Skip to main content
SpringerLink
Log in

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

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

This study was carried out to investigate and compare the effect of water-soluble polysaccharides extract of the green alga, Ulva rigida (WPU), as a dietary supplement on growth performance, antioxidant enzyme activity, non-specific immune responses, and disease resistance of juvenile grey mullet, Mugil cephalus, subjected to bacterial infection with Photobacterium damselae. Three replicate groups of fish (initial mean weight, 15 ± 0.1 g) were fed with four isonitrogenous and isolipidic diets containing four levels, 0 or control, 5, 10, and 15 mg kg−1 of WPU (WPU0 or control, WPU5, WPU10, and WPU15) for 8 weeks over the growth trial. Thereafter, ten fish from each dietary treatment were infected with bacteria P. damselae to evaluate disease resistance of infected fish. Feeding grey mullet at 10 mg kg−1 WPU level (WPU10 diets) produced higher weight gain (211.36 ± 6%), specific growth rate (1.88 ± 0.03%) and protein efficiency ratio (4.26 ± 0.1%) compare to the control group. The diets supplemented with three levels of WPU-stimulated lysozyme, phagocytic, and respiratory burst activity of fish, but, the stimulatory capacities of the extracts varied greatly, depending on the concentrations used and diet; WPU10 was higher than WPU 5 and WPU15 diets. The best responses in antioxidant enzyme activities of superoxide dismutase (4.8 U mL−1), glutathione (3.6 U mL−1), and malondialdehyde (25.0 U mL−1) were induced by the extracts obtained from WPU10 diet. In addition, using WPU extract in all diets decreased mortality in M. cephalus in a dose-dependent manner after challenge with P. damselae. These results suggest that the use of water-soluble polysaccharides from U. rigida at 10 mg kg−1 dose improve growth, immune responses, and antioxidant activity in M. cephalus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abbassa A-H (2006) The impact of striped mullet, Mugil cephalus on natural food and phytoplankton selectivity at different feeding regimes in earthen fishponds. J Fish Aquat Sci 1:87–96

    Article  Google Scholar 

  • Alderman D, Hastings T (1998) Antibiotic use in aquaculture: development of antibiotic resistance–potential for consumer health risks. Int J Food Sci Technol 33:139–155

    Article  CAS  Google Scholar 

  • Ardó L, Yin G, Xu P, Váradi L, Szigeti G, Jeney Z, Jeney G (2008) Chinese herbs (Astragalus membranaceus and Lonicera japonica) and boron enhance the non-specific immune response of Nile tilapia (Oreochromis niloticus) and resistance against Aeromonas hydrophila. Aquaculture 275:26–33

    Article  Google Scholar 

  • Austin B, Austin D (2007) Bacterial fish pathogens: diseases of farmed and wild fish. Springer, Cham, pp 15–46

    Google Scholar 

  • Bikker P, van Krimpen MM, van Wikselaar P, Houweling-Tan B, Scaccia N, van Hal JW, Huijgen WJ, Cone JW, López-Contreras AM (2016) Biorefinery of the green seaweed Ulva lactuca to produce animal feed, chemicals and biofuels. J Appl Phycol 28:3511–3525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyd CE, Massaut L (1999) Risks associated with the use of chemicals in pond aquaculture. Aquac Eng 20:113–132

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Bricknell I, Dalmo RA (2005) The use of immunostimulants in fish larval aquaculture. Fish Shellfish Immunol 19:457–472

    Article  CAS  PubMed  Google Scholar 

  • Cabello FC (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8:1137–1144

    Article  CAS  PubMed  Google Scholar 

  • Castro R, Piazzon M, Zarra I, Leiro J, Noya M, Lamas J (2006) Stimulation of turbot phagocytes by Ulva rigida C. Agardh polysaccharides. Aquaculture 254:9–20

    Article  CAS  Google Scholar 

  • Castro R, Zarra I, Lamas J (2004) Water-soluble seaweed extracts modulate the respiratory burst activity of turbot phagocytes. Aquaculture 229:67–78

