Effect of Spirulina Suplemantation to Canola Meal-Containing Goldfish (Carrasius auratus) Diets on Growth Performance, Nutrient Digestibility and Digestive Enzyme Activity

Öz

The aim of this study was to determine the effects of spirulina added to diets containing canola meal in juvenile goldfish (Carrasius auratus) on growth, feed utilization, nutrient digestibility and intestinal digestive enzyme activity. In the experiment planned as 4 groups and 3 replications, fish with an average weight of 2.3 ± 0.9 g were placed in 12 glass aquaria with a capacity of 60 liters (60x30x35) with 20 fish per aquarium. Diets were prepared to contain 30% canola meal. 10%, 20% and 30% spirulina was added to the diets except the control diet, respectively. Fish were fed twice a day until satiated for 7 weeks. At the end of the experiment, it was determined that diets containing spirulina significantly (p<0.05) increased the growth of fish. The best FCR value was obtained from the group containing 30% spirulina. It was determined that nutrient digestibility (dry matter, protein, lipid) increased significantly (p<0.05) in groups fed diets containing spirulina compared to the control group and similarly, the activity of the digestive enzyme lipase enzyme in the intestines increased (p<0.05). While an increase in protease enzyme activity was detected, it was determined that there was no significant difference between the groups (p>0.05). The results showed that adding spirulina to diets containing 30% canola meal increased the nutrient digestibility that decreased with the presence of canola meal and the digestive enzyme activity, thus increasing fish growth. When the groups added spirulina together with canola meal were compared among themselves, it was shown that adding 30% spirulina was more effective on these parameters.

Anahtar Kelimeler

• Goldfish (Carrasius auratus)
• canola meal
• spirulina
• apparent digestibility
• digestive enzyme
• growth

Kanola unu içeren Japon balığı (Carrasius auratus) yemlerine spirulina ilavesinin büyüme performansı, besin maddesi sindirimi ve sindirim enzimleri aktivitesi üzerine etkisi

Öz

Bu çalışmanın amacı canola unu içeren yavru Japon balığı (Carrasius auratus) diyetlerine ilave edilen spirulinanın büyüme, yemden yararlanma, besin maddesi sindirebilirliği ve bağırsak sindirim enzim aktivitesi üzerine etkisini belirlemektir. 4 grup 3 tekerrür olarak planlanan denemede ortalama ağırlığı 2.3 ±0.9 g olan balıklar, 60 litre kapasiteli (60x30x35) 12 adet cam akvaryuma her bir akvaryuma 20 adet balık olacak şekilde yerleştirildi. Diyetler %30 oranında Canola meal içerecek şekilde hazırlandı. Kontrol diyeti dışındaki diyetlere sırası ile %10, %20 ve %30 oranında spirulina ilave edildi. Balıklar 7 hafta boyunca doyuncaya kadar günde iki kez yemlendi. Deneme sonunda spirulina içeren diyetlerin balığın büyümesini önemli (p < 0.05) ölçüde arttırdığı tespit edildi. En iyi FCR değeri %30 oranında spirulina içeren gruptan elde edildi. Kontrol grubuna kıyasla spirulina içeren diyetlerle yemlenen gruplarda besin maddesi sindirilenilirliğinin (kuru madde, protein, lipid) önemli ölçüde (p < 0.05) arttığı ve benzer olarak bağırsaklardaki sindirim enzimlerinden lipaz enziminin aktivitesini arttırdığı (p < 0.05) tespit edildi. Proteaz enzim aktivitesinde artış tespit edilirken gruplar arasında önemli bir fark olmadığı (p > 0.05) saptandı. Sonuçlar %30 oranında canola unu içeren diyetlere spirulina ilave etmenin canola unu varlığı ile azalan besin madde sindirilebilirliğini ve sindirim enzim aktivitesini arttırarak balığın büyümesini arttırdığını ortaya koydu. Kanola unu ile birlikte spirulina ilave edilen gruplar kendi aralarında karşılaştırıldığında %30 spirulina ilave etmenin bu parametreler üzerinde daha etkili olduğunu gösterdi.

