Skip to main content
Log in

Alterations of pattern in immune response and vitellogenesis during induced ovarian development by unilateral and bilateral ablation in Litopenaeus vannamei

  • Original Article
  • Biology
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

Eyestalk ablation is often used to induce ovarian development in female shrimp, but it possibly alters the animal’s hormonal balance, and affects its physiology and immune system. Therefore, this study was conducted to investigate alterations to the immune response during induced ovarian development by unilateral and bilateral ablation in Litopenaeus vannamei. Sub-adult female shrimp could be induced to undergo ovarian development over a 20-day period by both unilateral and bilateral eyestalk ablation; however, ovaries did not reach the final mature stage in which cortical rods are observed. In terms of immune response, total hemocyte count decreased significantly at 4 h after unilateral ablation, and at 20 days after bilateral ablation. After 20 days, expression in the hemocytes of the immune-related genes prophenoloxidase and peroxinectin in bilaterally ablated shrimp increased significantly, whereas that for penaeidin, for lipopolysaccharide- and β-glucan-binding protein, and for transglutaminase mRNA expression did not change significantly. The results of this study suggest that, while eyestalk ablation induces ovarian development, it may also bring about a hormonal imbalance that leads to immune-related genes being activated.

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

Similar content being viewed by others

References

  1. FAO FIPS (2012) FAO year book: fishery and aquaculture statistics 2010. FAO, Rome

  2. Smith VJ, Brown JH, Hauton C (2003) Immunostimulation in crustaceans: does it really protect against infection? Fish Shellfish Immunol 15:71–90

    Article  PubMed  Google Scholar 

  3. Huang X, Zhou H, Zhang H (2006) The effect of Sargassum fusiforme polysaccharide extracts on vibriosis resistance and immune activity of the shrimp, Fenneropenaeus chinensis. Fish Shellfish Immunol 20:750–757

    Article  PubMed  CAS  Google Scholar 

  4. Tsutsui N, Kim YK, Jasmani S, Ohira T, Wilder MN, Aida K (2005) The dynamics of vitellogenin gene expression differs between intact and eyestalk ablated kuruma prawn Penaeus (Marsupenaeus) japonicus. Fish Sci 71:249–256

    Article  CAS  Google Scholar 

  5. Okumura T, Kim YK, Kawazoe I, Yamano K, Tsutsui N, Aida K (2006) Expression of vitellogenin and cortical rod proteins during induced ovarian development by eyestalk ablation in the kuruma prawn, Marsupenaeus japonicus. Comp Biochem Physiol A 143:245–253

    Google Scholar 

  6. Okumura T (2007) Effects of bilateral and unilateral eyestalk ablation on vitellogenin synthesis in immature female Kuruma prawns, Marsupenaeus japonicus. Zool Sci 24:233–240

    Article  PubMed  CAS  Google Scholar 

  7. Jayasankar V, Tsutui N, Jasmani S, Saido-Sakanaka H, Yang WJ, Okuno A, Hien TTT, Aida K, Wilder MN (2002) Dynamics of vitellogenin mRNA expression and changes in hemolymph vitellogenin levels during ovarian maturation in the giant freshwater prawn Macrobrachium rosenbergii. J Exp Zool 293:675–682

    Article  PubMed  CAS  Google Scholar 

  8. Jasmani S, Ohira T, Jayasankar V, Tsutsui N, Aida K, Wilder MN (2004) Localization of vitellogenin mRNA expression and vitellogenin uptake during ovarian maturation in the giant freshwater prawn, Macrobrachium rosenbergii. J Exp Zool 301A:334–343

    Article  CAS  Google Scholar 

  9. Uawisetwathana U, Leelatanawit R, Klanchui A, Prommoon J, Klinbunga S, Karoonuthaisiri N (2011) Insights into eyestalk ablation mechanism to induce ovarian maturation in the black tiger shrimp. PLoS One 6(9):e24427

    Article  PubMed  CAS  Google Scholar 

  10. Rosas C, Fernández I, Brito R, Iglesias ED (1993) The effect of eyestalk ablation on the energy balance of pink shrimp, Penaeus notiales. Comp Biochem Physiol 104A:183–187

    Article  Google Scholar 

  11. Perazzolo LM, Gargioni R, Ogliari P, Barranco MA (2002) Evaluation of some hemato-immunological parameters in the shrimp Farfantepenaeu paulensis submitted to environmental and physiological stress. Aquaculture 214:19–33

    Article  Google Scholar 

  12. Verghese B, Radhakrishnan EV, Padhi A (2008) Effect of moulting, eyestalk ablation, starvation and transportation on the immune response of the Indian spiny lobster, Panulirus homarus. Aquac Res 39:1009–1013

    Article  Google Scholar 

  13. Sainz-Hernández JC, Racotta IS, Dumas S, Hernández-López J (2008) Effect of unilateral and bilateral eyestalk ablation in Litopenaeus vannamei male and female on several metabolic and immunologic variables. Aquaculture 283:188–193

