copepoda species such as Paracyclops fimbriatus and Apocyclops royi are even successfully cultured on a large scale to supply foods for cultured aquatic animals [67]. Copepods are generally considered superior to rotifers and Artemia for larval fish culture due to their high dietary profiles. Farmers normally develop its mass culture technology by adding concentrates of filtered culture to nutrient-rich water to enhance its growth during different stages such as eggs, nauplii, subadults, and adults in semiextensive ponds [26]. Cladocera such as Daphnia sp. and Moina sp., widely distributed in various water environments, are ideal live feeds in fish or crayfish larval developmental processes because of their small sizes, high nutritional values, and abundant energy storage [34, 65].

In most ponds, seasonal variations of Rotifera (from 5243 Ind/m³ in winter to 9196 Ind/m³ in summer), Copepoda (from 4685 Ind/m³ in winter to 5601 Ind/m³ in autumn), and Cladocera (from 3863 Ind/m³ in winter to 5980 Ind/m³ in autumn) were observed, with the total zooplankton biomass ranging from 73085 Ind/m³ in winter to 110900 Ind/m³ in summer [72]. The biomass of Rotifera, Copepoda, and Cladocera also ranged between 22.7 × 10³–26.5 × 10³ cells/L, 74.4 × 10³–93.8 × 10³ cells/L, and 55.9 × 10³–76 × 10³ cells/L for different ponds (bottom with sandy loam, loam, and clay loam) [35]. Different strategies of fertilization (simple fertilization, organic substrates, and fertilization) and the water environment also significantly influenced their biomass. For example, the concentration of zooplankton (copepods, polychaetes, protozoans, barnacles, gastropods, ciliatea, hydrozoans, and others) ranged from 124 org/L to 309 org/L, where the copepods (83%) were the most abundant organisms in ponds with organic substrates and fertilization, followed by polychaetes (5%), barnacles (5%), protozoans (3%), ciliate (2%), gastropods (1%), and others (1%) [73]. In the ponds supplied with surface water/groundwater, the biomass of Rotatoria, Cladocera, and Copepoda across the seasons was 14.1–10466 ind./L, 1.7–691 ind./L, and 369–889 ind./L, respectively [40]. Furthermore, Rotifera and Cladocera sharply declined in biomass and abundance (66% of species disappeared) when the ponds changed from surface water to groundwater [40].

2.4. Zoobenthos

Zoobenthos normally include Chironomidae (Chironomus sp. and Pentaneura sp.), Oligochaeta (Branchiura sowerbyi, Peloscolex ferox, and Aeolosoma sp.,), Ceratopogonidae (Culiciodes sp. and Amphizoa sp.), and Mollusca (Viviparous bengalensis) (see Table 3 for detailed information). The biomass of Chironomidae, Mollusca, Oligochaeta, and Ceratopogonidae in ecosystems was 107–376 ind./m², 10–85 ind./m², 178–1200 ind./m², and 44–399 ind./m² [40, 79]. In the settlement pond, maximum biomass of Chironomidae and Mollusca (Cerithidea cingulata, Cerithium coralium, Thiara riqueti, and Stenothyra spp.) exceeded 491 ind. × 0.02 m⁻² and 10,000 ind./m² [75, 77]. It has been reported that Branchiura sowerbyi (21–47 ind./m²) [80], Peloscolex ferox (14–36 ind./m²), Aeolosoma sp. (10–27 ind./m²), Tubifex tubifex (41–82 ind./m²), Chironomus sp. (48–102 ind./m²), Pentaneura sp. (27–62 ind./m²), and Viviparous bengalensis (51–72 ind./m²) are frequently observed and used as live foods for fish, crayfish, crabs, and others [81].

