Have a personal or library account? Click to login
Dietary Administration of Green Macroalgae (Ulva intestinalis) on Growth Performance, Serum Immune Parameters, and Gene Expression in Common Carp (Cyprinus carpio) Cover

Dietary Administration of Green Macroalgae (Ulva intestinalis) on Growth Performance, Serum Immune Parameters, and Gene Expression in Common Carp (Cyprinus carpio)

Open Access
|Jan 2025

References

  1. Akbary P., Aminikhoei Z. (2018 a). Effect of polysaccharides extracts of algae Ulva rigida on growth, antioxidant, immune response and resistance of shrimp, Litopenaeus vannamei against Photobacterium damselae. Aquac. Res., 49: 2503–2510.
  2. Akbary P., Aminikhoei Z. (2018 b). Effect of water-soluble polysaccharide extract from the green alga Ulva rigida on growth performance, antioxidant enzyme activity, and immune stimulation of grey mullet Mugil cephalus. J. Appl. Phycol., 30: 1345–1353.
  3. Akbary P., Sohrabzaei Z. (2019). The effect of red seaweed Gracillaria arcuata extract on digestion and liver enzymes and the activity of antioxidant enzymes in grey mullet, Mugil cephalus. J. Aquat. Ecol., 9: 124–133.
  4. Barsanti L., Gualtieri P. (2014). Algae: anatomy, biochemistry, and biotechnology. CRC Press. 362 pp.
  5. Becker E. (2004). Microalgae in human and animal nutrition. Handbook of Microalgal Culture. Blackwell, Oxford, UK.
  6. Bita S., Ghorbani Ranjbari N. (2016). Antioxidant and immune-stimulating effects of Sargassum angustifolium extract on the common carp (Cyprinus carpio) juvenile. JAPB, 3: 15–32.
  7. Bustin A.S., Benes V., Garson J.A., Healmans J., Huggett J., Kubista M., Muller R., Nolaan T., Pfaffl M., Shipley G., Vandesompele J., Wittwer C.T. (2009). The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin. Chem., 55: 611–622.
  8. Clerton P., Troutaud D., Verlhac V., Gabaudan J., Deschaux, P. (2001). Dietary vitamin E and rainbow trout (Oncorhynchus mykiss) phagocyte functions: effect on gut and on head kidney leukocyte. Fish Shellfish Immunol., 11: 1–13.
  9. Daneshvar Ghorbani M., Hosseini Shekarabi S.P., Hosseini S.E. (2019). The antioxidant effects of green macroalgae Ulva intestinalis hydroalcoholic extract on farm-raised beluga minced meat during refrigerated storage. J. Aquacult. Sci., 6: 60–74.
  10. Davies S.J., Brown M.T., Camilleri M. (1997). Preliminary assessment of the seaweed Porphyra purpurea in artificial diets for thick-lipped grey mullet (Chelonlabrosus). Aquaculture, 152: 249–258.
  11. Dawes C.J., Orduna-Rojas J., Robledo D. (1998). Response of the tropical red seaweed Gracilaria cornea to temperature, salinity and irradiance. J. Appl. Phycol., 10: 419–425.
  12. Doan H., Hoseinifar S.H., Ringo E., Ángeles Esteban M., Dadar M., Dawood M.A.O., Faggio C. (2020). Host-associated probiotics: A key factor in sustainable aquaculture. Rev. Fish. Sci. Aquac., 28: 16–42.
  13. Farhoudi A., Sourinejad I., Nafisi Bahabadi M., Sajjadi M.M., Salarzadeh A.R. (2017). Effect of partial substitution of fishmeal by red algae Gracilaria pygmaea on the growth performance, hematology and serum biochemistry parameters of Asian seabass Lates calcarifer (Bloch, 1790). IFSRI, 26: 77–89.
  14. Fischbach F., Zawta B. (1992). Age-dependent reference limits of several enzymes in plasma at different measuring temperatures. Klin Labor., 38: 555–561.
  15. Fumanal M., Di Zeo D.E., Anguís V., Fernández-Diaz C., Alarcón F.J., Piñera R., Balebona M.C. (2020). Inclusion of dietary Ulva ohnoi 5% modulates Solea senegalensis immune response during Photobacterium damselae subsp. piscicida infection. Fish Shellfish Immunol., 100: 186–197.