Anahtar Kelimeler

• Goldfish (Carrasius auratus)
• canola meal
• spirulina
• apparent digestibility
• digestive enzyme
• growth

Kaynakça

1. Abdel-Tawwab, M., & Ahmad, M. H. (2009). Live Spirulina (Arthrospira platensis) as a growth and immunity promoter for Nile tilapia, Oreochromis niloticus (L.), challenged with pathogenic Aeromonas hydrophila. Aquaculture Research, 40(9): 1037–1046. https://doi.org/10.1111/j.1365-2109.2009.02195.x
2. Abdulrahman, N.M. (2014). Evaluation of Spirulina spp. as food supplement and its effect on growth performance of common carp fingerlings. International Journal of Fisheries Aquatic Studies, 2(2): 89–92. https://doi.org/10.1111/j.1365-2109.2009. 02195.x.
3. Adel, M., Yeganeh, S., Dadar, M., Sakai, M., Dawood, M.A.O. (2016). Effects of dietary Spirulina platensis on growth performance, humoral and mucosal immune responses and disease resistance in juvenile great sturgeon (Huso huso Linnaeus, 1754). Fish Shellfish Immunology, 56: 436–444. https://doi.org/10.1016/j.fsi.2016.08.003
4. Alagawany, M., Taha, A.E., Noreldin, A., El-Tarabily, K.A. & Abd El-Hack, M.E. (2021). Nutritional applications of species of Spirulina and Chlorella in farmed fish: A review. Aquaculture, 542: 736841. https://doi.org/10.1016/j.aquaculture.2021.736841
5. Al-Deriny, S. H., Dawood, M. A. O., Zaid, A. A. A., El-Tras, W. F., Paray, B. A., Van Doan, H., & Mohamed, R. A. (2020). The synergistic effects of Spirulina platensis and Bacillus amyloliquefaciens on the growth performance, intestinal histomorphology, and immune response of Nile tilapia (Oreochromis niloticus). Aquaculture Reports, 17: Article 100390. https://doi.org/10.1016/j.ejar.2023.08.008
6. AlMulhim, N. M., Virk, P., Abdelwarith, A. A. & AlKhulaifi, F. M., (2023). Effect of incorporation of Spirulina platensis into fish diets, on growth performance and biochemical composition of Nile Tilapia, Oreochromis niloticus Egyptian Journal of Aquatic Research, 49: 537-541. https://doi.org/10.1016/j.ejar.2023.08.008
7. Ansarifard, F., Rajabi Islami, H., Shamsaie Mehrjan, M. & Soltani M., (2018). Effects of Arthrospira platensis on growth, skin color and digestive enzymes of Koi, Cyprinus carpio. Iranian Journal of Fisheries Sciences, 17(2): 381-393. https://doi.org/10.22092/IJFS.2018.115878
8. AOAC, (1995). Agriculture Chemicals; Contaminants, Drugs. 16th edn. Official Methods of Analysis of AOAC International vol. 1 AOAC International, Arlington, VA.