    Article  Google Scholar 

  • Crosetti D (2016) Current state of grey mullet fisheries and culture. In: Biology, Ecology and Culture of Grey Mullets (Mugilidae). CRC Press, Boca Raton pp 398–450

  • Quezada-Rodríguez P, Fajer-Ávila EJ (2017) The dietary effect of ulvan from Ulva clathrata on hematological-immunological parameters and growth of tilapia (Oreochromis niloticus). J Appl Phycol 29:423–431

    Article  Google Scholar 

  • Dügenci SK, Arda N, Candan A (2003) Some medicinal plants as immunostimulant for fish. J Ethnopharmacol 88:99–106

    Article  PubMed  Google Scholar 

  • El Zarka S, Fahmy FK (1968) Experiments in the culture of the grey mullet Mugil cephalus in brackishwater ponds in the UAR. FAO Fish Rep 44(5):255–266

    Google Scholar 

  • Ellis AE (1990) Lysozyme assays. Techn Fish Immunol 1:101–103

    Google Scholar 

  • Ergün S, Soyutürk M, Güroy B, Güroy D, Merrifield D (2009) Influence of Ulva meal on growth, feed utilization, and body composition of juvenile Nile tilapia (Oreochromis niloticus) at two levels of dietary lipid. Aquac Int 17:355

    Article  Google Scholar 

  • Kakoolaki S, Akbary P, Zorriehzahra MJ, Salehi H, Sepahdari A, Afsharnasab M, Mehrabi MR, Jadgal S (2016) Camellia sinensis supplemented diet enhances the innate non-specific responses, haematological parameters and growth performance in Mugil cephalus against Photobacterium damselae. Fish Shellfish Immunol 57:379–385

    Article  CAS  PubMed  Google Scholar 

  • Kim D-H, Austin B (2006) Innate immune responses in rainbow trout (Oncorhynchus mykiss, Walbaum) induced by probiotics. Fish Shellfish Immunol 21:513–524

    Article  CAS  PubMed  Google Scholar 

  • Kokabi M, Yousefzadi M (2015) Checklist of the marine macroalgae of Iran. Bot Mar 58:307–320

    Article  Google Scholar 

  • Lahaye M, Robic A (2007) Structure and functional properties of ulvan, a polysaccharide from green seaweeds. Biomacromolecules 8:1765–1774

    Article  CAS  PubMed  Google Scholar 

  • Liao IC, Chao NH, Tseng CC (2016) Capture and culture of Mugilidae in Taiwan. In: Biology, Ecology and Culture of Grey Mullets (Mugilidae). CRC Press, Boca Raton pp 487–500

  • Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157:2893–2902

    Article  CAS  PubMed  Google Scholar 

  • Moffitt CM, Cajas-Cano L (2014) Blue growth: the 2014 FAO state of world fisheries and aquaculture. Fisheries 39:552–553

    Article  Google Scholar 

  • Parry RM Jr, Chandan RC, Shahani KM (1965) A rapid and sensitive assay of muramidase. Proc Soc Exp Biol Med 119:384–386

    Article  CAS  PubMed  Google Scholar 

  • Peixoto MJ, Svendsen JC, Malte H, Pereira LF, Carvalho P, Pereira R, Gonçalves JF, Ozório RO (2016) Diets supplemented with seaweed affect metabolic rate, innate immune, and antioxidant responses, but not individual growth rate in European seabass (Dicentrarchus labrax). J Appl Phycol 28:2061–2071

    Article  CAS  Google Scholar 

  • Pérez MJ, Falqué E, Domínguez H (2016) Antimicrobial action of compounds from marine seaweed. Mar Drugs 14(3):52

    Article  PubMed Central  Google Scholar 

  • Qi H, Zhang Q, Zhao T, Hu R, Zhang K, Li Z (2006) In vitro antioxidant activity of acetylated and benzoylated derivatives of polysaccharide extracted from Ulva pertusa (Chlorophyta). Bioorg Med Chem Lett 16:2441–2445