The diversity of zoobenthos varies among different ponds. For example, in grass carp culture ponds, the benthic community mainly consisted of Mollusca (Planorbis sp., Lymnaea sp., and Napaeus sp.) and Chironomidae [78]. In the Hediste diversicolor enrichment ponds, Mollusca (Akera bullata, Jujubinus striatus, Hydrobia ulvae, and Rissoidae) greatly increased their abundances, while in the traditional ponds, Hydrobia ulvae and Abra ovata were generally dominated [74]. Drake and Arias [76] pointed out that in the semienclosed polyculture lagoons and monoculture ponds, the abundant benthic species were Oligochaetes (1.3–18.5 ind./225 cm²), Abra ovata (0.8–68.9 ind./225 cm²), Cerastoderma glaucum (0.3–12.7 ind./225 cm²), Hydrobia minoricensis (0.4–559.2 ind./225 cm²), Hydrobia ulvae (0.1–6.7 ind./225 cm²), Hydrobia ventrosa (0.1–92.1 ind./225 cm²), and Chironomus salinarius (1.3–151.1 ind./225 cm²). These benthic species benefit numerous fish species (Sparus aurata, Oncorhynchus gorbuscha, Salmo salar, Tilapia, Cobitis taenia, Perca fluviatilis L., Pelteobagrus fulvidraco, and Leuciscus cephalus orientalis), shrimp (Crangon crangon and Litopenaeus vannamei), crayfish (Austropotamobius torrentium, Orconectes limosus, and Pontastacus leptodactylus), and crab (Eriocheir sinensis) [82–85].

3. General Properties of Natural Biota as Promising Candidates for Aquatic Animal Foods

Natural biota contain essential proteins, lipids, carbohydrates, vitamins, amino acids, fatty acids, sterols, organic minerals, enzymes, carotenoids, chlorophyll, and trace elements, which are directly available for larvae and adults [86].

3.1. Phytoplankton

Phytoplankton, which contain valuable phytonutrients and bioactive compounds (1909.1 mg/l of protein, 55.4 mg/L of carbohydrates, and 6.5 mg/L of lipid, and 0.064–0.234 ng/10⁶ cells of retinoid-like activity of metabolites), have significant implications for hatcheries and larval development [87, 88]. The contents ((%) of total fatty acid) of main fatty acid from the classes Cyanophyceae, Chlorophyceae, Chlorodendrophyceae, Pyramimonadophyceae, Mamiellophiceae, Trebouxiophyceae, Porphyridophyceae, Cryptophyceae, Coccolithophyceae, Pavlovophyceae, Eustigmatophyceae, Raphidophyceae, Pelagophyceae, Dinophyceae, and the phylum Bacillariophyta are shown in Table 4. The fatty acids are present in different proportions in various classes, with the highest contents of 14:0, 16:0, 16:1n-7, 18:1n-9, 18:2n-6, 18:3n-3, and 18:4n-3 observed in Coccolithophyceae, Porphyridophyceae, Bacillariophyta, Chlorodendrophyceae, Trebouxiophyceae, Chlorophyceae, and Cryptophyceae. This ensures aquatic animals’ optimal growth, development, and reproduction, which also improves their chemical composition, especially the fatty acid composition [89]. According to Suh et al. [90], Bacillariophyceae had the highest PUFA contents but similar C14:0, C16:0, C18:0, C20:5n-3, and C22:6n-3 contents as Dinophyceae. For Chlorophyceae, major fatty acids were 16:0, 16:1 (n-13) t, 16:2 (n-6), 16:3 (n-3), 18:2 (n-6), and 18:3 (n-3) [91]. Most phytoplankton species contain 7%–34% of eicosapentaenoic acid (EPA) and high docosahexaenoic acid (DHA, 0.2%–11%, in cryptomonads and prymnesiophytes such as Pavlova spp. and Isochrysis sp.), with the mean ratio of n-3 and n-6 in freshwater phytoplankton being 1.0–16.8 [86]. Eustigmatophytes (e.g., Nannochloropsis spp.) and diatoms often have the highest percentages of arachidonic acid (AA, up to 4%) [92]. As the important components of phytoplankton, they are the main live feed for cultured aquatic animals, providing various phytonutrients such as PUFA, saturated fatty acids (SAFA), monounsaturated fatty acids (MUFA), AA, DHA, and EPA, which are of great importance for animals’ growth and development. Especially for the diatom Cyclotella cryptica from Bacillariophyceae, the total fatty acids and unsaturated fatty acids were 40.2–74 mg/g and 42–64.4%, with the most abundant fatty acids being palmitic acid (16:0), palmitoleic acid (16:1 n-7), stearidonic acid (18:4 n-3, SDA), EPA, and DHA [93, 94].

