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Article

Effects of Phosphate-Enriched Nutrient in the Polyculture of Nile Tilapia and Freshwater Prawn in an Aquaponic System

by
Soko Nuswantoro
1,2,†,
Tzu-Yuan Sung
3,†,
Meki Kurniawan
3,
Tsung-Meng Wu
4,
Bonien Chen
1,* and
Ming-Chang Hong
3,*
1
Institute of Aquatic Science and Technology, College of Hydrosphere, National Kaohsiung University of Science and Technology, Kaohsiung 811213, Taiwan
2
Study Program of Aquaculture, Faculty of Fisheries and Marine Science, Brawijaya University, Malang 65145, Indonesia
3
Department and Graduate Institute of Aquaculture, College of Hydrosphere, National Kaohsiung University of Science and Technology, Kaohsiung 811213, Taiwan
4
Department of Aquaculture, National Pingtung University of Science and Technology, Pingtung 91201, Taiwan
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Fishes 2023, 8(2), 81; https://doi.org/10.3390/fishes8020081
Submission received: 22 December 2022 / Revised: 21 January 2023 / Accepted: 28 January 2023 / Published: 30 January 2023
(This article belongs to the Section Sustainable Aquaculture)
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Abstract

:
Aquaponic systems are made up of hydroponic beds and recycled aquaculture systems. The significant elements that determine how effectively an aquaponic system operates are the nitrogen cycle (nitrification) and the phosphorus cycle (phosphate). Because some research indicates that aquaponics systems are primarily deficient in phosphorus, phosphate-enriched nutrients were added to raise the phosphorus levels. During an eight-week experimental period, the effects of water quality parameters and microbiology, animal and plant growth performance, chlorophyll compounds in lettuce, and the bacterial community were analyzed. Phosphate concentration (1.604 ± 1.933 mg L−1) and ammonia-oxidizing bacteria (AOB) (1.19 × 102 ± 1.30 CFU mL−1) give significant positive reactions to the added nutrients. However, the prawn survival rate (17.00 ± 0.63%) showed a significantly negative response to nutrition modification containing phosphate, and the percentage of bacterial pathogens became more dominant (pathogen 40.51%; N_bacteria 35.05%; probiotics 24.44%). This study shows that adding phosphate increases phosphorus levels in an aquaponics system and changes the microbial community and species growth performance.

1. Introduction

Aquaponics is an approach for merging aquaculture and hydroponics in an environment that grows crops in recycled aquaculture water [1]. Hydroponics is the practice of growing plants in water without soil. The two are combined in an enclosed, recirculating system called aquaponics. The organic wastes accumulated in the water are filtered and removed with a typical recirculating aquaculture system, keeping the water clean for the fish. However, an aquaponics system passes the nutrient-rich wastewater through a plant-filled inert substrate. Here, microorganisms break down the waste from the fish, plants absorb the resulting nutrients, and finally, the water is cleaned and returned to the fish tanks [2]. By cleaning the water to dispose of harmful waste and reusing water, recirculating systems are intended to rear mass amounts of fish in relatively small amounts [3].
In soils, natural water streams, and municipal sewage, nitrification is vital in cycling nutrients [4]. Nitrification results in the oxidation of ammonia to nitrate in agricultural land fertilized with ammonia-based fertilizers [5]. Through nitrifying microbes, NH4+ is easily converted to NO3 in oxic conditions, such as deep-cleaning soils. Due to the ease with which plants can absorb nitrate, the process is crucial for soil health [6].
In general, in addition to the nitrogen cycles with nitrification, phosphorus cycles in aquaponics settings cannot be separated. Phosphorus, an essential mineral, frequently determines biological mechanisms, including crop growth, in soils [7]. As it is a necessary component for supporting all living and agricultural production on our earth, phosphorus (P) is a critical component. All crops require three macronutrients (N, K, and P), and it is one of them [8]. Crop production is slowed by phosphorus deficiency, while too much phosphorus might react negatively with other nutrients [9].
Previous investigations have discovered a deficiency in total P in their aquaponics systems [10,11]. This could be because P precipitated as solids, separated in purification chambers, and rendered inaccessible. If the system water has much calcium, orthophosphate might precipitate once at neutral pH to generate calcium phosphate or dicalcium phosphate [12,13]. When calcium phosphate (Ca3(PO4)2) is in a solid form, it will not be possible for crops to utilize it, and it can be removed from the system with a purification chamber [14]. When crops cannot utilize P in solid form, they will grow slower because of a lack of P uptake, primarily in higher nutritional crops such as fruits or vegetables [15].
The purpose of this study was to evaluate the effect of the addition of phosphate-enriched nutrients (MN) and without (NN) in an aquaponic system, using lettuce (Lactuca sativa L.) and tilapia (Oreochromis niloticus) maintained with freshwater shrimp (Macrobrachium rosenbergii), on water quality and microbiology, aquaponics performance (tilapia, giant freshwater prawn, and lettuce), chlorophyll compounds in lettuce, and the bacterial community using a metagenomics technique.

2. Materials and Methods

2.1. Aquaponics Design

The aquaponics system comprised two 500 L fish tanks, a 1 × 4 × 0.5-m hydroponic tank with a water volume of 1200 L and hydroton (8–12 mm) at a minimum depth of 30 cm, a 2 × 1 × 0.5-m sump tank with a water volume of 400 L, and two filtration tanks (a solid separator and biofilter) with a water volume of 200 L each. Water from the fish tanks flows through a solid separator and biofilter (equipped with a K1 filter, an aerator, and live bacteria) before reaching the media bed where plants are grown. The water then flows to the sump tank and is recirculated back to the fish tanks. The system uses gravity to move water and a bell siphon to automatically flood and drain the bed media. A water pump (SP500 AH, 1/2 HP, 110/220 V) with a flow rate of 600 L per hour and a ball valve regulates the flow rate from the sump tank back to the fish tanks (Figure 1).

2.2. Phosphorus Solution Preparation

A phosphorus solution was made by mixing urea (30 g), calcium nitrate (236 g), monopotassium phosphate (90 g), monoammonium phosphate (37 g), magnesium sulfate (246 g), chimeric iron (10 g), boric acid (3 g), manganese chloride (1 g), zinc sulfate (0.09 g), copper sulfate (0.04 g), and sodium molybdate (0.01 g) in 1 L of distilled water to make a 1000× phosphorus solution [16]. The solution was only given at the beginning of the experimental period when the lettuce was planted to raise the phosphate level.