9. Bligh, E.G. & Dyer, W.J., (1959). A rapid method of total lipid extraction and purification. Can. J. Biochem Phys., 37: 911–917. https://doi.org/10.1139/o59-099
10. Blanco, A.M. & Unniappan, S. (2022). Goldfish (Carassius auratus): biology, husbandry, and research applications, pp. 373-408. In: D’angelo, L., de Girolamo, P. (Ed.), Laboratory Fish in Biomedical Research, Elsevier, 450 p. https://doi.org/10.1016/B978-0-12-821099-4.00012-2
11. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Author links open overlay panel. Analytical Biochemistry, 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
12. Brown, C., Wolfenden, D. & Sneddon, L. (2019). Goldfish (Carassius auratus), pp 467-478. In: Yeates MRCVS, J. (Ed). Companion Animal Care and Welfare: The UFAW Companion Animal Handbook, Wiley, pp 478. https://doi.org/10.1002/9781119333708.ch23
13. Burel, C., Boujard, T., Escaffre, A.M., Kaushik, S.J., Boeuf, G., Mol, K. A., Geyten, S. V. & Kühn, E. R. (2000). Dietary low-glucosinolate rapeseed meal affects thyroid status and nutrient utilization in rainbow trout (Oncorhynchus mykiss). British Journal of Nutrition, 83: 653–664. https://doi.org/ 10.1017/s0007114500000830.
14. Cao, S. P., Zou, T., Zhang, P.Y., Han, D., Jin, J. Y., Liu, H. K., Yang, Y. X., Zhu, X. M., & Xie, S. Q. (2018). Effects of dietary fishmeal replacement with Spirulina platensis on the growth, feed utilization, digestion and physiological parameters in juvenile gibel carp (Carassis auratus gibelio var. CAS III). Aquaculture Research, 49: 1320–1328. https://doi.org/10.1111/are.13590
15. Cheng, Z., Ai, Q., Mai, K., Xu, W., Ma, H. , Li, Y. & Zhang, J. (2010). Effects of dietary canola meal on growth performance, digestion and metabolism of Japanese seabass, Lateolabrax japonicus. Aquaculture, 305: 102–108. https://doi.org/10.1016/j.aquaculture.2010.03.031
16. Dernekbasi, S., Unal, H., Karayucel, I., & Aral, O. (2010). Effect of dietary supplementation of different rates of Spirulina (Spirulina platensis) on growth and feed conversion in guppy (Poecilia reticulata Peters, 1860). Journal of Animal Veterinary Advances, 9: 1395–1399.
17. Dossou, S., Koshio, S., Ishikawa, M., Yokoyama, S., Dawood, M.A., El Basuini, M.F., El- Hais, A.M. & Olivier, A. (2018a). Effect of partial replacement of fish meal by fermented rapeseed meal on growth, immune response and oxidative condition of red sea bream juvenile, (Pagrus major). Aquaculture, 490: 228–235. https://doi.org/10.1016/j. aquaculture.2018.02.010.
18. Dossou, S., Koshio, S., Ishikawa, M., Yokoyama, S., Dawood, M.A., El Basuini, M.F., El- Hais, A.M., Olivier, A. & Zaineldin, A. I. (2018b). Growth performance, blood health, antioxidant status and immune response in red sea bream (Pagrus major) fed Aspergillus oryzae fermented rapeseed meal (RM-Koji). Fish and Shellfish Immunology, 75: 253-262. https://doi.org/10.1016/j.fsi.2018.01.032
19. El-Sheekh, M., El-Shourbagy, I., Shalaby, S. & Hosny, S. (2014). Effect of feeding Arthrospira platensis (Spirulina) on growth and carcass composition of hybrid red tilapia (Oreochromis niloticus x Oreochromis mossambicus). Turkish Journal of Fisheries and Aquaculture Sciences, 14: 471–478.
20. Erdogan, F. & Ölmez, M. (2009). Kanola küspesinin melek balığının (Pterophyllum scalare Lichtenstein 1823) büyüme, somatik indeksler ve vücut kompozisyonuna etkileri. Tarım Bilimleri Dergisi, 15(2): 181-187. https://doi.org/10.1501/Tarimbil_0000001089
