Subscribe Now Subscribe Today
Research Article
 

Nitrogen and Phosphorus Waste Production from Different Fish Species Cultured at Floating Net Cages in Lake Maninjau, Indonesia



Hafrijal Syandri, Azrita and Ainul Mardiah
 
Facebook Twitter Digg Reddit Linkedin StumbleUpon E-mail
ABSTRACT

Background and Objective: Aquaculture operations that use floating net cages have become one of the primary mean of intensive fish-culture in Lake Maninjau. The fish-culture species studied were Cyprinus carpio (C. carpio) (T1), Oreochromis niloticus (O. niloticus) (T2), Osphronemus goramy (O. goramy) (T3) and Clarias gariepinus (C. gariepinus) (T4). The objective of the research was to estimate the nitrogen (N) and phosphorus (P) loads into Lake Maninjau. Materials and Methods: The capacity of floating net cages was approximately 32 m3 (4×4×2 m) with densities of 32 fish m–3 in triplicate groups. Approximately 1,500 kg of feed was used in each cage during the experiment. The difference of N and P loads from different fish species were analyzed using one-way ANOVA (SPSS 16.0) computer software. Results: The total N loads into the water bodies from T1, T2, T3 and T4 were estimated at 37.93±2.59, 49.90±5.17, 45.90±4.18 and 20.35±4.12 kg t–1 of fish production, respectively. The P load was estimated to be 18.30±0.12, 20.01±0.99, 22.60±0.80 and 13.93±1.47 kg t–1 of fish production, respectively. Every ton of feed consumed by each fish species will contribute as much as 38.26±2.55, 35.68±1.69, 32.12± 0.39 and 48.99±2.35 kg N load into the water bodies, respectively. The P load was 11.45±2.43, 9.11±0.21, 8.34±0.04 and 12.51±0.30 kg, respectively. Conclusion: The C. gariepinus species is preferred for aquaculture operations at Lake Maninjau, because it minimizes N and P load releases into water bodies which can maintain sustainable aquaculture operations.

Services
Related Articles in ASCI
Similar Articles in this Journal
Search in Google Scholar
View Citation
Report Citation

 
  How to cite this article:

Hafrijal Syandri, Azrita and Ainul Mardiah, 2018. Nitrogen and Phosphorus Waste Production from Different Fish Species Cultured at Floating Net Cages in Lake Maninjau, Indonesia. Asian Journal of Scientific Research, 11: 287-294.

DOI: 10.3923/ajsr.2018.287.294

URL: https://scialert.net/abstract/?doi=ajsr.2018.287.294
 
Received: August 28, 2017; Accepted: November 16, 2017; Published: March 15, 2018


Copyright: © 2018. This is an open access article distributed under the terms of the creative commons attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.

INTRODUCTION

The high levels of nutrients and suspended solids released into water bodies from aquaculture operations is one of the major environmental problems causing water pollution1-5. Intensive aquaculture operations can result in the release of dissolved organic and inorganic nutrients, such as nitrogen (N) and phosphorus (P)6-8. N and P levels from intensive aquaculture operations can cause or accelerate eutrophication in natural water systems9-11. In addition, N and P levels released into water bodies depend on diet composition12,13, type of feed10, fish species14, feed conversion ratio15, stocking densities, feed quality16, fish mass mortality17 and the local environment18. Lazzari and Baldisserotto19 state that N and P are the primary end products of fish loading, which has had an effect on fish rearing waters and the environment.

Aquaculture around the world has grown at a rapid rate in recent years, including in Indonesia20,21. Medium and large scale freshwater aquaculture operations in Indonesia were conducted in the lake, reservoir and river21-23. Fish-cultured species in this location were Cyprinus carpio, Oreochromis niloticus, Osphronemus goramy, Hemibagrus nemerus, Clarias gariepinus, Pangasius spp. and Leptobarbus hoevenii20,24,25.