  16. Gabillard J.C., Kamangar B.B., Montserrat N. (2006). Coordinated regulation of the GH/IGF system genes during refeeding in rainbow trout (Oncorhynchus mykiss). J. Endocrinol., 191: 15–24.
  17. Garcia-Poza S., Leandro A., Cotas C., Cotas J., Marques J.C., Pereira L., Gonçalves A.M.M. (2020). The evolution road of seaweed aquaculture: cultivation technologies and the industry 4.0. Int. J. Environ. Res. Public Heal., 17: 1–42.
  18. Ghasemi Pirbalouti A., Pirali E., Pishkar G., Jalali S.M., Raissy M., Jafarian Dehkordi M., Hamedi B. (2011). The essential oils of some medicinal plants on the immune system and growth of rainbow trout (Oncorhynchus mykiss). J. Med. Plant Res., 2: 149–155.
  19. Guerreiro I., Magalhães R., Coutinho F., Couto A., Sousa S., Deleruematos C. (2019). Evaluation of the seaweeds Chondrus crispus and Ulva lactuca as functional ingredients in gilthead seabream (Sparus aurata). J. Appl. Phycol., 31: 2115–2124.
  20. Hashem Dabbaqian E., Rezaei M., Tabarsa M. (2016). Ethanolic extraction and solvent-solvent partitioning of antioxidant compounds from green seaweed Enteromorpha intestinalis. J. Fish., 69: 385–396.
  21. Hoseinifar S.H., Yousefi S., Capillo G., Paknejad H., Khalili M., Tabarraei A., Faggio C. (2018). Mucosal immune parameters, immune and antioxidant defence related genes expression and growth performance of zebrafish (Danio rerio) fed on Gracilaria gracilis powder. Fish Shellfish Immunol., 83: 232–237.
  22. Hoseinifar S.H., Jahazi M.A., Nikdehghan N., Van Doan H., Volpe M.G., Paolucci M. (2020). Effects of dietary polyphenols from agricultural by-products on mucosal and humoral immune and antioxidant responses of convict cichlid (Amatitlania nigrofasciata). Aquaculture, 517: 1–7.
  23. Hoseinifar S.H., Fazelan Z., Bayani M., Yousefi M., Van Doan H., Yazici M. (2022). Dietary red macroalgae (Halopithys incurva) improved systemic an mucosal immune and antioxidant parameters and modulated related gene expression in zebrafish (Danio rerio). Fish Shellfish Immunol., 123: 164–171.
  24. Humbel R.E. (1990). Insulin-like growth factors 1 and 2. Eur. J. Biochem., 190: 445–462.
  25. Imanpoor M., Roohi Z. (2015). Effect of a multi-strain probiotic (Primalac) on growth performance, some blood biochemical parameters, survival and stress resistance on Caspian kutum (Rutilus kutum) fry. IFSRI, 24: 95–102.
  26. Jahanbakhshi A., Pourmozaffar S., Adeshina I., Vayghan A.H., Reverter M. (2022). Effect of garlic (Allium sativum) extract on growth, enzymological and biochemical responses and immune-related gene expressions in giant freshwater prawn (Macrobrachium rosenbergii). J. Anim. Physiol. Anim. Nutr. (Berl.), 106: 947–956.
  27. Jaime-Ceballos B., Villarreal H., Grasia T., Pérez Jar L., Alfonso E. (2005). Effect of Spirulina platensis meal as feed additive on growth, survival and development in Litopenaeus schmmiti shrimp larvae. Rev. Investig. Mar., 26: 235–241.
  28. Karami E., Mesbah M., Molayem Raftar T., Mohammadian T., Hoseini S.S., Nazari M. (2016). Effects of aqueous extract of Sargassum angustifolium (Agardh, 1820) on some of the hematological parameters in common carp Cyprinus carpio (Linnaeus, 1758). J. Aquat. Ecol., 6: 124–133.
  29. Kazemi M., Abediankenari A., Rabiei R. (2018). Effect of marine macroalgae on growth performance and immune response in rainbow trout fingerlings. JFST, 7: 9–16.
  30. Khezri Ahmad Abad M., Rezai M., Zolfaghari M. (2016). Studying the possibility of using the extract of Entromorpha intestinalis in order to control some food-borne pathogens. JFST, 13: 81–91.