21. Erdogan, F. (2019). Effects of Spirulina platensis as a feed additive on growth and coloration of blue dolphin cichlids (Cyrtocara moorii Boulunger, 1902) . Aquaculture Research, 50: 2326–2332. https://doi.org/10.1111/are.14112
22. Francis, G., Makkar, H. P.S. & Becker, K. (2001). Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture, 199: 197–227.
23. Furukawa, A. & Tsukahara, H. (1966). On the acid digestion method for determination of chromic oxide as an index substances in the study of digestibility of fish feed. Bull. Jpn. Soc. Sci. Fish., 32, 502–506.
24. Grosshagauer, S., Kraemer, K. & Somoza, V. (2020). The true value of Spirulina. Journal of Agricultural and Food Chemistry, 68 (14): 4109–4115. https://doi.org/10.1021/acs.jafc.9b08251
25. Güroy, B., Sahin, I., Mantoglu, S. & Kayalı, S. (2012). Spirulina as a natural carotenoid source on growth, pigmentation and reproductive performance of yellow tail cichlid Pseudotropheus acei. Aquaculture International, 20(5): 869–878.
26. Güroy, B., Güroy, D., Bilen, S., Kenanoglu, O. N., Sahin, İ., Terzi, E., Karadal, O. & Mantoglu, S. (2022). Effect of dietary Spirulina (Arthrospira platensis) on the growth performance, immune-related gene expression and resistance to Vibrio anguillarum in European seabass (Dicentrarchus labrax). Aquaculture Research, 53: 2263–2274. https://doi.org/ 10.1111/are.15745
27. Han, P., Li, Jingjing, Zhong, H., Xie, J., Zhang, P., Lu, Q., Li, Jun, Xu, P., Chen, P., Leng, L. & Zhou, W. (2021). Anti-oxidation properties and therapeutic potentials of spirulina. Algal Research, 55: 102240. https://doi.org/10.1016/j.algal.2021.102240
28. Hernandez, C., Olmeda-Guerrero, L., Chávez-Sánchez, M.C., Ibarra-Castro, L., Gaxiola-Cortez, G. & Martínez-Cárdenas, L. (2020). Nutritional evaluation of canola meal as fish meal replacement for juvenile spotted rose snapper (Lutjanus guttatus): Effects on growth performance, hematological parameters, body composition, and nutrient digestibility. Animal Feed Science and Technology, 269: 114683. https://doi.org/10.1016/j.anifeedsci.2020.114683
29. James, R., Sampath, K. W., Thangarathinam, R., & Vasudhevan, I. (2006). Effect of dietary Spirulina level on growth, fertility, coloration and leucocyte count in red swordtail, Xiphophorus helleri. The Israel Journal of Aquaculture, 58: 97–104.
30. Kargın, H. & Dikbas, M. D. (2020). The Effects of diets supplemented With Spirulina platensis in different quantities on pigmentatıon and growth performance of goldfish (Carassıus auratus). Siberian Journal of Life Sciences and Agriculture, 12: 62-78. https://doi.org/10.12731/2658-6649-2020-12-5-62-78
31. Khanzadeh, M., Esmaeili, F.A. & Seifi, B.S. (2016). Effects of partial replacement of fish meal with Spirulina platensis meal in practical diets on growth, survival, body composition, and reproductive performance of three-spot gourami (Trichopodus trichopterus) (Pallas, 1770). Aquaculture International, 24: 69–84.
32. Kim, S.-S., Rahimnejad, S., Kim, K.-W. & Lee, K.-J. (2013). Partial replacement of fish meal with Spirulina pacifica in diets for parrot fish (Oplegnathus fasciatus). Turkish Journal of Fisheries and Aquatic Sciences,13: 197–204. http://doi.org/10.4194/1303-2712-v13_2_01
33. Kokou, F. & Fountoulaki, E. (2018). Aquaculture waste production associated with antinutrient presence in common fish feed plant ingredients. Aquaculture, 495: 295-310. https://doi.org/10.1016/j.aquaculture.2018.06.003
34. Kurtoglu, A., Çagıltay, F., Diler, İ. & Saglam, M. (2019). A Study on gilthead seabream (Sparus aurata) fish feed replacement of fishmeal at different rates use of canola meal (Brassica spp.) on growth rate, feed utilisation and digestibility. Kocatepe Veterinary Journal, 12(1): 33-38. https://doi.org/10.30607/kvj.470718