Lake Maninjau is tecto-volcanic with a surface area of 99.5 km2, both features that serve very important roles to many Indonesians for aquaculture operations of the O. niloticus and C. carpio in floating net cages8,22. Total number of floating net cages in the years of 2013, 2014 and 2015 are 16,120, 16,580 and 20,608 U, respectively8,22,24.

In the past decade, the water quality of Lake Maninjau has been decreasing due to the loading of organic matter from aquaculture operations of C. carpio and O.niloticus22,26. However, upwelling that has occured at Lake Maninjau every year has caused a lack of oxygen in the water which is a result of mass fish mortality16. Furthermore, since the year 2014, aquaculture operations of O. goramy and C. gariepinus have been successful in floating net cages. Both species were resistant to poor water quality and had a wide market in Indonesia, because they are favored by consumers. These species also have high prices and a high demand in the market.

The aim of the study was to estimate the quantitative, values of N and P loads released from each species cultured in floating net cages on Lake Maninjau. The results of this study were used to increase the scientific understanding of the effects of N and P load releases of different fish species into the water at Lake Maninjau.

MATERIALS AND METHODS

Study area: The experiment was conducted in Lake Maninjau of West Sumatera Province, Indonesia. The geographical position is S:00°12'26.63"-S:00°25'02.80" and E:100°07'43.74"-E:100°16'22.48" and it is located at an altitude of 461.50 m above sea level24. Based on the Schmidth Ferguson climate classification, Lake Maninjau has characteristics of climate types A and an annual rainfall of 3,490 mm.

In this study, the C. carpio, O. niloticus, O. goramy and C. gariepinus fingerlings were designated T1, T2, T3 and T4, respectively. All species were collected from a private hatchery in the Luak District, Lima Puluh Kota Regency, West Sumatera Province. The fingerlings were transferred by truck to the Research Center of the Faculty of Fisheries and Marine Science, Bung Hatta University near the Lake Maninjau. Each fish species was treated with a prophylactic formalin bath (100 mg L–1) for 1 h to remove external parasites and acclimatized in a floating net cage (4×4×2 m) for 1 month prior to the experiment. The average initial weight of the T1, T2, T3 and T4 fingerlings were 56.79±4.45, 53.08±1.60, 55.33±1.14 and 51.18±1.59 g, respectively.

This study was conducted between March, 2017 and June, 2017 (100 days). All species were cultured in the floating net cages. Each floating net cage had a capacity of approximately 32 m3 (4×4×2 m) and was constructed using a 10 mm mesh size sieve. The fingerlings were fed by a commercial feed (pelleted) with drowned type during 100 days of the experiment. The approximate composition of the feed was 12% moisture content, 29% crude protein, 6% crude lipid, 12% crude fiber and 6% crude ash.

The stocking density was 130 fish m–3 (4,160 fish/cage). There were 3 replicates for each fish species in each experiment. During the experiment, 1,500 kg of feed was used. The fish were fed daily at a rate of 4% of their biomass at 9:00, 14:00 and 18:00. All fish mortalities were removed and weighed daily. Fish mortality was replaced in each treatment. The amount of feed provided was adjusted according to temporal changes of biomass and growth of fish in the floating net cages.

Measurements parameters: To determine the growth performance of the fish, the following parameters were calculated based on Aryani et al.27:

and

Water quality: The water transparency was measured with a Secchi disc. The water samples were collected at a depth of 10 cm from each floating net cage to determine the dissolved oxygen (DO) levels. An oxygen meter (YSI model 52, Yellow Spring Instrument Co., Yellow Springs, OH, USA) was used in situ and pH values were determined using a pH meter (Digital Mini-pH Meter, 0-14 pH, IQ Scientific, Chemo-science [Thailand]) Co., Ltd, Thailand). Water temperature was measured using a thermometer (Celsius scale). The levels of alkalinity and hardness of the water in each replication were measured according to standard procedures27. The water quality parameters were measured once every month.