  31. Klongklaew N., Praiboon J., Tamtin M., Srisapoome P. (2021). Chemical composition of a hot water crude extract (HWCE) from Ulva intestinalis and its potential effects on growth performance, immune responses, and resistance to white spot syndrome virus and yellowhead virus in Pacific white shrimp (Litopenaeus vannamei). Fish Shellfish Immunol., 112: 8–22.
  32. Lieke T., Meinelt T., Hoseinifar S.H., Pan B., Straus D.L., Steinberg C.E. (2020). Sustainable aquaculture requires environmental-friendly treatment strategies for fish diseases. Rev. Aquacult., 12: 943–965.
  33. Mahmoudi N., Safari R., Shabani A., Hoseinifar S.H., Yazici M., El-Haroun E. (2022). Can dietary Dictyota dichotoma powder affect performance, serum, and mucus immune parameters, and antioxidant defense in zebrafish (Danio rerio)? Aquac. Rep., 26: 101279.
  34. Mansuya P., Aruna P., Sridhar S., Kumar J.S., Babu S. (2010). Antibacterial activity and qualitative phytochemical analysis of selected seaweeds from Gulf of Mannar region. J. Exp. Sci., 1: 23–26.
  35. Marques A., Marçal R., Pereira V., Pereira P., Mieiro C., Guilherme S., Marques C., Santos M.A., Pereira R., Abreu H., Gaivão I., Pacheco M. (2020). Macroalgae-enriched diet protects gilthead seabream (Sparus aurata) against erythrocyte population instability and chromosomal damage induced by aqua-medicines. J. Appl. Phycol., 32: 1477–1493.
  36. Mazlum Y., Yazici M., Sayin S., Habiboğlu O., Uğur S. (2020). Effects of two different macroalgae (Ulva lactuca and Jania rubens) species on growth and survival of red swamp crayfish (Procambarus clarkii) as feed additive. Mar. Sci. Tech. Bull., 10: 154–162.
  37. Mustafa M.D.G., Umino T., Nakagaw H. (1995). A comparison of body constituents of wild and cultured red sea bream, Pagrus major from different localities in Japan. AFS, 8: 143–150.
  38. Niroomand M., Sajadi M., Yahyavi M., Asadi M. (2011). Effects of dietary betaine on growth, survival, body composition and resistance of fry rainbow trout (Oncorhynchus mykiss) under environmental stress. Iran. J. Fish. Sci., 20: 135–146.
  39. Pezeshk F., Babaei S., Kenari A.A., Hedayati M., Naseri M. (2019). The effect of supplementing diets with extracts derived from three different species of macroalgae on growth, thermal stress resistance, antioxidant enzyme activities and skin color of electric yellow cichlid (Labidochromis caeruleus). Aquac. Nutr., 25: 436–443.
  40. Pirian K., Piri K., Sohrabipour J., Jahromi S., Rabiei R. (2017). Evaluation of chemical components and physicochemical properties of two green macroalgae species Ulva intestinalis and Ulva linza from the Persian Gulf. IJMAPR, 33: 62–72.
  41. Ponce M., Zuasti E., Anguís V., Fernández-Díaz C. (2020). Effects of the sulfated polysaccharide ulvan from Ulva ohnoi on the modulation of the immune response in Senegalese sole (Solea senegalensis). Fish Shellfish Immunol., 18: 250–285.
  42. Pradhan B., Patra S., Behera C., Nayak R., Jit B.P., Ragusa A., Jena M. (2021). Preliminary investigation of the antioxidant, anti-diabetic, and anti-inflammatory activity of Enteromorpha intestinalis extracts. Molecules, 26: 1–16.
  43. Ravi Kumar S., Ramanathan G., Subhakaran M., Inbaneson S.G. (2009). Antimicrobial compounds from marine alophytes for silk-worm disease treatment. IJMMS, 1: 184–191.
  44. Reinecke M., Bjornsson B.T., Dickho V.W., McCormick S.D., Navarro I., Power D.M., Gutierrez J. (2005). Growth hormone and insulin-like growth factors in fish: where we are and where to go. Gen. Comp. Endocrinol., 142: 20–24.
  45. Reitman S., Frankel A.S. (1957). A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am. J. Clin. Pathol., 28: 56–63.
  46. Ringo E. (1991). Effects of dietary lactate and propionate on growth and digesta in Arctic charr, Salvelinus alpinus. Aquaculture, 10: 321–333.