Besides the fatty acids, diatoms also contained recommendable contents of protein (17.81%–51.86%), carbohydrate (3.72%–17.23%), carotenoids (0.23%–0.28%), monosaccharides (1.58%–3.57%), and polysaccharides (2.25%–13.75%), with the contents of 7.29–16.91 pg/cell and 4.37–9.24 pg/cell for EPA and DHA [95–97]. Although limited studies have focused on the amino acid profiles, there is some evidence suggesting phytoplankton have excellent amino acid profiles, which makes them nutritionally cost-effective food sources for cultured aquatic animals. For instance, Ahlgren and Hyenstrand [98] and Ahlgren et al. [99] stated that green alga Scenedesmus quadricauda (Chlorophyceae), the commonly used live foods in aquaculture, contained all amino acids (306–392 mg/g) necessary for aquatic animals’ growth, which were 9.6%–10.3% aspartic acid, 4.9%–5.1% threonine, 4.6%–4.7% serine, 11.8%–13.4% glutamic acid, 4.5%–5.9% proline, 5.6%–5.9% glycine, 7.1%–7.7% alanine, 1.5%–2.7% half-cystine, 5.6%–6.0% valine, 2.2%–2.3% methionine, 3.9%–4.3% isoleucine, 7.9%–8.8% leucine, 3.8%–4.3% tyrosine, 4.9%–5.7% phenylalanine, 2.1%–2.3% histidine, 7.5%–7.8% lysine, and 5.9%–10.1% arginine. These attractive nutritional characteristics indicate that phytoplankton are high-quality foods for aquatic animals.

3.2. Bacteria

The potential of bacteria in providing nutrients for aquatic animals has been demonstrated by numerous studies. For instance, beneficial bacteria are recognized as promising candidates for aquaculture feed (dosed typically at 10⁶ to 10¹⁰ cell·g⁻¹ of feed) by Newaj-Fyzul and Austin [100] and Wang et al. [27], which provide micronutrients such as fatty acids and amino acids for Trachinotus carolinus, Oncorhynchus mykiss, Salmo salar, L. vannamei, Paralichthys olivaceus, A. japonicus, and Ctenopharyngodon idellus. Brown et al. [101] reported that the protein was a major constituent (25%–49% of their dry weight) of the bacteria (Aeromonas sp., Derxia sp., and Methylophilus methylotrophus NCIB 10515, Pseudomonas testosterone ACM 4768, Pseudomonas testosterone ACM 4768, Pseudomonas sp. ACM 4770). The contents of lipid, carbohydrate, nucleic acids, and ash were 2.5%–9%, 2.5%–11%, 8%–12%, and 3%–7% of their dry weight [101, 102], respectively. Besides containing 60%–82% protein on their dry matter basis, the bacteria (Brevibacterium, Methylophilus methylotrophus, Bacillus megaterium, Acinetobacter calcoaceticus, Achromobacter delvaevate, Aeromonas hydrophilla, Cellulomonas spp. B. subtilis, Methylomonas methylotrophus, Thermomonospora fusca, Lactobacillus spp. Rhodopseudomonas capsulate, Flavobacterium species, and Pseudomonas fluorescens) also consist of carbohydrates (2.5%–11% of bacterial dry weight), nucleic acids (15–18 fg·C·cell⁻¹), lipid (2.5%–9% of dry weight), minerals (Zn: 20.41–32.21 μg/g, Fe: 70.22–117.2 μg/g, Cu: 1.13–2.43 μg/g, Mn: 1.50–2.64 μg/g, Mg: 4.60–6.60 μg/g, Ca: 9.10–12.7 μg/g), and vitamins (e.g. 1.4 ng/g B₁₂), especially for rich essential amino acids (e.g. 7.72% lysine, 2.38% methionine). They (yeast, all lactic acid bacteria, Enterococcus sp., Lactobacillus sp., Bacillus sp., Vibrio harveyi, Vagococcus fluvialis, Brevibacillus brevis, and Saccharomyces cerevisiae) also contain trace antimicrobial peptides, acting as natural antioxidants and enhancing the immune systems of aquatic animals such as Macrobrachium rosenbergii and Penaeus monodon [103]. These ingredients are not sufficient in animal feed resources [62, 104]. As live microbial feed supplements, they help modify the gastrointestinal microbiota communities and encourage the immune responses of numerous cultured aquatic animals [105]. Furthermore, the significant roles of natural biota in stimulating digestive enzyme activities have been proven in cultured organisms such as blue shrimp, Litopenaeus stylirostris [106], and it also enhances the efficiency of feed utilization [107]. There is a strong indication from Salger et al. [107] that natural biota in the ponds help reduce feeding frequency (feeding Nile tilapia on formulated feed alternate days weekly), which finally enhances feed efficiency by 76% and has no deleterious effects on the growth and survival of tilapia. The excellent characteristics make beneficial bacteria promising alternatives to protein sources for feeds [27].