35. Lim, C., Webster, C.D. & Lee, C.S. (Eds) (2008). Alternative Protein Sources in Aquaculture Diets. New York, USA: CRC Press, Taylor & Francis. 571 p.
36. Liu, F., Qu, Y.-K., Wang, A.-M., Yu, Y.-B., Yang, W.-P., Lv, F., & Nie, Q. (2019). Effects of carotenoids on the growth performance, biochemical parameters, immune responses and disease resistance of yellow catfish (Pelteobagrus fulvidraco) under high-temperature stress. Aquaculture, 503: 293–303. https://doi.org/10.1016/j.aquaculture.2019.01.008
37. Man, Y. B., Zhang, F., Ma, K. L., Mo, W. Y., Kwan, H. S., Chow, K. L., Man, K. Y., Tsang, Y. F., Li, W. C., & Wong, M. H. (2020). Growth and intestinal microbiota of Sabah giant grouper reared on food waste-based pellets supplemented with spirulina as a growth promoter and alternative protein source. Aquaculture Reports, 18: 100553. https://doi.org/10.1016/j.aqrep.2020.100553
38. Mohammadia, M., Imania, A., Farhangib, M., Gharaeic, A. & Hafezieh, M. (2020). Replacement of fishmeal with processed canola meal in diets for juvenile Nile tilapia (Oreochromis niloticus): Growth performance, mucosal innate immunity, hepatic oxidative status, liver and intestine histology. Aquaculture, 518: 734824. https://doi.org/10.1016/j.aquaculture.2019.734824
39. Mohammadiazarm, H., Maniat, M., Ghorbanijezeh, K. & Ghotbeddin, N. (2021). Effects of Spirulina powder (Spirulina platensis) as a dietary additive on Oscar fish, Astronotus ocellatus: Assessing growth performance, body composition, digestive enzyme activity, immune-biochemical parameters, blood indices and total pigmentation. Aquaculture Nutrition, 27(1): 252–260.
40. Nagel, F., von Danwitz, A., Tusche, K., Kroeckel, S., van Bussel, C.G.J., Schlachter, M., Adem, H., Tressel, R.-P. & Schulz, C. (2012). Nutritional evaluation of rapeseed protein isolate as fish meal substitute for juvenile turbot (Psetta maxima L.) - impact on growth performance, body composition, nutrient digestibility and blood physiology, Aquaculture, 356: 357–364. https://doi.org/10.1016/j.aquaculture.2012.04.045.
41. Ravardshiri, M., Bahram, S., Javadian, S. R. & Bahrekazemi, M. (2021). Cinnamon promotes growth performance, digestive enzyme, blood parameters, and antioxidant activity of rainbow trout (Oncorhynchus mykiss) in low-carbohydrate diets. Turkish Journal of Fisheries and Aquatic Sciences, 21(7): 309-322. http://doi.org/10.4194/1303-2712-v21_7_01.
42. Roohani, A.M., Abedian Kenari, A., Fallahi Kapoorchali, M., Borani, M.S., Zoriezahra, S.J., Smiley, A.H., Esmaeili, N. & Rombenso, A.N. (2019). Effect of spirulina Spirulina platensis as a complementary ingredient to reduce dietary fishmeal on the growth performance, whole-body composition, fatty acid and amino acid profiles, and pigmentation of Caspian brown trout (Salmo trutta caspius) juveniles. Aquaculture Nutrition, 25: 633–645. https://doi.org/10.1111/anu.12885
43. Sehgal, H. H., Sehgal, G. K. & Dhawan, J. (2022). Dietary supplementation of Spirulina platensis enhances body colouration of shubunkin gold fish, Carassius auratus (Linn.) even in high-alkalinity rearing water. Journal of Applied Ichthyology, 38: 223–231. https://doi.org/ 10.1111/jai.14288
44. Shafaeipour, A., Yavari, V., Falahatkar, B., Maremmazi, J. G. & Gorjipour, E. (2008). Effects of canola meal on physiological and biochemical parameters in rainbow trout (Oncorhynchus mykiss). Aquaculture Nutrition, 14: 110–119. https://doi.org/10.1111/j.1365-2095.2007.00509.x