2.3. Experimental Setup

The study was conducted using six aquaponic setups, with three serving as the control group with unmodified nutrition (NN) and three as the treatment group with modified nutrition (MN). In each setup, 100 tilapias (100 ± 2 g) were placed in both of the two fish tanks, and 30 prawns (20.0 ± 0.3 g) in the sump tank. Once the system is running smoothly and stable for two weeks, 50 lettuce plants (Lactuca sativa L-Known-You Seed) can be transplanted into the grow bed of the aquaponic system, one week after they have been seeded in seedling trays with compost media. An eight-week experiment was conducted from January to March 2020 at the Aquaculture Department of National Kaohsiung University Science and Technology in Kaohsiung, Taiwan, using open-space outdoor laboratories. During the experiment, tilapia and giant freshwater prawns were fed a 32% crude protein commercial diet (Quanxing 1.6 mm, Grobest, Pingtung County, Taiwan) twice daily, with the amount given proportionate to 3% of their body weight.

2.4. Water Quality Monitoring

Temperature, pH, and dissolved oxygen were measured twice daily (8:00 am and 5:00 pm) using HI98194 (HANNA Instruments, Smithfield, RI). Ammonia, nitrite, nitrate, and phosphate levels were measured weekly using HI83300 (HANNA Instruments, Smithfield, RI) [17]. The measurements were taken in each of the water columns (fish tank, filter tank, sump tank) and an average was calculated for each water quality parameter.

2.5. Microbiology

At the end of the experiment, 50 mL of sediment was collected from the aquaponic system’s sediment bed for microbiological assessment. The samples were homogenized and diluted in a serially (10−1, 10−2, 10−3) sterile solution (0 ppt) before being plated on selective media for ammonia-oxidizing [18] and nitrifying-oxidizing bacteria [19]. The samples were incubated at 35 °C, and colony-forming units (CFU) were counted after 72 h. In addition, hydrotone granules were collected, crushed, and preserved at −5 °C for microbial species identification using Next Generation Sequencing (NGS) in Tools Biotechnology (Taipei, Taiwan). Descriptive analysis was conducted to determine the variation of the bacterial population using the OTU bar chart. Three replicates of samples were collected at randomly selected positions.

2.6. Tilapia, Giant Freshwater Prawn, and Lettuce Growth Performance

The performance of tilapia and giant prawns was assessed weekly by taking samples of 10 fish/prawn from each tank. The weight of the fish/prawn sample was measured at the beginning and end of the experiment. Survival (percentage) and final mean weight (g) were measured at the end of the rearing period. At the end of the experiment, the lettuce was weighed. Overall biomass and productivity of fish, prawns, and lettuce were also assessed to calculate total productivity.

2.7. Chlorophyll-a Content of Lettuce

Grinding–settling (GS) methods can be used to extract chlorophyll [20], which involve immersing the sample in 95% aqueous ethanol and then measuring the amount of chlorophyll present using an optical density spectrophotometer (OD). The spectrophotometer measures the concentration of both chlorophyll a and b by measuring the optical density at 645 nm and 663 nm [21], respectively. This information is then used to calculate the total concentration of chlorophyll (chlorophyll a and chlorophyll b) in the sample. Three replicates of samples were collected at randomly selected positions.

2.8. Data Analysis

Statistics were completed using SPSS Software. Before statistical treatments, Shapiro–Wilk and Levene tests were used to determine data normality and homogeneity, respectively. Before analysis, microbiological data were Log10 transformed to normalize the data [22]. The Student’s t-test was then used to compare variables, considered significance at p < 0.05.

3. Results

3.1. Water Quality and Microbiology

During the experiment, the average temperature was 23.78 ± 3.27 °C (NN) and 23.08 ± 3.12 °C (MN), the dissolved oxygen was 7.37 ± 0.82 mg L−1 (NN) and 7.36 ± 1.04 mg L−1 (MN), and the pH was 7.59 ± 0.30 (NN) and 7.52 ± 0.29 (MN). Averages for ammonia, nitrite, nitrate, phosphate, and microbiological results are shown in Table 1. The weekly values for ammonia, nitrite, nitrate, phosphate, and microbiological results are shown in Figure 2.

3.2. Tilapia, Giant Freshwater Prawn, and Lettuce Growth Performance

After eight weeks of rearing, the integration of prawn, tilapia, and lettuce with and without nutritional addition for the soilless culture influences prawn, tilapia, and lettuce performance, except for the survival of tilapia (Table 2). Prawn performance for the treatment with additional nutrition is worse than without nutrition. Prawns lose mass during culture in both treatments. However, the most significant loss after treatment is with additional nutrition—the lowest prawn survival was in the aquaponic setting using additional nutrition with only 17.00 ± 0.63% surviving. At the end of the experiment, 1.90 ± 0.37 kg of lettuce per experimental unit was harvested for the treatment without additional nutrition, which is more significant than the 1.65 ± 0.42 kg with additional nutrition.

3.3. Chlorophyll Compounds in Lettuce (Lactuca sativa L.)

The results of these compounds in lettuce (Lactuca sativa L.) are shown in Table 3. Chlorophyll-a and chlorophyll-b were higher after treatment with additional nutrition than without nutritional addition for the soilless culture. However, no significant differences were found in the statistical analysis for both treatments.

3.4. Bacterial Community

The presence of bacteria that can be cultured in each condition was determined depending on the diversity of the phyla obtained with the OTU analysis. Proteobacteria (24.96%) followed by Bacteroidetes (20.89%) was the order of those with the largest relative abundance in the aquaponic system without the addition of nutrients (NN). In comparison, Proteobacteria (27.69%) followed by Bacteroidetes (20.14%) was the order of the largest relative abundance in the aquaponic system with the addition of nutrients (MN) (Figure 3). Using the OTU analysis, 21 genera were found for the genus in both conditions. Flavobacterium (6%), Cetobacterium (7%), and Aurantimicrobium (2%) accounted for the most significant proportion in the aquaponic system without the addition of nutrients (NN). In comparison, Flavobacterium (13%) followed by Cetobacterium (6%) and Aurantimicrobium (6%) was the order of those with the most significant relative abundance in the aquaponic system with the addition of nutrients (MN) (Figure 4). Table 4 shows the presence or absence of culturable microorganisms under both conditions.