Analytical methods: Nitrogen (N) concentrations (as % of dry weight) of feed and fish were determined by standard methods of the Association of Official Analytical Chemists28. The P concentrations were determined using a spectrophotometer (UV 160 A, Japan) and the molybdate-ascorbic acid method indicated by the Association of Official Analytical Chemists28 at the Chemistry Laboratory of the University of Bung Hatta Padang, Indonesia. The results were expressed as absorbance at 400 mm. All samples were performed in triplicate.

Estimation of N and P loads: The levels of N and P loads from fish-culture was estimated according to Ackefors and Enell29. The following parameters were analyzed according to the formulas given below:

N load (kg of N) = [(Feed×FeedN)-(Fish×FishN)]

P load (kg of P) = [(Feed×FeedP)-(Fish x FishP)]

where, Feed is total feed used during the experiment, Fish is wet weight of fish produced per harvested, FeedN is N content of feed. FeedP is P content of feed (expressed as % of dry weight). FishN is N content of fish and FishP= P content of fish (expressed as % of wet weight).

N and P loads from the production of 1 t of fish = (1 t feed×FCR ×FeedN and P content)-(1 t fish×FishN and P content)

Statistical analysis: The mean values for final weight, feed conversion ratio, mortality parameters of different treatments and monthly variations of water quality parameters, were subjected to a one-way ANOVA test followed by Duncan’s new multiple range test30. All statistical analyses were performed using SPSS software (version 16.0 for Windows, SPSS Inc., Chicago, IL). The standard deviation of each parameter and treatment was determined and expressed as the Mean±SD. The treatment effects were considered to be significant at p<0.05.

RESULTS

The results for certain growth parameters, FCR, mortality and chemical analyses, from each feed and fish species are presented in Table 1. The difference in fish species has a significant (p<0.05) effect on the final mean weight, FCR and mortality. The N and P content of the feed were 5.52±0.29 and 1.41±0.03%, respectively. The N and P content of each fish species is presented in Table 1. Monthly variations in the water quality parameter in Lake Maninjau are as indicated in Table 2. There was no significant difference in the water transparency, water temperature, dissolved oxygen, pH, alkalinity or hardness values for months of March, April, May and June, of 2017.

Table 1:Growth parameters and chemical analysis of different fish species
Values are Mean±SD, *Values in the same row with a different superscript are significantly different (p<0.05), T1: C. carpio, T2: O. niloticus, T3: O. goramy and T4: C. gariepinus

Table 2:Monthly variations in physicochemical and water quality parameters
*Values in the same row with the same superscript are not significantly different (p>0.05)

Fig. 1:Nitrogen and phosphorus loads from the production of 1 t of fish in Lake Maninjau

Table 3 presented the summaries of the mass balance of N and P content from four fish species, while Fig. 1 and 2 provide an estimation of N and P loads from the production of 1 t of fish and 1 t of feed consumption.

DISCUSSION

The present study was conducted to report the N and P loads introduced by floating net-cages in Lake Maninjau.

Fig. 2:Nitrogen and phosphorus loads released into Lake Maninjau from 1 t of feed consumption

These results indicated that species T4 had a better growth rate compared to those of T1, T2 and T3. The differences in growth rate might be due to the specific growth rate of each fish species. The specific growth rates (SGR, % day–1) for T1, T2, T3 and T4 used with the feeding rate of 4% were 1.16, 1.19, 0.98 and 1.52, respectively. Numerous studies elsewhere have shown that the specific growth rate (SGR) of each species of fish is different. The SGRs (% day–1) are 1.63 for C.carpio31, 2.14 for O. niloticus32, 2.47 for C.gariepinus33 and 1.66 for O. goramy34.

