Abstract
Background
The objective of the present study was to evaluate the growth performance and feed utilization of African catfish Clarias gariepinus fed a commercial diet and reared in the biofloc system enhanced with probiotic.
Methods
The treatment was the frequency of probiotic application into the cultured system, namely, 5-day interval, 10-day interval, and 15-day interval for 60 days of experiment. Biofloc culture was grown in an experiment tank (vol. 2000 L) by mixing the probiotic ( Bacillus sp.) 10 mL and molasses 200 mL per liter of water. The fish was stocked into the biofloc system 7 days after cultured at stocking density of 1000 fish tank -1. The fish was fed a commercial diet that contains 38% crude protein, twice a day at satiation. The application of probiotic was reperformed after 5 days, 10 days, and 15 days after stocking.
Results
The study showed that the growth performance, survival, and feed utilization of African catfish were higher in the treatment at 5-day intervals over 60 days. The ANOVA test showed that the application frequency of probiotic into biofloc system of cultured media had the significant effect on the growth performance, survival rate, and feed utilization of African catfish.
Conclusion
The best growth performance and feed utilization were found at the application of probiotic into biofloc system at 5-day intervals over 60 days.
Keywords: Biofloc, Probiotic Frequency, Survival Rate
Introduction
Feed is one of the important agro-inputs in aquaculture production system that contributes to approximately 40–60% of production cost 1, 2 and it has direct effect on the growth rate of the fish 3– 6. The aquaculture activity is commonly produced waste, for example, feed remains and feces which changes into ammonia and nitrite once the oxygen level is low. In the closed culture system the concentrations of ammonia (NH 3) and nitrite (NO 2) are increasing rapidly and would be toxic to organisms 7, 8.
According to Asaduzzaman et al. 9 and De Schryver et al. 10 the intensive application of commercial feed in the aquaculture causes environmental pollution and increases the possibility of the disease outbreak. Therefore, the water quality management is crucial in the aquaculture system. The objective of water quality management is to provide the comfortable environment and meet the optimum requirements for cultured organisms 11. According to Gunadi and Hafsaridewi 12 the microbial activities can be used to improve water quality and reduce the burden of contamination by fish farming waste. Therefore, the heterotrophic bacteria have promising potency to be applied in the utilization of waste ammonia in the fish culture. Beside, these bacteria are formed as a floc (clumps) in the cultures media; hence it can be used as an alternative feed source for cultured fish 13. Biofloc has abilities to suppress the toxic compounds such as ammonia and harmful bacteria (pathogenic) so that the cultured organisms grow well 14. Application of biofloc in the cultures system has been reported by several researchers, for example, in the culture of channel catfish 14, 15, in the South American catfish Rhamdia quelen 16, in Nile tilapia Oreochromis niloticus 17, 18, Farfantepenaeus brasiliensis 19, and in the cultured system of the shrimps Litopenaeus vannamei and Penaeus monodon 11, 20. However, application of biofloc on African catfish Clarias gariepinus cultures has never been reported previously.
African catfish is the popular species for aquaculture business in Southeast Asian countries 21. This species has several advantages, for example, resistance to diseases and handling stress and high growth rate 22, thus accounting for its commercial importance worldwide 23. Nowadays, the fish farmer fed a commercial diet for African catfish. The protein requirement for African catfish ranges from 25% to 40%, lipid 9.5 to 10%, carbohydrates 15 to 30%, vitamins 0.25 to 0.40%, and minerals 1.0% 1, with energy level of 2000 cal/g to 3000 cal/g 24. In addition, the application of probiotic into African catfish diet has been reported by several researchers, for example, Al-Dohail et al. 25, Ige 26, and Dennis and Uchenna 27. However, application of probiotic combing with biofloc has never been reported previously. Hence, the aim of the study was to evaluate the growth performance and feed utilization of African catfish fed experimental diet reared in the biofloc cultured system and enhanced with probiotic.
Methods
Site and time
The research was conducted from June 2016 to August 2016 at Aquaculture Technology Laboratory, Faculty of Fishery and Marine Sciences, Riau University, Indonesia. The experiments were carried out within the ethical guidelines provided by the research institution and national or international regulations.