4. Discussion

In an aquaponic system, water quality is a limiting element. Maintaining appropriate water quality will ensure that the performance of the animals and plants in the system follows our goal. This seems to be difficult in a connected system since the quality of the water moving in the hydroponic and aquaculture subsystems is the same and continuously flowing in both systems. One main water quality parameter that is challenging to control at optimal values is pH. The optimal pH for plants will be different from that for fish, in general. The plant pH should be 5.5, and the fish pH should be around 7.5 [48]. In this case, for soilless lettuce culture, the pH is around 6.5–7.0 [16]. Our results show that a pH of around 7.5 should be optimal for fish but less for lettuce soilless culture. The survival rate of 100% for tilapia (Table 2) is acceptable for fish living in these aquaponic systems. Tilapia is a widely used fish in aquaponic systems due to its ability to adapt to a range of water conditions and its hardiness [49]. These fish must be able to tolerate the high levels of nutrients in the water, which are added to promote plant growth [50]. On the other hand, the survival rate for giant freshwater prawns (Table 2) is 30.00 ± 0.90% for the non-treatment (NN) and 17.00 ± 0.63% for the with-treatment (MN). Both of these results are not as good as those found in another study of around 55% [51], thus survival should be affected by another factor.
Another significantly different water quality between both treatments is phosphate (PO43−) (Table 1). Phosphorus in aquaculture water bodies is often in an un-proportional amount [52]. Considering aquaculture pond contents are frequently more phosphorus-rich than natural waters, and because their discharge could contaminate receiving waters with phosphorus compounds and promote increased growth of plants, phosphorus is essential [53]. Around 30–65% of the phosphorus in the fish diet is still inaccessible to plants because it is fixed in the solid excretions, which are subsequently filtered out mechanically [54]. On the other hand, plants cannot easily access the kinds of phosphate found in fish waste. Because it is the only form that plants can absorb and assimilate, inorganic ionic is needed in adequate levels [55]. Above pH 7.0, inorganic phosphate bonds to calcium; hence, aquaponic systems should be careful about keeping pH levels near 7.0. Various insoluble derivatives of calcium phosphate can accumulate in sediment as pH levels rise above 7.0 [55,56]. The amount of phosphorus delivered by fish meal might vary regarding to the production state in a system that grows lettuce. Based on how the system is set up, roughly 100% of the phosphorus water can be recycled in the plant biomass [57]. In this study, there was much less in the treatment with added nutrition than in the treatment without nutrition (Table 2). It appears that phosphorus tends to be restricting and might thus inhibit plant growth including lettuce production [13,58]. P has a few distinct qualities; one is its poor availability brought on by slow absorption and increased soil fixing. This all indicates that P may pose a significant growth-limiting challenge to plants. Although using animal waste and chemical P for fertilization on cropland has increased crop yield and inorganic P richness, they have also damaged the ecosystem throughout the years [59].
Although feed remains the primary source of phosphorus for prawn ponds [60], the higher phosphate concentration in this study (Table 1) is likely influenced by the phosphate levels in the water flow. The added nutrition contains 90-g Monopotassium Phosphate (KH2PO4) and 37-g Monoammonium Phosphate (NH4H2PO4) in every 1000 L; this should be one of the sources of phosphate in the water aquaponic system with additional nutrition. When phosphate in water increases, it will positively affect AOB communities [61,62]. Trends in the significance of high phosphate and AOB (Table 1) clearly define that AOB in an aquaponic system with supplemental nutrition has a more significant population than without supplemental nutrition. As soon as particulate or soluble organic phosphorus breaks down into dissolved inorganic phosphorus and sinks to the bottom, substrate algae and phytoplankton take up the phosphorus [63]. Following phosphate dosing, a shift in the microbial community towards organisms that can utilize or metabolize phosphate was observed, including an increase in certain types of bacteria. [64].
A total of 13 phyla and 21 genera of known bacteria in this non-phosphorus-adding treatment system (>0.5% from population abundance) is dominated by N-related bacteria, which represent the majority of all bacteria in systems, followed by probiotic bacteria and pathogens (Figure 5). A total of 11 genera of bacteria involved in nitrogen cycles have been found (Table 4). This type of bacteria has the potential to successfully co-culture plant and animal symbiosis. Their primary function is converting the ammonia from the excrement and uneaten fish/prawn diet to nitrate and nitrite, allowing aquatic plants to use the end material more easily for growth. One species known to obtain energy through the anaerobic oxidation of ammonia is one of the Pirellula-like organisms considered typical root-associated bacteria [24,65]. They act as catalysts for significant changes in the global carbon and nitrogen cycles. Pirellula sp. strain 1 contains a gene that encodes a bacterial hemoglobin that is thought to detoxify nitric oxide (NO) by oxidation. Some carbon-starvation proteins, such as DNA-protection proteins, have homologs in the genome [29]. Nitrospira would fit into the comammox’s theoretically projected ecological niche. Biofilm or floc production is a feature of the engineered systems examined in this work. In biofilms, diffusion barriers and ammonium or nitrite concentration gradients could form niches with limited substrate influx, allowing comammox to outcompete incomplete nitrifiers. Diverse nitrifier communities may be supported by complex biofilm or floc designs with multiple microenvironments [25].
Next, the phosphorus-adding nutrition treatment group is dominated by pathogens, which represent the majority of all bacteria in systems, followed by N-related and probiotic bacteria (Figure 4). A total of three genera of pathogen bacteria have been found (Table 4). Even though just three genera have been found, they are likely to impact fish and prawn culture significantly. The total density of harmful bacteria that developed in the aquaponic system with nutrients added (MN) was substantially more significant than that of harmful bacteria that developed in the aquaponic system without nutrients added (NN). Flavobacterium, the most significant percentage in this group, could be one of the factors behind the dramatically varied survival rates of freshwater prawns in this study. In several studies, Flavobacterium, known as a pathogen [43,44], can be found in the early embryonic phase of M. rosenbergii when in the blastula stage [66]. According to some studies, Aeromonas is one of the diseases bvastria that has put the huge freshwater prawn growth system at risk [67,68,69]. The damage produced by mycobacteria invasion and spread had not yet manifested clinical indications, such as aberrant conduct. The cytoplasm of fixed phagocytes of this animal did not contain acid-fast bacteria. According to the histopathology findings, M. rosenbergii’s predominant host response to mycobacteria infection was hemocyte encapsulation rather than phagocytes [46].
Chlorophyll, the principal pigment of leafy green vegetables, is essential in determining their health condition. Because most nitrogen is absorbed in leaf chlorophyll, the nutritional status of leafy green vegetables can also be assessed by quantifying chlorophyll content. In this study, the amount of chlorophyll extracted using both procedures (grinding–settling and immersion) had no significant difference between the aquaponic systems with and without added nutrition (Table 3), which is consistent with earlier studies [70,71]. It has been proven that chlorophyll activity is still regular.

