Skip to main content
Log in

Identification of haematological markers in shrimp health assessment from the immune profile of Fenneropenaeus indicus on β-1,3-glucan administration and white spot syndrome virus challenge

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Haematological alterations in Fenneropenaeus indicus fed marine yeast glucan-incorporated diet and challenged with white spot syndrome virus were analysed. Adult F. indicus 16.45 ± 2.12 g (mean ± SD) were reared in 25 ‰ sea water and allowed to acclimate for a period of 7 days. Diet was prepared incorporating glucan (0.2 %) extracted from marine yeast, Debaryomyces hansenii S169. The shrimps were reared on experimental diet for 28 days and then challenged with white spot syndrome virus through oral administration. Random sampling was done (n = 6 shrimps) on 1st, 15th and 28th day of the experiment and on post-challenge day 2 (PCD 2) and PCD 7 for haematological analysis. The immune parameters viz. plasma protein, total haemocyte count, phenoloxidase activity, superoxide anion production, alkaline phosphatase and acid phosphatase activities were estimated in the haemolymph. Superoxide dismutase, catalase, glutathione peroxidase, hydroperoxide, conjugated dienes and malondialdehyde concentrations in the haemolymph of shrimps were also analysed. Analysis of variance showed that there are significant differences (p < 0.05) in the immune and antioxidant parameters in different treatment groups of F. indicus. The shrimps fed glucan-incorporated diet showed higher survival rate with comparatively lower accumulation of lipid peroxidation products. Correlation coefficients showed that all haematological variables except hydroperoxides and conjugated dienes exhibited positive correlation with the survival rate. The immune variables and antioxidant parameters exhibited a greater degree of correlation with each other. When multiple regression of survival rate on all immune parameters was considered, the amount of variability explained was 93 % (R Square = 0.932). When significant regression coefficients among the immune parameters were taken into account, it was found that total haemocyte count (p < 0.001), phenoloxidase activity (p < 0.05), alkaline phosphatase activity (p < 0.05) and plasma protein concentration (p < 0.05) together are explaining 84 % (R 2 = 0.842) of the variability, indicating that these four parameters are mainly supporting the survival. The amount of variability explained by the antioxidant parameters was 94 % (R 2 = 0.938). When significant regression coefficients among the antioxidant parameters were taken into account, it was found that superoxide dismutase activity (p < 0.01) and catalase activity (p < 0.05) together are explaining 87.4 % (R 2 = 0.874) of the variability, indicating that these two antioxidants act as the major immune effectors supporting the survival in shrimps.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13

Similar content being viewed by others

References

  • APHA (1995) In: Eaton AD, Clescenri LS, Greenberg AE (eds) Standard methods for the examination of water and wastewater. American Public Health Association, Washington

  • Beckage NE (1996) Interactions of viruses with invertebrate cells. In: Soderhall K, Iwanaga S, Vasta GR (eds) New directions in invertebrate immunology, SOS Publication, New York, pp 375–399

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

    Article  PubMed  CAS  Google Scholar 

  • Campa-Cordova AI, Hernandez-Saavedra NY, De Philippis R, Ascencio F (2002) Generation of superoxide anion and SOD activity in haemocytes and muscle of American white shrimp (Litopenaeus vannamei) as a response to β-glucan and sulphated polysaccharide. Fish Shellfish Immunol 12:353–366

    Article  PubMed  CAS  Google Scholar 

  • Chang CF, Su MS, Chen HY (1999) A rapid method to quantify total haemocyte count of Penaeus monodon using ATP analysis. Fish Pathol 34:211–212

    Article  Google Scholar 

  • Chang CF, Chen HY, Su MS, Liao IC (2000) Immunomodulation by dietary β-1,3-glucan in the brooders of the black tiger shrimp, Penaeus monodon. Fish Shellfish Immunol 10:505–514

    Article  PubMed  CAS  Google Scholar 

  • Chang CF, Su MS, Chen HY, Liao IC (2003) Dietary-1,3-glucan effectively improves immunity and survival of Penaeus monodon challenged with white spot syndrome virus. Fish Shellfish Immunol 15:297–310

    Article  PubMed  CAS  Google Scholar 

  • Dalmo RA, Bogwald J (2008) Beta-glucans as conductors of immune symphonies. Fish Shellfish Immunol 25:384–396

    Article  PubMed  CAS  Google Scholar 

  • Dandapat J, Chainy GBN, Rao KJ (2003) Lipid peroxidation and antioxidant defence status during larval development and metamorphosis of giant prawn Macrobrachium rosenbergii. Comp Biochem Physiol C 135:221–233

    Article  Google Scholar 

  • Fridovich I (1989) Superoxide dismutases an adaptation to a paramagnetic gas. J Biol Chem 264:7761–7764

    PubMed  CAS  Google Scholar 

  • Gonzalez F, Esther Ferez-Vidal M, Arias JM, Mantoya E (1994) Partial purification and biochemical properties of acid and alkaline phosphatases from Myxococcus coralloides D. J Appl Bacteriol 77:567–573