Experimental design
The completely random design (CRD) method was used in this study. The tested treatment was the frequency of probiotics application (bacteria inoculation), namely, at 5-day interval (treatment A), 10-day interval (treatment B), and 15-day interval (treatment C). The treatment was conducted at three replications. The experimental fish was maintained in the canvas tank (vol. 2000 L) at stocking density of 1000 fishes and reared for 60 days.
Biofloc culture and feeding
The biofloc was cultured in the nine canvas tanks with a volume of 2000 L. Each tank was filled with water up to a water level of 100 cm or equivalent to 2000 L. Biofloc culture was done by mixing the probiotic ( Bacillus sp.) 10 mL and molasses 200 mL L -1 of water and then mixed into the cultures fish tanks and aerated continuously for 7 days to grow the floc.
The catfish larvae were stocked at the density of 1000 fish tank -1 with average weight 1.12±0.05 g and average total length 4.42±0.09 cm. The application of 10 mL inoculants bacteria with density of Bacillus sp. about 5×10 10 colony forming units (CFU) was performed according to respective treatment, that is, 5-day, 10-day, and 15-day intervals. The experimental catfish feed was a commercial diet with 38% crude protein, crude lipid 5%, and crude fiber 6%, mineral mix 13%, and 13% moisture contents. The fish were fed twice a day at satiation. The weight gain of fish was measured every 12 -days for 60 days.
Measured parameters
The weight gain was calculated as follows: W = Wt – Wo, where W is weight gain (g), Wt is the weight of the fish at the end of experiment (g), and Wo is the weight of fish at the start of experiment (g). The daily growth rate, survival rates, and feed utilization were calculated based on Muchlisin et al. 28, 29 The main water quality parameters such as dissolved oxygen (DO), pH, and temperature were measured using a digital water checker (YSI-550 A, ASTM, Alla, France) at 6-day intervals, while total ammonia nitrogen (TAN) was measured every 6 days using spectrophotometric method 30.
Data analysis
The data were subjective to one-way analysis of variant (ANOVA) test to determine the effect of treatment on the tested parameters and followed by Newman-Keuls multiple range test with a confidence level of 95%, while the water quality of the data was analyzed descriptively.
Results
The ANOVA test showed that the treatment had a significant effect on the weight gain (WG), specific growth rate and survival rate (SGR), feed efficiency (FE), and feed conversion ratio (FCR) (P<0.05). The study showed that the highest weight gain and specific growth rate were recorded at treatment A; these values were different significantly from other treatments. A similar trend was also found in the survival rate (SR) where the highest survival rate was recorded in treatment A, but this value was not different significantly from treatment C ( Table 1). The highest feed efficiency and lower feed conversion ratio were also found in fish with application of probiotic into biofloc system at 5-day intervals (treatment A). However, these values were not different significantly from treatment C (probiotic application at 15-day intervals). In addition, the water temperature ranges from 29.50°C to 29.62°C, dissolved oxygen rages from 3.64 mg L -1 to 3.88 mg L -1, and pH ranges from 6.93 to 7.02. In addition, the ammonia (NH 3) content ranged from 0.292 mg L -1 to 0.411 mg L -1 and nitrite content ranged from 0.08 mg L -1 to 0.09 mg L -1. Therefore, there were no significant differences regarding water quality among the treatments; however, the quality in treatment A was slightly better compared to two other treatments ( Table 2). The data showing the total length, body weight and total feed consumed by fish at every experiment can be found in Dataset 1.
Table 1. The growth performance, survival rate, and feed utilization of African catfish, Clarias gariepinus.
No | Parameter | Application frequency of probiotic | ||
---|---|---|---|---|
5-day interval | 10-day interval | 15-day interval | ||
1. | Weight gain
(g) |
125.89±1.96 b | 85.57±5.80 a | 94.19±22.81 a |
2. | SGR
(% day -1) |
7.91±0.06 b | 7.28±0.06 a | 7.34±0.40 a |
3. | Survival rate
(%) |
95.77±0.66 b | 75.23±9.70 a | 91.37±4.78 b |
4. | Efficiency of
the feed (%) |
110.86±2.60 b | 88.17±6.89 a | 90.98±5.69 a |
5. | Feed
conversion ratio |
0.90±0.02 a | 1.14±0.08 b | 1.10±0.07 b |
Table 2. The main water quality parameter of the cultured media of African catfish ( Clarias gariepinus).