5. Conclusions

Adding a fertilizer containing phosphate directly into a body of water can significantly increase phosphorus levels in an aquaponic system. This strongly supports the observation that AOB and NOB alter their community. An increase in pathogenic bacteria, particularly Flavobacterium and Aeromonas, was observed as a result of nutrient addition. However, there is no significant change in water quality (DO, pH, temperature, ammonia, nitrate, nitrite) or the growth performance of tilapia and lettuce. The only result not in favor of this system is the giant prawns’ meager survival rate, which could have been affected by pathogenic bacteria in the nutrient-rich system. Both Flavobacterium and Aeromonas are known pathogens in most shrimp or prawn ponds. Further research is needed on the sources of phosphate in aquaponic systems that need to be controlled for their forms that are rather accessible for plants, but that should not support the proliferation of microbial pathogens. Additionally, using other species that have a high tolerance to fluctuations in macro- and micro-nutrients, such as catfish, may be considered during the experiment.

Author Contributions

Conceived the idea and developed the theory and experimental design, M.-C.H. and B.C.; measurements, planning and supervised the work, M.K.; processed the experimental data, performed the analysis, drafted the manuscript, and designed the figures, S.N. and M.K.; manufactured the samples and characterized them with statistics, S.N. and T.-Y.S.; co-aided in interpreting the results and worked on the manuscript, M.-C.H. and T.-M.W. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Ministry of Science and Technology, Taiwan (MOST 107-2311-B-992-003-MY3) and the MOE Teaching Practice Research Program (PSR1100590). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Institutional Review Board Statement

This animal study was reviewed and approved by the Institutional Animal Care and Use Committee of National Pingtung University of Science and Technology (approval code NPUST-108-017, approved on 17 March 2019).