Table 3: Mass balance of nitrogen (N) and phosphorus (P) of different fish species
Data are presented as the (Mean±SD) of triplicate samples, *The difference between means with different lower case letters in a column and the difference between means with different capitalized letters for each parameter (N, P) are statistically significant (p<0.05), T1: C. carpio, T2: O. niloticus, T3: O. goramy and T4: C. gariepinus

In this study, the water quality in each floating net cage during the months of March, April, May and June showed no significant differences. The growth of the fish species depends not only the water quality35-38 but also on the fish species39,40. Although each fish species used the drowned feed type with a feeding rate of 4%, the feed conversion ratio (FCR) for each species was significantly different (p<0.05) (Table 1). The FCR is usually used to estimate the efficiency of converting feed into body mass. In this study, the lowest FCR value was observed in T4 (1.13), while the highest was observed in T3 (1.69). The differences among the FCR values are caused by differences in fish species (T1, T2, T3 and T4) and possibly also by food habits. Conversely, a lower FCR value indicated that the efficiency of feed utilization was better. An FCR value that is less than 2.0 or very close to 2.0 is considered "good" in the aquaculture industry41. In contrast, the FCR for Tilapia fish cages in Lake Malawi are between 2.1 and 3.9 and FCR values tended to be higher in recent production cycles. Production cycles during the study period were on average (±SE), 376±9 days long14.

Negative environmental impacts of cage aquaculture operations have been reported in many parts of the world20,42-46. In this study, the difference in fish species has a significant effect (p<0.05) on the mass balance of N and P (Table 3). N and P retention (kg) was significantly higher in T4 compared to that of T1, followed by T3 and T2, while N and P load (kg) was significantly higher for T2 compared to that of T1, T3 and T4. Although the same feed was applied at an equal ratio, the mass balance of N and P differed significantly among all fish species. The reason for this difference might be due to the differences in FCR for each species and there was less difference in genetic improvement for feed consumption. The N loads in T1, T2, T3 and T4 were 47.60, 58.34, 49.94 and 33.46%, respectively, while the P loads in T1, T2, T3 and T4 were 90.62, 91.83, 94.60 and 81.77%, respectively. For Oreochromis karongae and O. shiranus in Lake Malawi, N loads were 59 and 80%, respectively and P loads were 85 and 92%, respectively14. In addition, for Rainbow Trout (Oncorhynchus mykiss) in the Kesikköprü Dam Lake, N loads were 54.37% and P loads were 70.00%10. According to Yogev et al.47 fish only use 20-30% of the N in feed and 50% of P in feed, while the remainder is released into the water.

In this study, total N and P load releases into water bodies were different for each ton of fish production in T1 (37.93±2.59 and 18.30±0.12), T2 (49.90±5.17 and 20.01±0.99), T3 (45.90±4.18 and 22.60±0.80) and T4 (20.35±4.12 and 13093±1.47) kg t–1, respectively (Fig. 1). These differences could be caused by the FCR and the N and P content of feed and fish. There was a strong linear relationship between FCR and N (r2 = 0.87) and P (r2 = 0.99) loads for the floating net cages. In comparison other values in the literature, show that N released into water bodies (t–1 of live-weight fish) for Tilapia, Black Pacu and Trout were 34.7, 25.8 and 66.1 kg, respectively. Alternatively, the P was 3.0, 9.7 and 9.6 kg, respectively43. Other research found that 56.0 kg of N and 10.66 kg P were released for Trout10 and 64.0 kg of N and 4.6 kg of P were released for Tilapia47. The N loading values also varied considerably with fish species with Rainbow trout having the lowest values of 47.3-124.2 kg t–1, while values given by other fishes ranged from 103.5-320.6 kg t–1 15.