    Article  CAS  Google Scholar 

  • Hall MR, van Ham EH (1998) The effects of different types of stress on blood glucose in the giant tiger prawn Penaeus monodon. J World Aquacult Soc 29:290–299

    Article  Google Scholar 

  • Itami T, Takahashi Y, Tsuchihira E, Igusa H (1994) Enhancement of disease resistance of kuruma prawn Penaeus japonicus and increase in phagocytic activity of prawn haemocytes after oral administration of β-1,3-glucan (Schizophyllan). In: Chou LM, Munro AD, Lam TJ, Chen TW, Cheong LKK, Ding JK, Hooi KK, Khoo HW, Phang VPE, Shim KF, Tan CH (eds) Proceedings of the third Asian Fisheries Forum, Singapore, 26–30 October 1992. Asian Fisheries Society, Manila, pp 375–378

  • Itami T, Asano M, Tokushige K (1998) Enhancement of disease resistance of Kuruma shrimp, Penaeus japonicus after oral administration of peptidoglycan derived from Bifidobacterium thermophilum. Aquaculture 164:277–288

    Article  CAS  Google Scholar 

  • Kakkar P, Das B, Viswanathan DN (1984) A Modified spectrometric assay of superoxide dismutase. Ind J Biochem Biophys 21:130

    CAS  Google Scholar 

  • Le Moullac G, Haffner P (2000) Environmental factors affecting immune response in crustacea. Aquaculture 191:12–131

    Article  Google Scholar 

  • Le Moullac G, Soyez C, Saulnier D (1998) Effect of hypoxic stress on the immune response and the resistance to vibriosis of the shrimp Penaeus stylirostris. Fish Shellfish Immunol 8:621–629

    Article  Google Scholar 

  • Lin T, Xing J, Jiang J, Tang X, Zhan W (2011) β-glucan-stimulated activation of six enzymes in the haemocytes of the scallop Chlamys farreri at different water temperatures. Aquaculture 315:213–221

    Article  CAS  Google Scholar 

  • Liu SQ, Jiang XL, Mou HJ, Wang HM, Guan HS (1999) Effects of immunopolysaccharide on LSZ, ALP, ACP and POD activity of Penaeus chinensis serum. Oceanol Limnol Sinica 30:278–283

    CAS  Google Scholar 

  • Liu XL, Xi QY, Yang L, Li HY, Jiang QY, Shu G, Wang SB, Gao P, Zhu XT, Zhang YL (2011) The effect of dietary Panax ginseng polysaccharide extract on the immune responses in white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 30:495–500

    Article  PubMed  CAS  Google Scholar 

  • Lo CF, Leu JH, Ho CH, Chen CH (1996) Detection of baculovirus associated with white spot syndrome (WSBV) in penaeid shrimps using polymerase chain reaction. Dis Aquat Org 25:133–141

    Article  CAS  Google Scholar 

  • Lo CF, Ho CH, Chen CH, Liu KF, Chiu YL, Yeh PY (1997) Detection and tissue tropism of white spot syndrome baculovirus (WSBV) in captured brooders of Penaeus monodon with a special emphasis on reproductive organ. Dis Aquat Org 30:53–72

    Article  Google Scholar 

  • Machly AC, Chance B (1955) Assay of catalases and peroxidases. In: Colowick SP, Kaplan NO (eds) Methods of biochemical Analysis, vol 2, Academic Press, New York, pp 764

  • Mair RD, Hall T (1977) In: Swem C, Witky (eds) Inorganic peroxides. Intersciences, New York, pp 532

  • Mar Costa M, Novoa B, Figueras A (2008) Influence of β-glucans on the immune responses of carpet shell clam (Ruditapes decussatus) and Mediterranean mussel (Mytilus galloprovincialis). Fish Shellfish Immunol 24:498–505

    Article  PubMed  CAS  Google Scholar 

  • Mathew S, Ashok Kumar K, Anandan R, Viswanathan Nair PG, Devadasan K (2007) Changes in tissue defence system in white spot syndrome virus (WSSV) infected Penaeus monodon. Comp Biochem Physiol C 145:315–320

    Google Scholar 

  • Misra CK, Das BK, Pradhan J, Pattnaik P, Sethi S, Mukherjee SC (2004) Changes inlysosomal enzyme activity and protection against Vibrio infection in Macrobrachium rosenbergii (De Man) post larvae after bath immunostimulation with β-glucan. Fish Shellfish Immunol 17:389–395

    Article  PubMed  CAS  Google Scholar 

  • Niehaus WG Jr, Samuelson B (1968) Formation of malondialdehyde from phospholipids arachidonate during microsomal lipid peroxidation. Eur J Biochem 6:126

    Article  PubMed  CAS  Google Scholar 

  • Rajan PR, Ramasamy P, Purusothaman V, Brennan GP (2000) White spot baculovirus syndrome virus in the Indian shrimp Penaeus monodon and Penaeus indicus. Aquaculture 184:31–44