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We acknowledge the T-M, Wu’s lab. in Taiwan for kindly providing of the source of tilapias and also for technical and equipment support as well as for providing comments that greatly improved the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Somerville, C.; Cohen, M.; Pantanella, E.; Stankus, A.; Lovatelli, A. Small-Scale Aquaponic Food Production. Integrated Fish and Plant Farming; FAO Fisheries and Aquaculture Technical Paper No.­589; FAO: Rome, Italy, 2014; 262p. [Google Scholar]
  2. Campanhola, C.; and Pandev, S. Sustainable Food and Agriculture: An Integrated Approach; Academic Press: Cambridge, MA, USA, 2019; 585p. [Google Scholar] [CrossRef]
  3. Rakocy, J.E. Aquaponics–integrating fish and plant culture. In Aquaculture Production Systems, 1st ed.; Tidwell, J., Ed.; John Wiley & Sons Inc.: Hoboken, NJ, USA, 2012; pp. 343–386. [Google Scholar] [CrossRef]
  4. Ward, B.B. Nitrification in marine systems. In Nitrogen in the Marine Environment, 2nd ed.; Capone, D.G., Bronk, D.A., Mulholland, M.R., Carpenter, E.J., Eds.; Academic Press: Cambridge, MA, USA, 2008; pp. 199–261. [Google Scholar]
  5. Arp, D.J.; Stein, L.Y. Metabolism of Inorganic N Compounds by Ammonia-Oxidizing Bacteria. Crit. Rev. Biochem. Mol. Biol. 2003, 38, 471–495. [Google Scholar] [CrossRef]
  6. Ergas, S.J.; Aponte-Morales, V. Biological Nitrogen Removal. In Comprehensive Water Quality and Purification; Ahuja, S., Ed.; Elsevier: Amsterdam, The Netherland, 2014; Volume 3, pp. 124–149. [Google Scholar] [CrossRef]
  7. Valsami-Jones, E. Phosphates. In Encyclopedia of Geology, 2nd ed.; Alderton, D., Elias, S.A., Eds.; Academic Press: Cambridge, MA, USA, 2021; Volume 1, pp. 422–427. [Google Scholar] [CrossRef]
  8. Liu, Y.; Chen, J. Phosphorus cycle. In Encyclopedia of Ecology, 2nd ed.; Fath, B., Ed.; Elsevier: Amsterdam, The Netherland, 2019; Volume 4, pp. 181–191. [Google Scholar] [CrossRef]
  9. Barben, S.A.; Hopkins, B.G.; Jolley, V.D.; Webb, B.L.; Nichols, B.A. Optimizing phosphorus and zinc concentrations in hydroponic chelator-buffered nutrient solution for Russet Burbank potato. J. Plant Nutr. 2010, 33, 557–570. [Google Scholar] [CrossRef]
  10. Endut, A.; Jusoh, A.; Ali, N.; Wan Nik, W.B.; Hassan, A. A study on the optimal hydraulic loading rate and plant ratios in recirculation aquaponic system. Bioresour. Technol. 2010, 101, 1511–1517. [Google Scholar] [CrossRef]
  11. Yang, T.; Kim, H. Comparisons of nitrogen and phosphorus mass balance for tomato-, basil-, and lettuce-based aquaponic and hydroponic systems. J. Clean. Prod. 2020, 274, 122619. [Google Scholar] [CrossRef]
  12. Rakocy, J.E.; Masser, M.P.; Losordo, T.M. Recirculating aquaculture tank production systems: Aquaponics–integrating fish and plant culture. SRAC Publ. 2006, 454, 1–16. [Google Scholar]
  13. Seawright, D.E.; Stickney, R.R.; Walker, R.B. Nutrient dynamics in integrated aquaculture hydroponics systems. Aquaculture 1998, 160, 215–237. [Google Scholar] [CrossRef]
  14. Cerozi, B.D.S.; Fitzsimmons, K. The effect of pH on phosphorus availability and speciation in an aquaponics nutrient solution. Bioresour. Technol. 2016, 219, 778–781. [Google Scholar] [CrossRef] [Green Version]
  15. Cerozi, B.D.S.; Fitzsimmons, K. Effect of dietary phytase on phosphorus use efficiency and dynamics in aquaponics. Aquac. Int. 2017, 25, 1227–1238. [Google Scholar] [CrossRef]
  16. Kao, T.-C. The Deployment and Application of Liquid Fertilizer Formula in Facility Vegetable Cultivation. Seminar on R&D and Application of Facility Vegetables and Soilless Culture. The Agricultural Improvement Field of Taichung District, Agricultural Committee of the Executive Yuan, Taichung, Taiwan. Available online: https://www.tdais.gov.tw/upload/tdais/files/web_structure/11962/TC02-133-12.pdf (accessed on 7 July 2017).
  17. Kopp, J.F. Method for Chemical Analysis of Water and Wastes, 3rd ed.; United States Environmental Protection Agency: Columbus, OH, USA, 1978; 920p.
  18. MacDonald, R.M.; Spokes, J.R. A selective and diagnostic medium for ammonia oxidising bacteria. FEMS Microbiol. Lett. 1980, 8, 143–145. [Google Scholar] [CrossRef]
  19. Elbanna, K.; El-Shahawy, R.M.; Atalla, K.M. A new simple method for the enumeration of nitrifying bacteria in different environments. Plant Soil Environ. 2012, 58, 49–53. [Google Scholar] [CrossRef] [Green Version]
  20. Su, S.; Zhou, Y.; Qin, J.G.; Yao, W.; Ma, Z. Optimization of the Method for Chlorophyll Extraction in Aquatic Plants. J. Freshw. Ecol. 2010, 25, 531–538. [Google Scholar] [CrossRef] [Green Version]
  21. Zhang, J.; Han, C.; Liu, Z. Absorption spectrum estimating rice chlorophyll concentration: Preliminary investigations. J. Plant Breed. Crop Sci. 2009, 1, 223–229. [Google Scholar] [CrossRef]
  22. Zar, J.H. Biostatistical Analysis, 5th ed.; Prentice-Hall: Hoboken, NJ, USA, 2010; 944p. [Google Scholar]
  23. Nakai, R.; Fujisawa, T.; Nakamura, Y.; Nishide, H.; Uchiyama, I.; Baba, T.; Toyoda, A.; Fujiyama, A.; Naganuma, T.; Niki, H. Complete Genome Sequence of Aurantimicrobium minutum Type Strain KNCT, a Planktonic Ultramicrobacterium Isolated from River Water. Genome Announc. 2016, 4, e00616-16. [Google Scholar] [CrossRef] [Green Version]