In this study, total N and P load releases into water bodies were different for each ton of feed consumed by T1, T2, T3 and T4 (Fig. 2). This difference is also caused by FCR and feed composition. The FCRs for T1, T2, T3 and T4 were 1.44±0.02, 1.55±0.03, 1.69±0.03 and 1.13±0.10, respectively. There was a strong linear relationship between FCR and N (r2 = 0.99) and P (r2 = 0.87) loads for the floating net cages. The N and P levels in the feed used and the FCRs in the farms directly affected N and P loads for each ton of pelleted feed used. Every ton of feed consumed by each fish species (T1, T2, T3 and T4 will contributes N loads as much as 38.26±2.55, 35.68±1.69, 32.12±0.39, 48.99±2.35 and P loads as much as 11.45±2.43, 9.11±0.21, 8.34±0.04 and 12.51±0.30 into Lake Maninjau. Furthermore, releases of N and P t–1 into the Kesikköprü Dam Lake for Oncorhynchus mykiss were 44.78 and 8.60 kg, respectively10. The feed composition and feed conversion of aquaculture operations primarily had a negative effect on the environment. In addition, the aquaculture integrated model, recirculating aquaculture systems, site selection, feeding rate, size of the farm and species of cultivated fish should also be considered important factors32,43,45,47,48.

CONCLUSION

The present study observed clear evidence that different species of fish-cultured in floating net cages can release different levels of total N and P into water bodies of Lake Maninjau. The estimated N and P loads from the production of 1 t of fish were significantly lower for Clarias gariepinus compared to those for O. goramy, C. carpio and O. nilaticus while the estimated N and P loads from 1 t of feed consumption were significantly lower for O. goramy compared to other species. Based on the research, the appropriate species cultured in Lake Maninjau was C. Gariepinus because this species had low N and P loads into water bodies. Alternatively, N and P loads can be reduced by adjusting the stocking densities and feed regime timing of C. gariepinus. This approach will help to reduce the downstream negative effects on the lake and in turn positively affect the water quality.

SIGNIFICANCE STATEMENTS

This study analyzes the different levels of N and P load releases into water bodies of Maninjau Lake from each fish-culture species. The N and P loads were significantly lower for Clarias gariepinus compared to other fish species. Fish-culture of Clarias gariepinus in Lake Maninjau is an important consideration for fish farmers and authorities in the future due to the lower N and P load releases into water bodies of Lake Maninjau. This fish species is also resistant to poor water quality, has a higher growth rate and is favored by consumers.

ACKNOWLEDGMENTS

This study was funded by a study grant (Riset Unggulan Perguruan Tinggi) from the Directorate of Research and Community Service of the Ministry of Research Technology and Higher Education, Republic of Indonesia (No. SP.DIPA-042.06-0/2017).

REFERENCES
1:  Rosa, R.D.S., A.C.F. Aguiar, I.G. Boechat and B. Gucker, 2013. Impacts of fish farm pollution on ecosystem structure and function of tropical headwater streams. Environ. Pollut., 174: 204-213.
CrossRef  |  Direct Link  |  

2:  Zhu, Z.M., X.T. Lin, J.X. Pan and Z.N. Xu, 2014. Effect of cyclical feeding on compensatory growth, nitrogen and phosphorus budgets in juvenile Litopenaeus vannamei. Aquacult. Res., 47: 283-289.
CrossRef  |  Direct Link  |  

3:  Maccoux, M.J., A. Dove, S.M. Backus and D.M. Dolan, 2016. Total and soluble reactive phosphorus loadings to Lake Erie: A detailed accounting by year, basin, country and tributary. J. Great Lakes Res., 42: 1151-1165.
CrossRef  |  Direct Link  |  

4:  Prathumchai, N., C. Polprasert and A.J. Englande, 2016. Phosphorus leakage from fisheries sector-A case study in Thailand. Environ. Pollut., 219: 967-975.
CrossRef  |  Direct Link  |  

5:  Horppila, J., H. Holmroos, J. Niemisto, I. Massa and N. Nygren et al., 2017. Variations of internal phosphorus loading and water quality in a Hypertrophic lake during 40 years of different management efforts. Ecol. Eng., 103: 264-272.
CrossRef  |  Direct Link  |  