  47. Rouhani E., Safari R., Imanpour M.R., Hoseinifar S.H., Yazici M., El-Haroun E. (2022). Effect of dietary administration of green macroalgae (Ulva intestinalis) on mucosal and systemic immune parameters, antioxidant defence, and related gene expression in zebrafish (Danio rerio). Aquac Nutr., 4: 7693468.
  48. Ruslan F.S., Susanti D., Noor N.M., Iman N. (2021). Bioactive compounds, cosmeceutical and nutraceutical applications of green seaweed species (Chlorophyta). Squalen Bull., 16: 41–55.
  49. Saez M.I., Vizcaíno A., Galafat A., Anguís V., Fernández-Díaz C., Balebona M.C., Martínez T.F. (2020). Assessment of long-term effects of the macroalgae Ulva ohnoi included in diets on Senegalese sole (Solea senegalensis) fillet quality. Algal. Res., 47: 101885.
  50. Safari R., Hoseinifar S.H., Van Doan H., Dadar M. (2017). The effects of dietary myrtle (Myrtus communis) on skin mucus immune parameters and mRNA levels of growth, antioxidant, and immune-related genes in zebrafish (Danio rerio). Fish Shellfish Immunol., 66: 264–269.
  51. Safari R., Hoseinifar S.H., Dadar M., Van Doan H. (2021). Enrichment of common carp (Cyprinus carpio) diet with malic acid: Effects on skin mucosal immunity, antioxidant defense and growth performance. Ann. Anim. Sci., 21: 561–573.
  52. Safavi S.V., Kenari A.A., Tabarsa M., Esmaeili M. (2019). Effect of sulfated polysaccharides extracted from marine macroalgae (Ulva intestinalis and Gracilariopsis persica) on growth performance, fatty acid profile, and immune response of rainbow trout (Oncorhynchus mykiss). J. Appl. Phycol., 31: 4021–4035.
  53. Saligheh Zadeh R., Yavari V., Mousavi S.M., Zakeri M. (2015). Effect of dietary supplement of Spirulina platensis on immune indices complement and lysozyme of benny fish Mesopotamichthys sharpeyi (Günther, 1874). Aquat. Ecol., 5: 50–44.
  54. Siddik M.A.B., Rahman M.M., Anh N.T.N., Nevejan N., Bossier P. (2015). Seaweed, Entromorpha intestinalis, as a diet for Oreochromis niloticus fry. J. Appl. Aquac., 27: 113–123.
  55. Siwicki A.K., Anderson D.P. (1993). Nonspecific defense mechanisms assay in fish: II. Potential killing activity of neutrophils and macrophages, lysozyme activity in serum and organs and total immunoglobulin level in serum. Fish Dis. Diagn. Prev. Meth., Olsztyn, Poland, 10: 105–112.
  56. Sohrabipour J., Rabiei R. (2007). The checklist of green algae of the Iranian coastal lines of the Persian Gulf and the Gulf of Oman. Iran. J. Bot. 13: 146–149.
  57. Soler-Vila A., Coughlan S., Guiry M.D., Kraan S. (2009). The red alga Porphyra dioica as a fish-feed ingredient for rainbow trout (Oncorhynchus mykiss): effects on growth, feed efficiency, and carcass composition. J. Appl. Phycol., 21: 617–624.
  58. Sotoudeh E. (2020). Growth performance and blood indices of juvenile rainbow trout (Oncorhynchus mykiss) fed diets containing Sargassum cristaefolium and Gracilaria pygmaea extracts. JAIR, 8: 80–88.
  59. Sotoudeh E., Mardani F. (2017). Antioxidant-related parameters, digestive enzyme activity and intestinal morphology in rainbow trout (Oncorhynchus mykiss) fry fed graded levels of red seaweed (Gracilaria pygmaea). Aquac. Nutr., 24: 777–785.
  60. Srikong W., Bovornreungroj N., Mittraparparthorn P., Bovornreungroj P. (2017). Antibacterial and antioxidant activities of differential solvent extractions from the green seaweed Ulva intestinalis. Sci. Asia, 43: 88–95.
  61. Subramanian S., MacKinnon S.L., Ross N.W. (2007). A comparative study on innate immune parameters in the epidermal mucus of various fish species. CBPB, 148: 256–263.
  62. Taskin E., Ozturk M., Taskin E., Kurt O. (2007). Antibacterial activities of some marine algae from the Aegean Sea (Turkey). AJB, 6: 2746–2751.