Parameters | Unit | Application frequency of probiotic | ||
---|---|---|---|---|
5-day
interval |
10-day
interval |
15-day
interval |
||
Temperature | C° | 29.53±1.72 a | 29.62±1.82 a | 29.5±1.72 a |
DO | mg L -1 | 3.88±0.44 a | 3.64±0.32 a | 3.64±0.35 a |
pH | - | 7.02±0.10 a | 6.93±0.11 a | 6.97±0.09 a |
(NH 3) | mg L -1 | 0.292±0.11 a | 0.332±0.176 a | 0.411±0.195 b |
NO 2 | mg L -1 | 0.09±0.076 a | 0.08±0.036 a | 0.09±0.035 a |
Discussion
The study showed that the growth performance, survival rate, and feed utilization of African catfish were the highest in the application of probiotic into the biofloc system at 5-day intervals. This was presumably due to the fact that the applications of probiotics every 5-days can maintain the density of bacteria at suitable forms and effectively decompose organic materials well. This is indicated by lower ammonium (NH 3) content in treatment A. According to Widanarni 31 the application of biofloc into culture system can improve water quality and reduce the burden of contamination of fish culture waste in the surrounding waters. In addition Irianto 32 stated that Bacillus sp. can improve the quality of the cultured media by decomposing organic materials, suppress the growth of pathogenic, and balance the microbial and had a positive effect on fish health and growth.
Besides maintaining the water quality, biofloc is also playing an important role as alternative natural feed for cultured fish. This is because the biofloc contains crude protein that reached 48–53% 33, 34 and therefore the Feed Conversion Ratio (FCR) in treatment A was 0.90 (below 1.00) and the feed efficiency was higher than 100%. This is because of beside fed on the commercial diet the fish was also fed on floc that contain planktons. This value is better than fish fed on commercial diet without application of biofluc 33, 35, 36. According to Azim 34 the nutritional quality of biofloc was appropriate at least for herbivorous and omnivorous fish species. In this case, the African catfish is categorized as omnivorous feeding habits 35, 37.
It is clear that biofloc contributed to the growth and production of cultured organism as shown in this study. The basic principle of this technology is using the heterotrophic bacteria to manage the C: N ratio in the water media 33, 38, 39. However, biofloc not only contains the bacteria, but also is composed of other microorganisms including microalgae and zooplanktons as food for farmed fish or shrimps 33. According to Crab et al. 40 biofloc can be consumed and digested well by the shrimp and therefore possibly substitute for artificial commercial feed. Hence, application of biofloc into cultured system can increase feed efficiency up to 13% 39. For example, for feed efficiency of African catfish fed a commercial diet without biofloc was 89.83 % 33; it was increased up to 110.86% when the biofloc was applied as shown in this study.
In addition, according to Avnimelech 38, the addition of molasses as a source of carbon in aquaculture system can improve the C/N ratio waters and will further reduce inorganic nitrogen in the waters through increased growth of heterotrophic bacteria, where the heterotrophic bacteria will form a floc which can be fed by fish as feed source. Furthermore the C: N ratio of >10: 1 in the fish farming system is the optimum ratio to enhance the biofloc production and minimize the ammonia regeneration 39.
Conclusion
The application of probiotic bacteria with different frequencies in the biofloc system had the significant effect on the growth performance, survival rate, and feed utilization of African catfish ( Clarias gariepinus). The higher growth performance and best feed utilization were recorded in the application of probiotic into biofloc system at 5-day intervals.
Data availability
The data referenced by this article are under copyright with the following copyright statement: Copyright: © 2017 Putra I et al.
Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication). http://creativecommons.org/publicdomain/zero/1.0/
Dataset 1: The total length, body weight and total feed consumed by fish at every experiment. 10.5256/f1000research.12438.d174980 41
Acknowledgments
The authors thank the Ministry of Research, Technology and Higher Education of the Republic of Indonesia for supporting this study through the competitive grants scheme 2016 Contract number: 430/UN.19.5.1.3/LT/2016. The appreciation goes to all of our students who helped the authors during experiments in the laboratory.