6:  Qing-Jun, M., F. Qi-Yan, W. Qing-Qing, M. Lei and C. Zhi-Yang, 2009. Distribution characteristics of nitrogen and phosphorus in mining induced subsidence wetland in Panbei coal mine, China. Proc. Earth Planet. Sci., 1: 1237-1241.
CrossRef  |  Direct Link  |  

7:  Kawasaki, N., M.R.M. Kushairi, N. Nagao, F. Yusoff, A. Imai and A. Kohzu, 2016. Release of nitrogen and phosphorus from aquaculture farms to Selangor River, Malaysia. Int. J. Environ. Sci. Dev., 7: 113-116.
Direct Link  |  

8:  Syandri, H., Elfiondri, Junaidi and Azrita, 2015. Social status of the fish-farmers of floating-net-cages in lake Maninjau, Indonesia. J. Aquacult. Res. Dev., Vol. 7. 10.4172/2155-9546.1000391

9:  Cao, L., W.M. Wang, Y. Yang, C.T. Yang, Z.H. Yuan, S.B. Xiong and J. Diana, 2007. Environmental impact of aquaculture and countermeasures to aquaculture pollution in China. Environ. Sci. Pollut. Res., 14: 452-462.
PubMed  |  

10:  Asir, U. and S. Pulatsu, 2008. Estimation of the nitrogen-phosphorus load caused by rainbow trout (Oncorhynchus mykiss Walbaum, 1792) Cage-Culture farms in Kesikkopru Dam Lake: A comparison of pelleted and extruded feed. Turk. J. Vet. Anim. Sci., 32: 417-422.
Direct Link  |  

11:  Lepori, F and J.J. Roberts, 2017. Effects of internal phosphorus loadings and food-web structure on the recovery of a deep lake from eutrophication. J. Great Lakes Res., 43: 255-264.
CrossRef  |  Direct Link  |  

12:  Abou, Y., A. Saidou, D. Mama, E.D. Fiogbe and J.C. Micha, 2012. Evaluation of nitrogen and phosphorus wastes produced by Nile tilapia (Oreochromis niloticus L.) fed Azolla-diets in earthen ponds. J. Environ. Protect., 3: 502-507.
CrossRef  |  Direct Link  |  

13:  Boyd, C.E., C.S. Tucker and B. Somridhivej, 2016. Alkalinity and hardness: Critical but elusive concepts in aquaculture. J. World Aquacult. Soc., 47: 6-41.
CrossRef  |  Direct Link  |  

14:  Gondwe, M.J.S., S.J. Guildford and R.E. Hecky, 2011. Carbon, nitrogen and phosphorus loadings from tilapia fish cages in Lake Malawi and factors influencing their magnitude. J. Great Lakes Res., 37: 93-101.
CrossRef  |  Direct Link  |  

15:  Islam, M.S., 2005. Nitrogen and phosphorus budget in coastal and marine cage aquaculture and impacts of effluent loading on ecosystem: Review and analysis towards model development. Mar. Pollut. Bull., 50: 48-61.
CrossRef  |  Direct Link  |  

16:  Herbeck, L.S., D. Unger, Y. Wu and T.C. Jennerjahn, 2013. Effluent, nutrient and organic matter export from shrimp and fish ponds causing eutrophication in coastal and back-reef waters of NE Hainan, tropical China. Continental Shelf Res., 57: 92-104.
CrossRef  |  Direct Link  |  

17:  Syandri, H., Azrita, Junaidi and A. Mardiah, 2017. Levels of available nitrogen-phosphorus before and after fish mass mortality in Maninjau Lake of Indonesia. J. Fish. Aquat. Sci., 12: 191-196.
CrossRef  |  Direct Link  |  

18:  Carroll, M.L., S. Coahrane, R. Fieler, R. Velvin and P. White, 2003. Organic enrichment of sediments from salmon farming in Norway: Environmental factors, management practices and monitoring techniques. Aquaculture, 226: 165-180.
CrossRef  |  Direct Link  |  