  24. Derakshani, M.; Lukow, T.; Liesack, W. Novel bacterial lineages at the (sub) division level as detected by signature nucleotide-targeted recovery of 16S rRNA genes from bulk soil and rice roots of flooded rice microcosms. Appl. Environ. Microbiol. 2001, 67, 623–631. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Daims, H.; Lebedeva, E.V.; Pjevac, P.; Han, P.; Herbold, C.; Albertsen, M.; Jehmlich, N.; Palatinszky, M.; Vierheilig, J.; Bulaev, A.; et al. Complete nitrification by Nitrospira bacteria. Nature 2015, 528, 504–509. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Young, C.C.; Kampfer, P.; Ho, M.J.; Busse, H.J.; Huber, B.E.; Arun, A.B.; Shen, F.T.; Lai, W.A.; Rekha, P.D. Arenimonas malthae sp. nov., a gammaproteobacterium isolated from an oil-contaminated site. Int. J. Syst. Evol. Microbiol. 2007, 57, 2790–2793. [Google Scholar] [CrossRef]
  27. Lukwambe, B.; Nicholaus, R.; Zhao, L.; Yang, W.; Zhu, J.; Zheng, Z. Microbial community and interspecies interaction during grazing of ark shell bivalve (Scapharca subcrenata) in a full-scale bioremediation system of mariculture effluents. Mar. Environ. Res. 2020, 158, 104956. [Google Scholar] [CrossRef]
  28. Wu, Y.R.; He, J. Characterization of a xylanase-producing Cellvibrio mixtus strain J3-8 and its genome analysis. Sci. Rep. 2015, 5, 10521. [Google Scholar] [CrossRef] [Green Version]
  29. Glockner, F.O.; Kube, M.; Bauer, M.; Teeling, H.; Lombardot, T.; Ludwig, W.; Gade, D.; Beck, A.; Borzym, K.; Heitmann, K.; et al. Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc. Natl. Acad. Sci. USA 2003, 100, 8298–8303. [Google Scholar] [CrossRef] [Green Version]
  30. Kumar, M.; Zeyad, M.T.; Choudhary, P.; Paul, S.; Chakdar, H.; Rajawat, M.V.S. Thiobacillus. In Beneficial Microbes in Agro-Ecology; Amaresan, N., Kumar, M.S., Annapurna, K., Kumar, K., Sankaranarayanan, A., Eds.; Academic Press: Cambridge, MA, USA, 2020; pp. 545–557. [Google Scholar] [CrossRef]
  31. Kallscheuer, N.; Wiegand, S.; Heuer, A.; Rensink, S.; Boersma, A.S.; Jogler, M.; Boedeker, C.; Peeters, S.H.; Rast, P.; Jetten, M.S.M.; et al. Blastopirellula retiformator sp. nov. isolated from the shallow-sea hydrothermal vent system close to Panarea Island. Antonie Leeuwenhoek 2020, 113, 1811–1822. [Google Scholar] [CrossRef]
  32. Wang, J.; Wang, C.; Li, J.; Bai, P.; Li, Q.; Shen, M.; Li, R.; Li, T.; Zhao, J. Comparative Genomics of Degradative Novosphingobium Strains with Special Reference to Microcystin-Degrading Novosphingobium sp. THN1. Front. Microbiol. 2018, 9, 2238. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Fudou, R.; Jojima, Y.; Iizuka, T.; Yamanaka, S. Haliangium ochraceum gen. nov., Haliangium ochraceum sp. nov. and Haliangium tepidum sp. nov.: Novel moderately halophilic myxobacteria isolated from coastal saline environments. J. Gen. Appl. Microbiol. 2002, 48, 109–115. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Sangwan, P.; Chen, X.; Hugenholtz, P.; Janssen, P.H. Chthoniobacter flavus gen. nov., sp. nov., the First Pure-Culture Representative of Subdivision Two, Spartobacteria classis nov., of the Phylum Verrucomicrobia. Appl. Environ. Microbiol. 2004, 70, 5875–5881. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  35. Sakyi, M.E.; Cai, J.; Tang, J.; Abarike, E.D.; Xia, L.; Li, P.; Kuebutornye, F.K.A.; Zou, Z.; Liang, Z.; Jian, J. Effects of starvation and subsequent re-feeding on intestinal microbiota, and metabolic responses in Nile tilapia, Oreochromis niloticus. Aquac. Rep. 2020, 17, 100370. [Google Scholar] [CrossRef]
  36. Xie, M.; Hao, Q.; Olsen, R.E.; Ringø, E.; Yang, Y.; Zhang, Z.; Ran, C.; Zhou, Z. Growth performance, hepatic enzymes, and gut health status of common carp (Cyprinus carpio) in response to dietary Cetobacterium somerae fermentation product. Aquac. Rep. 2022, 23, 101046. [Google Scholar] [CrossRef]
  37. Beisser, D.; Bock, C.; Hahn, M.W.; Vos, M.; Sures, B.; Rahmann, S.; Boenigk, J. Interaction-specific changes in the transcriptome of Polynucleobacter asymbioticus caused by varying protistan communities. Front. Microbiol. 2019, 10, 1498. [Google Scholar] [CrossRef]
  38. Ohshiro, T.; Harada, N.; Kobayashi, Y.; Miki, Y.; Kawamoto, H. Microbial Fucoidan Degradation by Luteolibacter algae H18 with Deacetylation. Biosci. Biotechnol. Biochem. 2012, 76, 620–623. [Google Scholar] [CrossRef]
  39. Ghasemi, Y.; Rasoul-Amini, S.; Ebrahiminezhad, A.; Zarrini, G.; Kazemi, A.; Mousavi-Khorshidi, S.; Ghoshoon, M.B.; Raee, M.J. Halotolerant Amylase Production by a Novel Bacterial Strain, Rheinheimera aquimaris. Res. J. Microbiol. 2010, 5, 144–149. [Google Scholar] [CrossRef] [Green Version]
  40. Romanenko, L.A.; Tanaka, N.; Svetashev, V.I.; Kalinovskaya, N.I.; Mikhailov, V.V. Rheinheimera japonicasp. nov., a novel bacterium with antimicrobial activity from seashore sediments of the Sea of Japan. Arch. Microbiol. 2015, 197, 613–620. [Google Scholar] [CrossRef]
  41. Li, Y.; Zhang, Z.; Xu, Z.; Fang, D.; Wang, E.T.; Shao, S.; Du, Z.; Liu, W.; Xie, Z. Jeotgalibacillus proteolyticus sp. nov., a protease-producing bacterium isolated from ocean sediments. Int. J. Syst. Evol. Microbiol. 2018, 68, 3790–3795. [Google Scholar] [CrossRef]
  42. Ponpukdee, N.; Wangman, P.; Rodkhum, C.; Pengsuk, C.; Chaivisuthangkura, P.; Sithigorngul, P.; Longyant, S. Detection and identification of a fish pathogen Flavobacterium columnare using specific monoclonal antibodies. Aquaculture 2021, 545, 737231. [Google Scholar] [CrossRef]
  43. Saticioglu, I.B.; Ay, H.; Altun, S.; Sahin, N.; Duman, M. Flavobacterium bernardetii sp. nov., a possible emerging pathogen of farmed rainbow trout (Oncorhynchus mykiss) in cold water. Aquaculture 2021, 540, 736717. [Google Scholar] [CrossRef]
  44. Singh, S.; Mallik, S.K.; Kala, K.; Shahi, N.; Pathak, R.; Giri, A.K.; Chandra, S.; Pant, K.; Patiyal, R.S. Characterization of Flavobacterium columnare from farmed infected rainbow trout, Oncorhynchus mykiss (Walbaum, 1792) of Central Indian Himalayan region, India. Aquaculture 2021, 544, 737118. [Google Scholar] [CrossRef]