  63. Valente L.M.P., Goueia A., Rema P., Motas J., Gonez E.F. (2006). Evaluation of three seaweeds Gracilaria bursa-pastoris, Ulva rigida and Gracilaria cornea as dietary ingredients in European seabass (Dicentrarchus labrax) juveniles. Aquaculture, 252: 85–91.
  64. Valente L.M.P., Araújo M., Batista S., Peixoto M.J., Sousa-Pinto I., Brotas V., Rema P. (2016). Carotenoid deposition, flesh quality and immunological response of Nile tilapia fed increasing levels of IMTA-cultivated Ulva spp. J. Appl. Phycol., 28: 691–701.
  65. Vazirzadeh A., Marhamati A., Rabiee R., Faggio C. (2020). Immuno-modulation, antioxidant enhancement and immune genes up-regulation in rainbow trout (Oncorhynchus mykiss) fed on seaweeds included diets. Fish Shellfish Immunol., 106: 582–858.
  66. Vijayaram S., Ringø E., Ghafarifarsani H., Hoseinifar S.H., Ahani S., Chou C.C. (2024). Use of algae in aquaculture: A review. Fishes, 9: 63.
  67. Wassef E.A., El Sayed A.M., Kandeel K.M., Mansour H.A., Sakr E.M. (2005). Effect of feeding Pterocladia (Rhodophyta) and Ulva (Chlorophyta) meals in diets for gilthead bream (Sparus aurata). Egypt. J. Aquat. Res., 31: 321–332.
  68. Watanuki H., Ota K., Tassakka A.C.M., Kato T., Masahiro S. (2006). Immunostimulant effects of dietary Spirulina platensis on carp (Cyprinus carpio). Aquaculture, 258: 157–163.
  69. Xuan X., Li W., Zhu W., Wang S. (2019). Effects of different levels of macroalga Gracilaria lemaneiformis on growth performance and feed utilization on the red sea bream, Pagrosomus major. J. Appl. Phycol., 31: 3213–3222.
  70. Yangthong M., Ruensirikul J. (2020). Feed intake stimulation of juvenile spotted scat (Scatophagus argus) using dietary seaweed supplementation (Ulva sp.). Aquaculture, 529: 735626.
  71. Yildirim O., Ergun S., Yaman S., Turker A. (2009). Effects of two seaweeds (Ulva lactuca and Enteromorpha linza) as a feed additive in diets on growth performance, feed utilization, and body composition of rainbow trout (Oncorhynchus mykiss). Kafkas. Univ. Vet. Fak. Derg., 15: 455–460.
  72. Younis E.M., Al-Quffail A.S., Al-Asgah N.A., Abdel-Warith A.A., Al-Hafedh Y.S. (2018). Effect of dietary fish meal replacement by red algae (Gracilaria arcuate), on growth performance and body composition of Nile tilapia (Oreochromis niloticus). Saudi J. Biol. Sci., 25: 198–203.
  73. Zamannejad N., Emadi H., Hosseinzade Sahafi O. (2016). Effects of Sargassum illicifolium algae feeding on IgM level and lysozyme activity in rainbow trout (Oncorhynchus mykiss). JMST, 10: 59–70.
  74. Zhong H., Lou C., Ren B., Zhou Y. (2022). Insulin-like growth factor 1 injection changes gene expression related to amino acid transporting, complement and coagulation cascade in the stomach of tilapia revealed by RNA-seq. Front Immunol., 9: 959717.
  75. Zhou Z., Pan S., Wu S. (2020). Modulation of the growth performance, body composition and nonspecific immunity of crucian carp Carassius auratus upon Enteromorpha prolifera polysaccharide. Int. J. Biol. Macromol., 147: 29–33.
DOI: https://doi.org/10.2478/aoas-2024-0070 | Journal eISSN: 2300-8733 | Journal ISSN: 1642-3402
Language: English
Page range: 317 - 327
Submitted on: Jan 12, 2024
|
Accepted on: Jun 10, 2024
|
Published on: Jan 22, 2025
In partnership with: Paradigm Publishing Services
Publication frequency: Volume open

© 2025 Roghieh Safari, Seyed Hossein Hoseinifar, Ali Shabani, Hamed Ghafarifarsani, Mehdi Raissy, Seyed Reza Khaleghi, Hien Van Doan, Metin Yazici, Mina Rahbar, Mehdi Nouri, published by National Research Institute of Animal Production
This work is licensed under the Creative Commons Attribution 4.0 License.