Recently, more and more studies have explored the possibility of partially or fully replacing fish meal with bacteria. For example, in the culture of black tiger shrimp Penaeus monodon, the potential for microbial bioactive to complete replacement of fishmeal and fish oil has been proved [108], with the additional benefits in growth improvement [109]. Delamare-Deboutteville et al. [110] demonstrated that the replacement of fishmeal with purple phototrophic bacteria (at 33% and 66% replacement levels) did not significantly affect the palatability of the diet, survival, or growth performance of Asian sea bass (Lates calcarifer). Simon et al. [22] found that tilapia fed Novacq™ (microbial biomass) at 10% replacement of fish meal in diets had significantly higher net weight gain (15.5% increase) and feed intake (33% increase). A similar finding was observed in Pacific white shrimp, Litopenaeus vannamei, in which 15%, 30%, and 45% of fish meal was replaced with bacterial protein meal (Methylococcus capsulatus), resulting in no significant differences in growth performance, mortality, or feed utilization of L. vannamei [111, 112].

In addition to basic nutrients provided by bacteria, they (Vibrio sp., Bacillus sp., and Thalassobacter utilis) also produce various kinds of enzymes such as amylase, protease, cellulase, and lipase (improving the digestion and metabolism of cultured aquatic animals and enhancing their ability of stress resistance and health) and secondary metabolites [111, 113, 114]. For example, as a probiotic bacterium, B. subtilis increases the digestion and assimilation of nutrients by aquatic animals and secretes antimicrobial compounds, preventing pathogens’ development and improving the water environment [115, 116]. Flexibacter strain Inp3, which contains high polyunsaturated fatty acid (PUFA) content, not only serves as a food source for Artemia but also assists in the digestion of algae by Artemia [117, 118]. Some enzyme-producing bacteria have positive effects on improving feed efficiency, such as amylase-producing bacteria (Aeromonas hydrophila, Clostridium spp., Pseudomonas spp., Flavobacterium spp., Citrobacter sp., Enterobacter sp., Bacillus sp., and Brochothrix sp.), protease-producing bacteria (Enterobacter spp., Acinetobacter spp., and Bacillus cereus), cellulase-producing bacteria (Bacillus circulans, Bacillus licheniformis, Bacillus coagulans, Bacillus cereus, Enterobacter sp., Aeromonas sp., and Citrobacter sp. and Brochothrix sp.), and lipase-producing bacteria (Aeromonas hydrophila, Vibrio spp., Acinetobacter spp. Enterobacteriaceae, Pseudomonas spp., Bacillus sp., and Brochothrix sp.) [119]. The high nutritional values together with the probiotic effects make the bacteria suitable live foods for cultured aquatic animals.