    Article  Google Scholar 

  14. Chan SM, Rankin SM, Keeley LL (1988) Characterization of the molt stages in Penaeus vannamei: setogenesis and hemolymph levels of total protein, ecdysteroids, and glucose. Biol Bull 175:185–192

    Google Scholar 

  15. Bell TA, Lightner DV (1988) A handbook of normal penaeid shrimp histology. World Aquac Soc, Baton Rouge

    Google Scholar 

  16. Tinikul Y, Poljaroen J, Kornthong N, Chotwiwatthanakun C, Anuracpreeda P, Poomtong T, Hanna PJ, Sobhon P (2011) Distribution and changes of serotonin and dopamine levels in the central nervous system and ovary of the Pacific white shrimp, Litopenaeus vannamei, during ovarian maturation cycle. Cell Tissue Res 345:103–124

    Article  PubMed  CAS  Google Scholar 

  17. Fingerman M (1997) Crustacean endocrinology: a retrospective, prospective and analysis. Physiol Zool 70:257–269

    PubMed  CAS  Google Scholar 

  18. Parnes S, Mills E, Segall C, Raviv S, Davis C, Sagi A (2004) Reproductive readiness of the shrimp Litopenaeus vannamei grown in a brackish water system. Aquaculture 236:593–606

    Article  Google Scholar 

  19. Raviv S, Parnes S, Segall C, Davis C, Sagi A (2006) Complete sequence of Litopenaeus vannamei (Crustacea: Decapoda) vitellogeninc DNA and its expression in endocrinologically induced sub-adult females. Gen Comp Endocrinol 145:39–50

    Article  PubMed  CAS  Google Scholar 

  20. Medina A, Vila Y, Mourente G, Rodríguez A (1996) A comparative study of the ovarian development in wild and pond-reared shrimp, Penaeus kerathurus (Forskål, 1775). Aquaculture 148:63–75

    Article  Google Scholar 

  21. Maggioni DS, Andreatta ER, Hermes EM, Barracco A (2004) Evaluation of some hemato-immunological parameters in female shrimp Litopenaeus vannamei submitted to unilateral eyestalk ablation in association with a diet supplemented with superdoses of ascorbic acid as a form of immunostimulation. Aquaculture 241:501–515

    Article  CAS  Google Scholar 

  22. Maningas MBB, Kondo H, Hirono I, Saito-Taki T, Aoki T (2008) Essential function of transglutaminase and clotting protein in shrimp immunity. Mol Immunol 45:1269–1275

    Article  PubMed  CAS  Google Scholar 

  23. Fagutao FF, Maningas MBB, Kondo H, Aoki T, Hirono I (2012) Transglutaminase regulates immune-related genes in shrimp. Fish Shellfish Immunol 32(5):711–715

    Article  PubMed  CAS  Google Scholar 

  24. Maningas MBB, Kondo H, Hirono I (2013) Molecular mechanisms of the shrimp clotting system. Fish Shellfish Immunol 34(4):968–972

    Article  PubMed  CAS  Google Scholar 

  25. Jiravanichpaisal P, Lee BL, Söderhäll K (2006) Cell-mediated immunity in arthropods:hematopoiesis, coagulation, melanization and opsonization. Immunobiology 211:213–236

    Article  PubMed  CAS  Google Scholar 

  26. Theopold U, Li D, Fabbri M, Scherfer C, Schmidt O (2002) The coagulation of insect hemolymph. Cell Mol Life Sci 59:363–672

    Article  PubMed  CAS  Google Scholar 

  27. Hall M, Wang R, van Antwerpen R, Sottrup-Jensen L, Soderhall K (1999) The crayfish plasma clotting protein: a vitellogenin-related protein responsible for clot formation in crustacean blood. Proc Natl Acad Sci USA 96:1965–1970

    Article  PubMed  CAS  Google Scholar 

  28. Hall M, Vanheusden MC, Söderhäll K (1995) Identification of the major lipoproteins in crayfish hemolymph as proteins involved in immune recognition and clotting. Biochem Biophys Res Commun 216:939–946

    Article  PubMed  CAS  Google Scholar 

  29. Iwanaga S, Lee BL (2005) Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol 38:128–150

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Ms. Hiroko Endo and Ms. Yoko Furusawa of the Japan International Research Center for Agricultural Sciences (JIRCAS) for their technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marcy N. Wilder.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bae, SH., Okutsu, T., Kang, B.J. et al. Alterations of pattern in immune response and vitellogenesis during induced ovarian development by unilateral and bilateral ablation in Litopenaeus vannamei . Fish Sci 79, 895–903 (2013). https://doi.org/10.1007/s12562-013-0652-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-013-0652-3

Keywords

Navigation