19:  Lazzari, R. and B. Baldisserotto, 2008. Nitrogen and phosphorus waste in fish farming. Bolet. Inst. Pesca, 34: 591-600.
Direct Link  |  

20:  Henriksson, P.J.G., N. Tran, C.V. Mohan, C.Y. Chan and U.P. Rodriguez et al., 2017. Indonesian aquaculture futures-evaluating environmental and socioeconomic potentials and limitations. J. Cleaner Prod., 162: 1482-1490.
CrossRef  |  Direct Link  |  

21:  Tran, N., U.P. Rodriguez, C.Y. Chan, M.J. Phillips and C.V. Mohan et al., 2017. Indonesian aquaculture futures: An analysis of fish supply and demand in Indonesia to 2030 and role of aquaculture using the Asia Fish model. Mar. Policy, 79: 25-32.
CrossRef  |  Direct Link  |  

22:  Syandri, H., Azrita and Niagara, 2016. Trophic status and load capacity of water pollution waste fish-culture with floating net cages in Maninjau lake, Indonesia. Ecol. Environ. Conserv., 22: 459-466.
Direct Link  |  

23:  Rahman, M., 2013. Revitalization of fish cage aquaculture management in Riam Kanan stream of Kalimantan Selatan Province-Indonesia. Jurnal Iktiologi Indonesia, 13: 197-203.

24:  Syandri, H., Junaidi, Azrita and T. Yunus, 2014. State of aquatic resources Maninjau lake West Sumatra province, Indonesia. J. Ecol. Environ. Sci., 5: 109-113.
Direct Link  |  

25:  Suhenda, N., R. Samsudin and E. Nugroho, 2010. [Growth of green catfish (Hemibagrus nemurus) fry in floating net cage feed by artificial food with different protein content]. Jurnal Iktiologi Indonesia, 10: 65-71.
Direct Link  |  

26:  Junaidi, H. Syandri and Azrita, 2014. Loading and distribution of organic materials in Maninjau lake West Sumatra province-Indonesia. J. Aquacult. Res. Dev., Vol. 5. 10.4172/2155-9546.1000278

27:  Aryani, N., Azrita, A. Mardiah and H. Syandri, 2017. Influence of feeding rate on the growth, feed efficiency and carcass composition of the giant gourami (Osphronemus goramy). Pak. J. Zool., 49: 1775-1781.
Direct Link  |  

28:  APHA., 1995. Standard Methods for Examination of Water and Wastewater. 19th Edn., American Public Health Association, Washington DC., USA.

29:  AOAC., 1990. Official Methods of Analysis. 13th Edn., Association of Official Analytical Chemists, Washington, DC., USA.

30:  Ackefors, H. and M. Enell, 1990. Discharge of nutrients from Swedish fish farming to adjacent sea areas. Ambio, 19: 28-35.
Direct Link  |  

31:  Duncan, D.B., 1955. Multiple range and multiple F tests. Biometrics, 11: 1-42.
CrossRef  |  Direct Link  |  

32:  Ahmed, A.R., A.J. Moody, A. Fisher and S.J. Davies, 2013. Growth performance and starch utilization in common carp (Cyprinus carpio L.) in response to dietary chromium chloride supplementation. J. Trace Elem. Med. Biol., 27: 45-51.
CrossRef  |  Direct Link  |  

33:  Skov, P.V., C.P. Duodu and D. Adjei-Boateng, 2017. The influence of ration size on energetics and nitrogen retention in tilapia (Oreochromis niloticus). Aquaculture, 473: 121-127.
CrossRef  |  Direct Link  |  

34:  Widyantoro, W., Sarjito and D. Harwanto, 2014. The effect of fasting time on the growth and bloods profile of catfish (Clarias gariepinus) in the recirculating system. J. Aquacult. Manage. Technol., 2: 103-108.