3.3. Zooplankton

Zooplankton organisms constitute a major part of fish and crustaceans’ larval nutrition intake, especially during the periods of hatcheries and rearing [65]. Understanding their biochemical composition will hopefully provide the scientific foundation for the development of formulated feeds, which are crucial to sustainable aquaculture [120]. Several days after hatching, the main zooplanktons consumed by fish and crustaceans’ larvae are rotifers or copepod nauplii, and then they shifted to larger zooplanktonic organisms such as copepods and cladocerans [121, 122]. These zooplankton organisms have more desirable dietary nutritional characteristics as larval diets (e.g., higher protein, amino acids, saturated fatty acids, and unsaturated fatty acids [123]). In general, most zooplankton species contain a reliable protein source, which ranges over 1.9%–54.2% for protein, 79.2%–98.1% for moisture, 0.4%–11.2% for carbohydrate, 0.1%–27.9% for lipid, and 3.9%–76.4% for ash [124]. A study from Mitra et al. [125] even found that the protein could reach more than 70% (73%–79%) in zooplankton, with a high proportion of SAFA (64%–81%) as well as MUFA (10.79%–14.55%) and PUFA (3%–4.79%). Furthermore, the zooplankton also contains vitamins (e.g. vitamin A 13.61–63.95 μg/g, vitamin E 218–348 μg/g, on a dry matter basis), exogenous enzymes (protease 6.21–7.92 μg leucine/mg protein/h, lipase 25.82–39.1 μg α-naphthol/mg protein/h, and amylase 100–226.1 μg maltose/mg protein/h), minerals and trace elements such as P, Ca, Fe, Cu, Zn, and Mn, which play fundamental roles in larval development. However, these nutritional contents are highly variable among different classes. The fatty acid profile and proximate composition (protein, lipid, carbohydrate, ash, water, and fibre) and energy of zooplankton were summarized in Tables 5 and 6. For example, rotifers tend to have lower lipid contents (9.25%–11.78%) and slightly more than 50% of protein contents (52.23%–55.65%), with preferable fatty acid contents (2.9%–5.83% for EPA, 2.10%–4.52% for DHA, 23.03%–23.42% for n-3 PUFA, 12.88%–15.08% for n-6 PUFA, 8.22%–13.44% for n-3 HUFA, and 1.88%–2.47% for HUFA, Table 5). The copepods contain high protein contents (28.9%–84.9% of dry weight), lipid contents (3%–76% with the mean of 32.37% of dry weight), low carbohydrate contents (0.4%–6.1% of dry weight), and ash contents (10.3%–10.5% of dry weight), with a mean energy of 29.8 KJ/g of dry weight (Table 6). Compared to Calanoida copepod (DHA: 17.6%–20.1%, n-3 : n-6 ratio: 4.2%–5.2%) and Cyclopoid copepods (DHA: 14.8%–20.2%, n-3 : n-6 ratio: 4.7%–18.1%), cladocerans (e.g. Moina sp. and Daphnia sp.) are notable for containing higher SAFA (34.1%–34.6%), MUFA (18.7%–23.5%), ARA (5.2%–8.9%), and EPA (14.7%–22.1%) contents [130, 134]. Among cladocerans, Moina sp. has higher protein contents (59.95%–66.33%) but slightly lower carbohydrate contents (19.83%) than Daphnia sp. (39.24% and 21.87%) [24, 65, 130, 135]. Moina sp. also contains higher levels of most essential fatty acid components such as C14:0 (4.25%), C16:0 (10.53%), C16:1 (21.67%), and C18:1 (9.1%) [24].

The amino acid profiles of mixed zooplankton, rotifers, copepods, and cladocerans are shown in Table 7. In general, the rotifers (unenriched or enriched with multigrain, chlorella, Ori-green, or protein hydrolysate) contain higher contents of Alanine, Glycine, Valine, Aspartic acid, Glutamic acid, Proline, while Copepods have high contents of leucine, isoleucine, serine, methionine, phenylalanine, tyrosine, cystine, and Cladocerans contain higher contents of lysine, histidine, and arginine. Concerning the nutritional-richness in proteins, lipids, carbohydrates, fatty acids, and amino acids, there is no doubt that zooplankton are efficient, feasible, and economical live foods for cultured aquatic animals. More studies are encouraged to evaluate the effects of replacing fish meal with zooplankton on the growth performance, protein efficiency ratio, and feed conversion ratio of cultured aquatic animals such as European sea bass Dicentrarchus labrax [136].

3.4. Zoobenthos

Zoobenthos have a similar nutritional composition as zooplankton and are preferred by numerous larvae in their hatcheries and nurseries. The freshwater zoobenthos consist mostly of insect larvae, among which chironomids are common groups, and their nutritional attributes are comparable to those of fish meal. Chironomid larvae contain 49.56%–51.15% protein, 12.04%–14.22% lipid, 13.25%–14.24% ash, and 6.36%–6.66% moisture [137]. They also have satisfactory amino acids (5.45%–10.92% of methionine, 8.61%–9.44% of glutamic acid, 7.18%–7.96% of aspartic acid, 6.96%–8.25% of glycine, 4.09%–5.92% of serine, 4.67%–8.92% of alanine, and 4.66%–6.68% of cystine) and fatty acids contents (e.g. 10.68%–12.69% of C16:0, 12.52%–19.09% of C18:2n-6, 6.82%–18.04% of C18:1n-9, and 7.12%–9.25% of C18:3n-3) [137]. As a member of the chironomids, Chironomus plumosus has even higher protein content (57.53%) [138, 139] and contains recommendable essential amino acids and fatty acids for feeding most omnivorous and carnivorous freshwater fishery species, with 26.12% SAFA, 30.42% MUFA, and 34.03% of PUFA [138].