  45. Janda, J.M.; Abbott, S.L. The Genus Aeromonas: Taxonomy, Pathogenicity, and Infection. Clin. Microbiol. Rev. 2010, 23, 35–73. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Brock, J.A.; Nakagawa, L.K.; Shimojo, R.J. Infection of a cultured freshwater prawn, Macrobrachium rosenbergii de Man (Crustacea: Decapoda), by Mycobacterium spp., Runyon Group II. J. Fish Dis. 1986, 9, 319–324. [Google Scholar] [CrossRef]
  47. Payeur, J.B. Mycobacterium. In Encyclopedia of Food Microbiology, 2nd ed.; Batt, C.A., Tortorello, M.L., Eds.; Academic Press: Cambridge, MA, USA, 2014; pp. 841–843. [Google Scholar] [CrossRef]
  48. Lennard, W.; Goddek, S. Aquaponics: The Basics. In Aquaponics Food Production Systems, 1st ed.; Goddek, S., Joyce, A., Kotzen, B., Burnell, G.M., Eds.; Springer Cham: New York, NY, USA, 2019; pp. 113–143. [Google Scholar] [CrossRef] [Green Version]
  49. Pinho, S.M.; David, L.H.; Garcia, F.; Keesman, K.J.; Portella, M.C.; Goddek, S. South American fish species suitable for aquaponics: A review. Aquac. Int. 2021, 29, 1427–1449. [Google Scholar] [CrossRef]
  50. Yildiz, H.Y.; Robaina, L.; Pirhonen, J.; Mente, E.; Dominguez, D.; Parisi, G. Fish welfare in aquaponic systems: Its relation to water quality with an emphasis on feed and faeces: A review. Water 2017, 9, 13. [Google Scholar] [CrossRef] [Green Version]
  51. Dusci, J.C.; Hager, J.; Coyle, S.; Tidwell, J. Evaluation of freshwater prawn, Macrobrachium rosenbergii, for biological solids control in raft aquaponic systems and the protective effectiveness of root guards. J. World Aquac. Soc. 2021, 53, 1–19. [Google Scholar] [CrossRef]
  52. Yep, B.; Zheng, Y. Aquaponic trends and challenges—A review. J. Clean. Prod. 2019, 228, 1586–1599. [Google Scholar] [CrossRef]
  53. Boyd, C.E.; Tucker, C.S. Pond Aquaculture Water Quality Management, 1st ed.; Springer: New York, NY, USA, 1998; 712p. [Google Scholar] [CrossRef]
  54. Schneider, O.; Sereti, V.; Eding, E.H.; Verreth, J.A.J. Analysis of nutrient flows in integrated intensive aquaculture systems. Aquac. Eng. 2004, 32, 379–401. [Google Scholar] [CrossRef]
  55. Becquer, A.; Trap, J.; Irshad, U.; Ali, M.A.; Claude, P. From soil to plant, the journey of P through trophic relationships and ectomycorrhizal association. Front. Plant Sci. 2014, 5, 1–8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Siebielec, S.; Urbaniak, M.; Siebielec, G.; Kidd, P.; Smreczak, B.; Grzęda, E. Bacterial inoculation effect on bioavailability of trace elements and organic contaminants in bottom sediment contaminated soils. In Proceedings of the XII Symposium Trace elements in the environment, Puławy, Poland, 17–19 November 2014. [Google Scholar]
  57. Cerozi, B.S.; Fitzsimmons, K. Phosphorus dynamics modeling and mass balance in an aquaponics system. Agric. Syst. 2017, 153, 94–100. [Google Scholar] [CrossRef]
  58. Graber, A.; Junge, R. Aquaponic systems: Nutrient recycling from fish wastewater by vegetable production. Desalination 2009, 246, 147–156. [Google Scholar] [CrossRef]
  59. Shen, J.; Yuan, L.; Zhang, J.; Li, H.; Bai, Z.; Chen, X.; Zhang, W.; Zhang, F. Phosphorus Dynamics: From Soil to Plant. Plant Physiol. 2011, 156, 997–1005. [Google Scholar] [CrossRef] [Green Version]
  60. Xia, L.Z.; Yang, L.Z.; Yan, M.C. Nitrogen and Phosphorus Cycling in Prawn Ponds and the Measures for Sustainable Management. Environ. Geochem. Health 2004, 26, 245–251. [Google Scholar] [CrossRef] [PubMed]
  61. Kragh, T.; Søndergaard, M.; Tranvik, L. Effect of exposure to sunlight and phosphorus-limitation on bacterial degradation of coloured dissolved organic matter (CDOM) in freshwater. FEMS Microbiol. Ecol. 2008, 64, 230–239. [Google Scholar] [CrossRef]
  62. Lage, M.D.; Reed, H.E.; Weihe, C.; Crain, C.M.; Martiny, J.B. Nitrogen and phosphorus enrichment alter the composition of ammonia-oxidizing bacteria in salt marsh sediments. Microb. Ecol. 2010, 4, 933–944. [Google Scholar] [CrossRef]
  63. Shimoda, T.; Fujioka, Y.; Srithong, C.; Aryuthaka, C. Phosphorus budget in prawn aquaculture pond with mangrove enclosure and aquaculture performance. Fish Sci. 2005, 71, 1249–1255. [Google Scholar] [CrossRef]
  64. Douterelo, I.; Dutilh, B.E.; Calero, C.; Rosales, E.; Martin, K.; Husband, S. Impact of phosphate dosing on the microbial ecology of drinking water distribution systems: Fieldwork studies in chlorinated networks. Water Res. 2020, 187, 116416. [Google Scholar] [CrossRef]
  65. Strous, M.; Fuerst, J.A.; Kramer, E.H.; Logemann, S.; Muyzer, G.; van de Pas-Schoonen, K.T.; Webb, R.; Kuenen, J.G.; Jetten, M.S. Missing lithotroph identified as new planctomycete. Nature 1999, 400, 446–449. [Google Scholar] [CrossRef] [Green Version]
  66. Liu, B.; Liu, B.; Zhou, Q.; Sun, C.; Song, C.; Zhang, H.; Yang, Z.; Shan, F. Patterns of Bacterial Community Composition and Diversity Following the Embryonic Development Stages of Macrobrachium rosenbergii. Aquac. Rep. 2020, 17, 100372. [Google Scholar] [CrossRef]
  67. Saurabh, S.; Sahoo, P.K. Major diseases and the defence mechanism in giant freshwater prawn, Macrobrachium rosenbergii (de Man). Proc. Nat. Acad. Sci. India Sect. B 2008, 78, 103–121. [Google Scholar]
  68. Yathavamoorthi, R.; Alagarsamy, S.; Farvin, S. Enteric Bacteria and Water Quality of Freshwater Prawn Macrobrachium rosenbergii (De Man) in Culture Environment from Kerala, India. J. Fish Aquat. Sci. 2010, 5, 282–292. [Google Scholar] [CrossRef]
  69. Pillai, D.; Bonami, J.R. A review on the diseases of freshwater prawns with special focus on white tail disease of Macrobrachium rosenbergii. Aquac. Res. 2012, 43, 1029–1037. [Google Scholar] [CrossRef]
  70. Licamele, J.D. Biomass Production and Nutrient Dynamics in an Aquaponics System. Ph.D. Thesis, The University of Arizona, Tucson, AZ, USA, 16 November 2009. [Google Scholar]