35:  Mukai, Y. and L.S. Lim, 2011. Larval rearing and feeding behavior of African catfish, Clarias gariepinus under dark conditions. J. Fish. Aquat. Sci., 6: 272-278.
CrossRef  |  Direct Link  |  

36:  Masiha, A., E. Ebrahimi, N.M. Soofiani and M. Kadivar, 2015. Effect of dietary canola oil level on the growth performance and fatty acid composition of fingerlings of rainbow trout (Oncorhynchus mykiss). Iran. J. Fish. Sci., 14: 336-349.
Direct Link  |  

37:  Asuwaju, F.P., V.O. Onyeche, K.E. Ogbuebunu, H.F. Moradun and E.A. Robert, 2014. Effect of feeding frequency on growth and survival rate of Clarias gariepinus fingerlings reared in plastic bowls. J. Fish. Aquatic Sci., 9: 425-429.
CrossRef  |  Direct Link  |  

38:  Paray, B.A., M.K. Al-Sadoon and M.A. Haniffa, 2015. Impact of different feeds on growth, survival and feed conversion in stripped snakehead Channa striatus (Bloch 1793) larvae. Indian J. Fish., 62: 82-88.
Direct Link  |  

39:  Milstein, A., A. Kadir and M.A. Wahab, 2008. The effects of partially substituting Indian carps or adding silver carp on polycultures including small indigenous fish species (SIS). Aquaculture, 279: 92-98.
CrossRef  |  Direct Link  |  

40:  Medeiros, M.V., J. Aubin and A.F. Camargo, 2017. Life cycle assessment of fish and prawn production: Comparison of monoculture and polyculture freshwater systems in Brazil. J. Cleaner Prod., 156: 528-537.
CrossRef  |  Direct Link  |  

41:  Bag, N., S. Moulick and B.C. Mal, 2016. Effect of stocking density on water and soil quality, growth, production and profitability of farming Indian major carps. Indian J. Fish, 63: 39-46.

42:  Kassam, L. and A. Dorward, 2017. A comparative assessment of the poverty impacts of pond and cage aquaculture in Ghana. Aquaculture, 470: 110-122.
CrossRef  |  Direct Link  |  

43:  Avadi, A., N. Pelletier, J. Aubin, S. Ralite, J. Nunez and P. Freon, 2015. Comparative environmental performance of artisanal and commercial feed use in Peruvian freshwater aquaculture. Aquaculture, 435: 52-66.
CrossRef  |  Direct Link  |  

44:  David, G.S., E.D.D. Carvalho, D. Lemos, A.N. Silveira and M. Dall'Aglio-Sobrinho, 2015. Ecological carrying capacity for intensive tilapia (Oreochromis niloticus) cage aquaculture in a large hydroelectrical reservoir in Southeastern Brazil. Aquacult. Eng., 66: 30-40.
CrossRef  |  Direct Link  |  

45:  Tsagaraki, T.M., G. Petihakis, K. Tsiaras, G. Triantafyllou and M. Tsapakis et al., 2011. Beyond the cage: Ecosystem modelling for impact evaluation in aquaculture. Ecol. Model., 111: 2512-2523.
CrossRef  |  Direct Link  |  

46:  Asche, F., K.H. Roll and R. Tveteras, 2009. Economic inefficiency and environmental impact: An application to aquaculture production. J. Environ. Econ. Manage., 58: 93-105.
CrossRef  |  Direct Link  |  

47:  Yogev, U., K.R. Sowers, N. Mozes and A. Gross, 2017. Nitrogen and carbon balance in a novel near-zero water exchange saline recirculating aquaculture system. Aquaculture, 467: 118-126.
CrossRef  |  Direct Link  |  

48:  Besson, M., J. Aubin, H. Komen, M. Poelman and E. Quillet et al., 2016. Environmental impacts of genetic improvement of growth rate and feed conversion ratio in fish farming under rearing density and nitrogen output limitations. J. Cleaner Prod., 116: 100-109.
CrossRef  |  Direct Link  |  

©  2020 Science Alert. All Rights Reserved