    Article  Google Scholar 

  • Recknagel RO, Ghoshal AK (1966) Quantitative estimation of peroxidative degeneration of rat liver micosomal and mitochondrial lipids after carbon tetrachloride poisoning. Exp Mol Path 5:413–426

    Article  CAS  Google Scholar 

  • Robertson L, Bray W, Leung-Trujillo J, Lawrence J (1987) A practical molt staging of Penaeus setiferus and Penaeus stylirostris. J World Aquacult Soc 18:180–185

    Article  Google Scholar 

  • Roch P (1999) Defense mechanisms and disease prevention in farmed marine invertebrates. Aquaculture 172:125–145

    Article  Google Scholar 

  • Rotruck JT (1973) Selenium: biochemical role as a component of glutathione peroxidase. Science 179:588–590

    Article  PubMed  CAS  Google Scholar 

  • Sajeevan TP, Philip R, Singh ISB (2006) Immunostimulatory effect of a marine yeast Candida sake S165 in Fenneropenaeus indicus. Aquaculture 257:150–155

    Article  Google Scholar 

  • Sajeevan TP, Subramannian S, Philip R (2010) β-Mercapto-ethanol-treated yeast showed better protection against white spot syndrome virus infection in Indian white shrimp Fenneropenaeus indicus. Aquacult Res 41(10):e715–e718

    CAS  Google Scholar 

  • Sang HM, Ky TL, Fotedar R (2009) Dietary supplementation of mannan oligosaccharide improves the immune responses and survival of marron, Cherax tenuimanus (Smith, 1912) when challenged with different stressors. Fish Shellfish Immunol 27:341–348

    Article  PubMed  CAS  Google Scholar 

  • Shirali P, Teissier E, Marez T, Hildebrand HF, Haguenoer J (1994) Effect of alpha Ni3S2 on arachidonic acid metabolites in cultured human lung cells (L132 cell line). Carcinogenesis 15:759–762

    Article  PubMed  CAS  Google Scholar 

  • Smith VJ, Soderhall K (1983) β-1,3-glucan activation of crustacean haemocytes in vitro and in vivo. Biol Bullet 164:299–314

    Article  CAS  Google Scholar 

  • Soderhall K (1981) Fungal cell wall β-1,3-glucans induce clotting and phenoloxidase attachment to foreign surfaces of crayfish haemocyte lysate. Dev Comp Immunol 5:565–573

    PubMed  CAS  Google Scholar 

  • Soderhall K, Cerenius L (1998) Role of the prophenoloxidase activating system in invertebrate immunity. Curr Opin Immunol 10:23–28

    Article  PubMed  CAS  Google Scholar 

  • Song YL, Hsieh YT (1994) Immunostimulation of tiger shrimp, Penaeus monodon haemocytes for generation of microbicidal substances: analysis of reactive oxygen species. Dev Comp Immunol 18:201–209

    Article  PubMed  CAS  Google Scholar 

  • Song YL, Liu JJ, Chan LC, Sung HH (1997) Glucan-induced disease resistance in tiger shrimp, Penaeus monodon. Fish Vaccinol Dev Biol Stand 90:413–421

    CAS  Google Scholar 

  • Sung HH, Kou GH, Song YL (1994) Vibriosis resistance induced by glucan treatment in tiger shrimp, Penaeus monodon. Fish Pathol 29:11–17

    Article  CAS  Google Scholar 

  • Wang WN, Wang AL, Wang Y, Wang JX, Sun RY (2005) Effect of dietary vitamin C and ammonia concentration on the cellular defense response of Macrobrachium nipponense. J World Aquacult Soc 36(1):1–7

    Article  Google Scholar 

  • Williams DL, Mcnamee RB, Jones EL, Pretus HA, Ensley HE, Browder IW, Di Luzio NR (1991) A method for the solubilisation of a (1-3)-β-D-glucan isolated from Saccaromyces cerevisiae. Carbohydr Res 219:203–213

    Article  PubMed  CAS  Google Scholar 

  • Yadomae T, Ohno N (1996) Structure-activity relationship of immunomodulating (1,3)-β-glucans. Recent Res Dev Chem Pharm Sci 1:23–33

    Google Scholar 

  • Yemm EW, Cocking EC (1955) The determination of amino acids with ninhydrin. Analyst 80:209–213

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The work was supported by the University Grants Commission, India, through the award of JRF and SRF. The authors gratefully acknowledge Cochin University of Science and Technology for providing necessary facilities.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rosamma Philip.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Subramanian, S., Philip, R. Identification of haematological markers in shrimp health assessment from the immune profile of Fenneropenaeus indicus on β-1,3-glucan administration and white spot syndrome virus challenge. Aquacult Int 21, 1169–1184 (2013). https://doi.org/10.1007/s10499-013-9621-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-013-9621-1

Keywords

Navigation