Funding Statement
This study was supported by the Ministry of Research, Technology and Higher Education (Ristekdikti) of the Republic of Indonesia through the competitive grants scheme (Contract number: 430/UN.19.5.1.3/LT/2016).
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
[version 1; referees: 2 approved]
References
- 1. Sahwan MF: The feed fish and shrimp. Penebar Swadaya.Jakarta.1999. [Google Scholar]
- 2. Fadri S, Muchlisin Z, Sugito S: Growth performance, survival rate and feed utilization of Nile tilapia, Oreochromis niloticus fed experimental diet contains jaloh leafs, Salix tetrasperma Roxb at different levels of EM-4 probiotic. Jurnal Ilmiah Mahasiswa Kelautan dan Perikanan Unsyiah. 2016;1(2):210–221. [Google Scholar]
- 3. Muchlisin ZA, Hashim R, Chong AS: Preliminary study on the cryopreservation of tropical bagrid catfish ( Mystus nemurus) spermatozoa; The effect of extender and cryoprotectant on the motility after short-term storage. Theriogenology. 2004;62(1–2): 25–34. 10.1016/j.theriogenology.2003.05.006 [DOI] [PubMed] [Google Scholar]
- 4. Muhammadar AA, Mazlan AG, Samat A, et al. : Growth, survival and feed conversion of juvenile tiger grouper Epinephelus fuscoguttatus in different salinity regimes. AACL Bioflux. 2014;7(4):241–247. Reference Source [Google Scholar]
- 5. Karina S, Akbar M, Supriatna A, et al. : Replacement of soybean meal with Moringa oleifera leaf meal in the formulated diets of tilapia ( Oreochromis niloticus) fingerlings. AACL Bioflux. 2015;8(5):790–795. Reference Source [Google Scholar]
- 6. Putra DF, Fanni M, Muchlisin ZA, et al. : Growth performance and survival rate of climbing perch (Anabas testudineus) fed Daphnia sp. enriched with manure, coconut dregs flour and soybean meal. AACL Bioflux. 2016;9(5):944–948. Reference Source [Google Scholar]
- 7. Sidik AS, Sarwono, Agustina: The effect of stocking density on nitrification rate in a closed recirculating culture system. Jurnal Akuakultur Indonesia. 2002;1(2):47–51. 10.19027/jai.1.47-52 [DOI] [Google Scholar]
- 8. Sakala ME, Musuka CG: The effect of ammonia on growth and survival rate of tilapia rendalli in quail manured tanks. Int J Aquac. 2014;22(4):1–6. 10.5376/ija.2014.04.0022 [DOI] [Google Scholar]
- 9. Asaduzzaman M, Wahab MA, Verdegem MC, et al. : C/N ratio control and substrate addition for periphyton development jointly enhance freshwater prawn Macrobrachium rosenbergii production in ponds. Aquaculture. 2008;280(1–4):117–123. 10.1016/j.aquaculture.2008.04.019 [DOI] [Google Scholar]
- 10. De Schryver P, Crab R, Defoirdt T, et al. : The basics of bio-flocs technology: The added value for aquaculture. Aquaculture. 2008;277(3–4):125–137. 10.1016/j.aquaculture.2008.02.019 [DOI] [Google Scholar]
- 11. Nurhatijah N, Muchlisin ZA, Sarong MA, et al. : Application of biofloc to maintain the water quality in culture system of the tiger prawn ( Penaeus monodon). AACL Bioflux. 2016;9(4):923–928. Reference Source [Google Scholar]
- 12. Gunadi B, Hafsaridewi R: Waste utilization aquaculture of catfish ( clarias gariepenus) intensive maintenance system with heterotrophic for tilapia. Final Report of Research Activity in 2007. Research and Technology for Freshwater Aquaculture Stattion Sukamandi.2007. [Google Scholar]
- 13. Crab R, Avnimelech Y, Defoirdt T, et al. : Nitrogen removal techniques in aquaculture for a sustainable production. Aquaculture. 2007;270(1–4):1–14. 10.1016/j.aquaculture.2007.05.006 [DOI] [Google Scholar]