The red earthworm, Eisenia fetida, is one of the chironomid families used as feasible starter feeds for fish or crustacean larvae. It contains adequate levels of fatty acids such as 51.08%–53.04% of PUFA, 25.95%–26.90% of MUFA, and 21.16%–22% of SAFA, with the DHA content up to 15.81%–18.31% by enrichment with the bed-free technique [140]. The suitability of various earthworm species as a potential source of protein in aquatic feeds has also been proven by numerous studies. In terms of protein and lipid, the wild earthworm Perionyx excavatus (46.57% of protein and 8.03% of lipid) has comparable contents to that of fishmeal (54.97% of protein and 7.97% of lipid) [141]. Pucher et al. [142] investigated the effects of dried earthworms P. excavatus replacing fishmeal on the growth rate of carp Cyprinus carpio and recorded a better growth rate of carp at a level of 100% replacement. A study on shrimp P. vannamei found that diet containing soybean meal and earthworm meal at a ratio of 4:1 could significantly improve the growth performance and feeding efficiency [143]. It has been reported that up to 66.26% protein and 12.79% lipid in Tubifex tubifex have a proper profile of amino acids (13.47%–30.35% essential amino acids, 18.91%–43.44% total amino acids, 3.63% lysine, 7.25% linoleic acid, and 6.19% linolenic acid), and fatty acids (19.40%–40.13% SAFA, 24.36%–30.64% MUFA, 0.22%–2.18% EPA, 0.1%–1.17% DHA, and 8.06%–16.79% PUFA) [144]. This indicates the nutritional importance of zoobenthos in replacing conventional animal protein sources (fish meal) without compromising cultured aquatic animals’ growth, with tremendous benefits from economic and sustainable aspects.

4. Nutritional Contributions of Natural Biota to Cultured Aquatic Animals’ Growth

In semiintensive or intensive culture, juveniles exhibit a preference for feeding on natural biota over formulated feeds [145], and they derive a substantial part of their dietary nutrients from natural biota. They could promote better survival and growth of cultured aquatic animals compared with artificial diets alone [18, 125]. For example, the early (0.10 ± 0.05 g) and advanced juveniles (0.98 ± 0.43 g) of Cherax quadricarinatus fed on biofilm (Chlorophyta, xantophytas, pennate diatoms, cyanobacteria, flagellates, ciliates, rotifers, and nematodes) and formulated feed showed better survival, growth performance, and hepatopancreatic levels of total lipids when compared to the group only receiving formulated feed [146]. Natural foods such as mussels, Perna sp., squid, Loligo sp., trash fish, Leiognathus sp., Oreochromis sp., small bivalves, Potamocorbula sp., shrimp, and Fenneropenaeus sp. produce better larval quality in the mub crab genus Scylla than formulated feed [147]. The plankton could also improve the growth of rohu Labeo rohita, which was positively correlated with plankton availability [148]. Even provided with a formulated pellet, aquatic animals (e.g., C. destructor) consumed a high proportion of natural biota, and the dietary protein levels could be reduced from 30% to 19% without compromising their growth performance (e.g., weight, abdomen length, and abdomen width) [16]. Similar findings were also observed in channel catfish, hybrid catfish, common carp, and silver carp. Natural biota (rotifers, copepods, cladocerans, and ostracods) supported almost the same as formulated feed in their growth and survival [149], indicating farmers can benefit from improving feeding strategies by shifting towards more profitable natural food resources [150]. Overall, these studies further indicate the significant contribution natural biota make to different cultured aquatic animals’ growth.

Quantifying the contributions of natural biota to the growth of cultured aquatic animals and to what extent the input of formulated feed can be reduced without compromising their growth are critical to improving feeding strategies aquaculture efficiencies. Numerous studies have been carried out to nutritionally evaluate the contributions of natural biota and formulated feeds to different cultured aquatic animals’ growth. The analysis of stomach content showed that natural biota constitute main diets of many species such as juvenile P. monodon (only 21.7%–47.5% of formulated feed, 21.1%–42.3% of plant materials, 1.8%–31.7% of crustacean parts, and 8.6%–27% of diverse detrital matter) [151], Nile tilapia Oreochromis niloticus (64.2%–86.2% of detritus and phytoplankton, phytoplankton > detritus > zooplankton) [152, 153], the small freshwater fish Amblypharyngodon mola (50% of Chlorophyceae and nearly 30% of Cyanophyceae) [154], and Paranephrops zealandicus (58.3% of terrestrial detritus) [155]. This information provides an important indicator that formulated feed plays a limited role in the growth of these organisms.