45. Soni, R. A., Sudhakar, K., Rana, R. S. (2017). Spirulina – from growth to nutritional product: A review. Trends Food Sci. Technol., 69: 157–171. https://doi.org/10.1016/j.tifs.2017.09.010
46. Sotoudeh, E. & Esmaeili, M. (2022). Effects of Biotronic® Top3, a feed additive containing organic acids, cinnamaldehyde and a permeabilizing complex on growth, digestive enzyme activities, immunity, antioxidant system and gene expression of barramundi (Lates calcarifer). Aquaculture Reports, 24: 101152. https://doi.org/10.1016/j.aqrep.2022.101152
47. Sun, X., Chang, Y., Ye, Y., Ma, Z., Liang, Y., Li, T., Xing, W. & Luo, L. (2012). The effect of dietary pigments on the coloration of Japanese ornamental carp (koi, Cyprinus carpio L.). Aquaculture, 342-343: 62–68.
48. Teimouri, M., Amirkolaie, A. K. & Yeganeh, S. (2013). The effects of Spirulina platensis meal as a feed supplement on growth performance and pigmentation of rainbow trout (Oncorhynchus mykiss). Aquaculture, 396-399: 14-19. ll rights reserved. http://dx.doi.org/10.1016/j.aquaculture.2013.02.009
49. Thomas, T.B., Thirumalaikumar, E., Sathishkumar, R., Rajeswari, M.V., Vimal, S., Uma, G. & Jones, R.D.S. (2023). Effects of dietary Andrographis paniculata extract on growth, haematological, immune responses, immune-related genes expression of ornamental goldfish (Carassius auratus) and its susceptibility to Aeromonas hydrophila infection. Aquaculture Reports 33: 101850. https://doi.org/10.1016/j.aqrep.2023.101850
50. Velasquez, S. F., Chan, M. A., Abisado, R. G., Traifalgar, R. F. G., Tayamen, M. M., Maliwat, G. C. F. & Ragaza, J. A. (2016). Dietary Spirulina (Arthrospira platensis) replacement enhances performance of juvenile Nile tilapia (Oreochromis niloticus). J. Appl. Phycol., 28: 1023–1030 . https://doi.org/10.1007/s10811-015-0661-y
51. Wang, B., Liu, Q., Huang, Y., Yuan, Y., Ma, Q., Du, M., Cai, T., & Cai, Y. (2018). Extraction of polysaccharide from Spirulina and evaluation of its activities. Evidence-Based Complementary and Alternative Medicine, 2018: 3425615. https://doi.org/10.1155/2018/3425615
52. Wei, L. & Wee, W. (2014). Diseases in aquaculture. Research Journal of Animal, Veterinary and Fishery Sciences, 7: 1–6.
53. Yeganeh, S., Teimouri, M. & Amirkolaie, A. K. (2015). Dietary effects of Spirulina platensis on hematological and serum biochemical parameters of rainbow trout (Oncorhynchus mykiss). Res. Vet. Sci., 101: 84–88.
54. Yılmaz, S., Ergun, S., Çelik, E. Ş. & Yigit, M. (2018). Effects of dietary humic acid on growth performance,haemato‐immunological and physiological responses andresistance of Rainbow trout, Oncorhynchus mykiss to Yersini ruckeri. Aquaculture Research, 49: 3338–3349. https://doi.org/10.1111/are.137983338
55. Yigit, Ö. N., Bahadır Koca, S., Bayrak, H., Dulluc, A. & Diler, İ. (2012). Effects of canola meal on growth and digestion of rainbow trout (Oncorhynchus mykiss) fry. Turk. J. Vet. Anim. Sci., 36(5): 533-538. https://doi.org/10.3906/vet-1101-705.
56. Yigit, Ö. N., Dulluc, A., Bahadır Koca, S. & Didinen, B. I. (2013). Effects of canola meal use ınstead of soybean meal in mirror carp (Cyprinus carpio, L. 1758) diet on growth and body composition. Journal of Agricultural Sciences, 19: 140-147. https://doi.org/10.1501/Tarimbil_0000001238
57. Yigit, N. Ö. (2018). Sarı prenses (Labidochromis caeruleus) yavrularında kanola küspesi içeren yemlere selülaz ve fitaz enzimi ilavesinin yem dönüşüm oranı ve büyüme performansı üzerine etkileri. Süleyman Demirel Üniversitesi Eğirdir Su Ürünleri Fakültesi Dergisi, 14(2): 113-118.