- 14. Schrader KK, Green BW, Perschbacher PW: Development of phytoplankton communities and common off-flavors in a biofloc technology system used for the culture of channel catfish ( Ictalurus punctatus). Aquacult Eng. 2011;45(3):118–126. 10.1016/j.aquaeng.2011.08.004 [DOI] [Google Scholar]
- 15. Green BW, Schrader KK, Perschbacher PW: Effect of stocking biomass on solids, phytoplankton communities, common off-flavors, and production parameters in a channel catfish biofloc technology production system. Aquac Res. 2014;45(9):1442–1458. 10.1111/are.12096 [DOI] [Google Scholar]
- 16. Poli MA, Schveitzer R, De Oliveira Nuñer AP: The use of biofloc technology in a South American catfish ( Rhamdia quelen) hatchery: Effect of suspended solids in the performance of larvae. Aquac Eng. 2015;66:17–21. 10.1016/j.aquaeng.2015.01.004 [DOI] [Google Scholar]
- 17. Ekasari J, Zairin M, Putri DU, et al. : Biofloc-based reproductive performance of Nile tilapia Oreochromis niloticus L. broodstock. Aquac Res. 2015;46(2):509–512. 10.1111/are.12185 [DOI] [Google Scholar]
- 18. Emerenciano M, Ballester EL, Cavalli RO, et al. : Biofloc technology application as a food source in a limited water exchange nursery system for pink shrimp Farfantepenaeus brasiliensis (Latreille, 1817). Aquac Res. 2012;43(3):447–457. 10.1111/j.1365-2109.2011.02848.x [DOI] [Google Scholar]
- 19. Souza DM, Suita SM, Romano LA, et al. : Use of molasses as a carbon source during the nursery rearing of Farfantepenaeus brasiliensis (Latreille, 1817) in a biofloc technology system. Aquac Res. 2014;45(2):270–277. 10.1111/j.1365-2109.2012.03223.x [DOI] [Google Scholar]
- 20. Furtado PS, Gaona CA, Poersch LH, et al. : Application of different doses of calcium hydroxide in the farming shrimp Litopenaeus vannamei with the biofloc technology (BFT). Aquacult Int. 2014;22(3):1009–1023. 10.1007/s10499-013-9723-9 [DOI] [Google Scholar]
- 21. Muchlisin ZA, Nadiya N, Nadiah WN, et al. : Preliminary study on the natural extenders for artificial breeding of African catfish Clarias gariepinus (Burchell, 1822). AACL Bioflux. 2010;3(2):119–124. Reference Source [Google Scholar]
- 22. El Naggar GO, John G, Rezk MA, et al. : Effect of varying density and water level on the spawning response of African catfish Clarias gariepinus: implications for seed production. Aquaculture. 2006;261(3):904–907. 10.1016/j.aquaculture.2006.07.043 [DOI] [Google Scholar]
- 23. Muchlisin ZA, Nadiah WN, Nadiya N, et al. : Exploration of natural cryoprotectants for cryopreservation of African catfish, Clarias gariepinus, Burchell 1822 (Pisces: Clariidae) spermatozoa. Czech J Anim Sci. 2015;60(1):10–15. 10.17221/7906-CJAS [DOI] [Google Scholar]
- 24. Suhendra N: Grouth performance of working catfish Clarias batracus fed an experimental diet with varying levels of protein and energy. Buletin Penelitian Perikanan Darat. 1988;7(2):16–23. [Google Scholar]
- 25. Al-Dohail MA, Hashim R, Aliyu-Paiko M: Effects of the probiotic, Lactobacillus acidophilus, on the growth performance, haematology parameters and immunoglobulin concentration in African catfish (Clarias gariepinus, Burchell 1822) fingerling. Aquac Res. 2009;40(14):1642–1652. 10.1111/j.1365-2109.2009.02265.x [DOI] [Google Scholar]
- 26. Ige BA: Probiotics use in intensive fish farming. Afr J Mic Res. 2013;7(22):2701–2711. 10.5897/AJMR12x.021 [DOI] [Google Scholar]
- 27. Dennis EU, Uchenna OJ: Use of probiotics as first feed of larval African catfish Clarias gariepinus (Burchell 1822). Annu Res Rev Biol. 2016;9(2):1–9. 10.9734/ARRB/2016/23537 [DOI] [Google Scholar]