  71. Da Rocha, A.F.; Filho, M.B.; Stech, M.R.; da Silva, R.P. Lettuce Production in Aquaponic and Biofloc Systems with Silver Catfish Rhamdia quelen. Bol. Inst. Pesca 2017, 44, 64–73. [Google Scholar] [CrossRef]
Fishes 08 00081 g001 550
Figure 1. Aquaponic water flows experimental design.
Figure 1. Aquaponic water flows experimental design.
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Figure 2. Weekly values for (a) ammonia, (b) nitrite, (c) nitrate, (d) phosphate, (e) AOB, (f) NOB (n = 3).
Figure 2. Weekly values for (a) ammonia, (b) nitrite, (c) nitrate, (d) phosphate, (e) AOB, (f) NOB (n = 3).
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Figure 3. Microbial composition during the experiment. OTU analysis based on the phylum level (n = 3).
Figure 3. Microbial composition during the experiment. OTU analysis based on the phylum level (n = 3).
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Figure 4. Microbial composition during the experiment. OTU analysis based on the genus level. The same color on the genus level indicates from same phylum (n = 3).
Figure 4. Microbial composition during the experiment. OTU analysis based on the genus level. The same color on the genus level indicates from same phylum (n = 3).
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Figure 5. The average percentage is known bacteria cultivable in aquaponic systems for eight weeks (a) without treatment and (b) with additional nutrition. (n = 3).
Figure 5. The average percentage is known bacteria cultivable in aquaponic systems for eight weeks (a) without treatment and (b) with additional nutrition. (n = 3).
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Table
Table 1. Chemical and microbial loads in an integrated aquaponic culture system.
Table 1. Chemical and microbial loads in an integrated aquaponic culture system.
ParameterNNMNp-Value (t-Test)
Ammonia (NH3) (mg L−1)0.30 ± 0.210.42 ± 0.230.074
Nitrite (NO2−) (mg L−1)0.18 ± 0.210.21 ± 0.270.654
Nitrate (NO3−) (mg L−1)0.96 ± 1.461.05 ± 2.000.857
Phosphate (PO4−) (mg L−1)0.72 ± 0.581.60 ± 1.930.040 *
Total bacteria
AOB (CFU mL−1)0.09 × 102 ± 0.061.19 × 102 ± 1.300.000 *
NOB (CFU mL−1)2.26 × 104 ± 3.313.42 × 104 ± 2.830.198
Data presented as mean ± standard deviation (n = 3). CFU: Colony-forming unit. Asterisks (*) indicate statistical differences (p < 0.05).
Table
Table 2. Performance in an integrated giant freshwater prawn (Macrobranchium rosenbergii), tilapia (Oreochromis niloticus), and lettuce (Lactuca sativa L) system (n = 3).
Table 2. Performance in an integrated giant freshwater prawn (Macrobranchium rosenbergii), tilapia (Oreochromis niloticus), and lettuce (Lactuca sativa L) system (n = 3).
ParameterNNMNp-Value
Prawn
Mean final weight (g)19.20 ± 0.7519.00 ± 0.580.733
Survival (%)30.00 ± 0.9017.00 ± 0.630.000 *
Final biomass (Kg)0.580 ± 0.0400.323 ± 0.0250.001*
Tilapia
Mean final weight (g)170.32 ± 0.17172.10 ± 1.550.120
Survival (%)1001001
Final biomass (Kg)17.033 ± 0.01517.213 ± 0.1550.116
Lettuce
Final Mass (kg)1.90 ± 0.371.65 ± 0.420.482
Total
Final biomass (Kg)19.51 ± 0.3519.18 ± 0.260.256
Data presented as mean ± standard deviation (n = 3). Asterisks (*) indicate statistical differences (p < 0.05).
Table
Table 3. Chlorophyll a and chlorophyll b of the culture in the aquaponic system over eight weeks.
Table 3. Chlorophyll a and chlorophyll b of the culture in the aquaponic system over eight weeks.
CompoundNNMNp-Value
Chlorophyll a23.29 ± 1.8825.98 ± 5.060.436
Chlorophyll b10.495 ± 0.13510.510 ± 2.1400.991
Total33.785 ± 2.01536.495 ± 7.2050.564
Data presented as mean ± standard deviation (n = 3).
Table
Table 4. Primary bacterial composition in the experimental aquaponic system. OTU analysis based on the genus level.
Table 4. Primary bacterial composition in the experimental aquaponic system. OTU analysis based on the genus level.
BacteriaNN (%)MN (%)
Nitrogen cycle-related bacteria
Aurantimicrobium [23]2.456.22
Pir4_lineage [24]2.252.20
Nitrospira [25]2.400.96
Arenimonas [26]0.432.19
SH_PL14 [4]1.101.22
Aquiluna [27]1.950.33
Cellvibrio [28]1.181.07
Pirellula [29]1.200.67
Thiobacillus [30]1.350.30
Blastopirellula [31]0.710.75
Novosphingobium [32]0.710.65
Haliangium [33]1.070.20
Chthoniobacter [34]0.440.63
Probiotics
Cetobacterium [35,36]6.896.26
Polynucleobacter [37]0.942.83
Luteolibacter [38]1.392.02
Rheinheimera [39,40]0.670.49
Jeotgalibacillus [41]0.530.51
Pathogen
Flavobacterium [42,43,44]6.4512.87
Aeromonas [45]1.125.09
Mycobacterium [46,47]1.442.12
A total of 170 genera were identified in both experiments, and only 21 genera were mentioned in the table (>0.5% of the population).
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Nuswantoro, S.; Sung, T.-Y.; Kurniawan, M.; Wu, T.-M.; Chen, B.; Hong, M.-C. Effects of Phosphate-Enriched Nutrient in the Polyculture of Nile Tilapia and Freshwater Prawn in an Aquaponic System. Fishes 2023, 8, 81. https://doi.org/10.3390/fishes8020081

AMA Style

Nuswantoro S, Sung T-Y, Kurniawan M, Wu T-M, Chen B, Hong M-C. Effects of Phosphate-Enriched Nutrient in the Polyculture of Nile Tilapia and Freshwater Prawn in an Aquaponic System. Fishes. 2023; 8(2):81. https://doi.org/10.3390/fishes8020081

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Nuswantoro, Soko, Tzu-Yuan Sung, Meki Kurniawan, Tsung-Meng Wu, Bonien Chen, and Ming-Chang Hong. 2023. "Effects of Phosphate-Enriched Nutrient in the Polyculture of Nile Tilapia and Freshwater Prawn in an Aquaponic System" Fishes 8, no. 2: 81. https://doi.org/10.3390/fishes8020081

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