Besides gut content analysis, a stable isotope mixing model is often used to quantify the contributions of natural biota to cultured aquatic animals’ growth. Results found that the contributions of natural foods (e.g., detritus, diatoms, filamentous algae, macroalgae, protozoans, crustaceans, detritus, polychaetes, and rotifers) to cultured aquatic animals’ growth were 44% for omnivorous crayfish Pacifastacus leniusculus [156], 48%–89% for juvenile shrimp L. vannamei [157, 158], and 43.9% for red claw C. quadricarinatus [159]. These indicate the ineffectiveness of aquatic animals in utilizing formulated feeds. The situation is particularly true for P. clarkii, where the feeding levels of formulated feed could be reduced from 100% satiation to 60% satiation without compromising the growth performance (final weight, final length, gonadosomatic index, hepatosomatic index, specific growth rate, and muscle weight) and biochemical composition (crude protein, crude lipid, ash, and moisture) of P. clarkii due to the nutritional supplementation of natural food Hydrilla verticillata (60% of coverage in each pond). The stable isotope analysis revealed that the contribution of H. verticillata increased from 27.84% to 50.26% when feeding levels decreased from 100% satiation to 60% satiation. Another study also demonstrated that for P. clarkii, their main sources of energy demand are from preying on insect larvae (up to 67% by occurrence), followed by fresh macrophytes, detritus, and sediment grains [160]. Roy et al. [161] and Correia et al. [162] also reported the similar results that reducing the daily feeding ratio from 110% to 60% and from 100% to 50% (daily ration) did not significantly affect the growth of L. vannamei and freshwater prawn Macrobrachium rosenbergii due to the contribution of pond primary productivity. The study on juvenile blue shrimp L. stylirostris reported that juveniles’ biomass (consumed natural foods in the biofloc systems) was 4.4 times as that of those grown in clear water, with natural productivity contributing to 39.6%–39.8% of its growth [106]. With certainty about reproducibility and the application of research data to real-time fish and crustacean farming, more nutritional research on the utilization of natural biota in aquaculture ponds should be conducted in situ on typical crustacean aquaculture, and the generated data from the on-farm evaluation should be evaluated from an economic perspective.

4.1. Future Perspectives

Sustainable aquaculture is a cost-effective production of fishery products, with continuous interaction with the ecosystems via natural biota. In particular, as the larvae transition to juveniles, the capacity to store food in the gastrointestinal tract is limited; hence, stage mortality occurs most frequently. There is a need at this early stage to continuously supply foods to prevent starvation and promote optimal growth and maturity [163]. However, applying natural biota to meet this demand requires robust and sustainable practices to support aquaculture management. The future of aquaculture is premised on applying natural biota in combination with other innovative techniques to improve formulated feed conversion efficiency in aquaculture. Furthermore, the future of aquaculture production also highlights maintaining the balance between natural biota biomass and formulated feed input to achieve higher fishery production with lower operational costs, which might be highly dependent on the stability of culture systems. This scenario motivates new research into intrinsic and extrinsic factors (e.g., the natural biota’s functional and structural connectivity) mitigating the ecological integrity of fish and crustacean aquaculture.

Data Availability

The data used to support the findings of this study are included within the article.

Disclosure

The funding sponsors had no roles in the design of the study; in the collection, analysis, or interpretation of data; in the writing of the manuscript; nor in the decision to publish the results.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Authors’ Contributions

Shiyu Jin, Qingling Kong, and Chibuike Kemdi John contributed equally to this review.

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (grant nos. 52100218 and 32002408), Natural Science Foundation of the Higher Education Institutions of Jiangsu Province (grant no. 20KJB180015), Natural Science Research Project of Huaian (grant no. HAB202063), China Agriculture Research System of MOF and MARA (grant no. CARS-45), and the National Key Research and Development Program of China (grant no. 2019YFD0900304) National Undergraduate Training Program For Innovation (202211049005Z).

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Copyright © 2023 Shiyu Jin et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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