- 28. Muchlisin ZA, Arisa AA, Muhammadar AA, et al. : Growth performance and feed utilization of keureling ( Tor tambra) fingerlings fed a formulated diet with different doses of vitamin E (alpha-tocopherol). Arch Pol Fish. 2016;23:47–52. 10.1515/aopf-2016-0005 [DOI] [Google Scholar]
- 29. Muchlisin ZA, Afrido F, Murda T, et al. : The effectiveness of experimental diet with varying levels of papain on the growth performance, survival rate and feed utilization of keureling fish ( Tor tambra). Biosaintifika. 2016;8(2):172–177. 10.15294/biosaintifika.v8i2.5777 [DOI] [Google Scholar]
- 30. Eaton AD, Clesceri LS, Rice EW, et al. : Standard methods for the examination of water and wastewater. 21 stedition. American Public Health Association, American Water Works Association, Water Environment Federation. Washington, DC.2005. Reference Source [Google Scholar]
- 31. Widanarni, Ekasari J, Maryam S: Evaluation of biofloc technology application on water quality and production performance of red tilapia Oreochromis sp. cultured at different stocking densities. Hayati. 2012;19(2):73–80. 10.4308/hjb.19.2.73 [DOI] [Google Scholar]
- 32. Irianto A: Probiotic for aquaculture. Gadjah Mada University Press, Yogyakarta.2003. [Google Scholar]
- 33. Hastuti S, Subandiyono S: Production performance African catfish ( Clarias gariepinus, Burch) is maintained biofloc technology. Fisheries SANTEK Journal. 2014;10(1):37–42. Reference Source [Google Scholar]
- 34. Azim ME, Little D, North B: Growth and welfare of Nile tilapia ( Oreochromis niloticus) cultured indoor tank using biofloc technology (BFT). Procedings of Aquaculture Conference 2007, 26 February -3 March 2007. San Antonio, Texas, USA.2007. [Google Scholar]
- 35. Marimuthu K, Ang CC, Muralikrishnan S, et al. : Effect of different feeding frequency on the growth and survival of African catfish ( Clarias Gariepinus) fingerlings. Adv Environ Biol. 2010;4(2):187–193. Reference Source [Google Scholar]
- 36. Jimoh WA, Fagbenro OA, Adeparusi EO: Response of African catfish, Clarias gariepinus (Burchell 1822), fingerlings fed diets containing differently timed wet-heat-treated sesame ( Sesamum indicum) seedmeal. Agric Sci. 2014;5:1159–1171. 10.4236/as.2014.512126 [DOI] [Google Scholar]
- 37. Rad F, Kurt GI, Bozaoủlu AS: Effects of spatially localized and dispersed patterns of feed distribution on the growth, size dispersion and feed conversion ratio of the African Catfish ( Clarias gariepinus). Turk J Vet Anim Sci. 2003;28:851–856. Reference Source [Google Scholar]
- 38. Avnimelech Y: Carbon/nitrogen ratio as a control element in aquaculture systems. Aquaculture. 1999;176(3–4):227–235. 10.1016/S0044-8486(99)00085-X [DOI] [Google Scholar]
- 39. Hargreaves JA: Photosynthetic suspended-growth systems in aquaculture. Aquaculture Engineering. 2006;34(3):344–363. 10.1016/j.aquaeng.2005.08.009 [DOI] [Google Scholar]
- 40. Crab R, Chielens B, Wille M, et al. : The effect of different carbon sources on the nutritional value of bioflocs, a feed for Macrobrachium rosenbergii postlarvae. Aquac Res. 2010;41(4):559–567. 10.1111/j.1365-2109.2009.02353.x [DOI] [Google Scholar]
- 41. Putra I, Rusliadi R, Fauzi M, et al. : Dataset 1 in: Growth performance and feed utilization of African catfish Clarias gariepinus fed a commercial diet reared in the biofloc system enhanced with probiotic. F1000Research. 2017. Data Source [DOI] [PMC free article] [PubMed] [Google Scholar]