    Article  CAS  PubMed  Google Scholar 

  • Qi H, Zhao T, Zhang Q, Li Z, Zhao Z, Xing R (2005) Antioxidant activity of different molecular weight sulfated polysaccharides from Ulva pertusa Kjellm (Chlorophyta). J Appl Phycol 17:527–534

    Article  CAS  Google Scholar 

  • Reverter M, Bontemps N, Lecchini D, Banaigs B, Sasal P (2014) Use of plant extracts in fish aquaculture as an alternative to chemotherapy: current status and future perspectives. Aquaculture 433:50–61

    Article  Google Scholar 

  • Sakai M (1999) Current research status of fish immunostimulants. Aquaculture 172(1):63–92

    Article  CAS  Google Scholar 

  • Secombes CJ (1990) Isolation of salmonid macrophages and analysis of their killing activity. Techn Fish Immunol 1:137–154

    Google Scholar 

  • Tabarsa M, Han JH, Kim CY, You SG (2012) Molecular characteristics and immunomodulatory activities of water-soluble sulfated polysaccharides from Ulva pertusa. J Med Food 15:135–144

    Article  CAS  PubMed  Google Scholar 

  • Thirunavukkarasu R, Pandiyan P, Balaraman D, Jayaraman I, Subaramaniyan K, George EGJ (2015) Enhancements of non-specific immune response in Mugil cephlus by using seaweed extract protection against Vibrio alginolyticus (BRTR07). J Coast Life Med 3:776–786

  • Trevisani M, Mancusi R, Cecchini M, Costanza C, Prearo M (2017) Detection and characterization of histamine-producing strains of Photobacterium damselae sub sp. damselae isolated from mullets. Vet Sci 4(2):31

    Article  PubMed Central  Google Scholar 

  • Vatsos IN, Rebours C (2015) Seaweed extracts as antimicrobial agents in aquaculture. J Appl Phycol 27:2017–2035

    Article  CAS  Google Scholar 

  • Wassef EA, El-Sayed A-FM, Sakr EM (2013) Pterocladia (Rhodophyta) and Ulva (Chlorophyta) as feed supplements for European seabass, Dicentrarchus labrax L., fry. J Appl Phycol 25:1369–1376

    Article  CAS  Google Scholar 

  • Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982

    Article  CAS  PubMed  Google Scholar 

  • Yaich H, Garna H, Besbes S, Paquot M, Blecker C, Attia H (2013) Effect of extraction conditions on the yield and purity of ulvan extracted from Ulva lactuca. Food Hydrocoll 31:375–382

    Article  CAS  Google Scholar 

  • Yangthong M, Hutadilok-Towatana N, Thawonsuwan J, Phromkunthong W (2016) An aqueous extract from Sargassum sp. enhances the immune response and resistance against Streptococcus iniae in the Asian sea bass (Lates calcarifer Bloch). J Appl Phycol 28:3587–3598

    Article  CAS  Google Scholar 

  • Zhu D, Wen X, Xuan X, Li S, Li Y (2016) The green alga Ulva lactuca as a potential ingredient in diets for juvenile white spotted snapper Lutjanus stellatus Akazaki. J Appl Phycol 28:703–711

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge the generous support of Iranian Fisheries Sciences Research Institute (IFSRI) for the project no: 0-12-12-9353.

Author information

Authors and Affiliations

  1. Department of Marine Sciences, Fisheries Group, Chabahar Maritime University, Chabahar, Iran

    Paria Akbary

  2. Agricultural Research Education and Extension Organization (AREEO), Iranian Fisheries Science Research Institute (IFSRI), Offshore Research Center, Chabahar, Iran

    Zahra Aminikhoei

Authors
  1. Paria Akbary
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zahra Aminikhoei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paria Akbary.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akbary, P., Aminikhoei, Z. 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 (2018). https://doi.org/10.1007/s10811-017-1299-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1299-8

Keywords

Search

Navigation