Skip to main content
Log in

Adaptation of the black tiger shrimp, Penaeus monodon, to different salinities through an excretory function of the antennal gland

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Black tiger shrimps (Penaeus monodon) are able to survive and can be reared under various salinities, possibly by the cellular adaptation of their excretory system, particularly the antennal gland, which is known to regulate body fluid in crustaceans. We have investigated the morphological and biochemical alterations of the antennal glands in shrimp reared in 7, 15, or 30 ppt seawater. Drastic changes occur in animals reared under 7 ppt conditions. Ultrastructural studies of the antennal gland in shrimps reared in 7 ppt seawater have revealed that podocytic cells in the coelomosacs ramify with more cytoplasmic processes forming the filtration slits, and that the tubular labyrinth cells possess more mitochondria in their basal striation and a wider tubular lumen than those found in the other groups. Many apical cytoplasmic blebs from labyrinth cells have also been seen in the lumen of the labyrinths under 7 ppt conditions, a feature that is not as prominent under the other conditions. The expression and activity of the Na+/K+-ATPase in the antennal gland are also correlated with the surrounding environment: the lower the salinity, the higher the expression and activity of the enzyme. Immunohistochemistry results have demonstrated the highest staining intensity in the labyrinth cells of shrimps reared under 7 ppt conditions. Our findings thus suggest that one of the adaptation mechanisms of this shrimp to the surrounding salinity is the regulation of Na+/K+-ATPase expression in the antennal gland, in conjunction with subcellular changes in its excretory cells.

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

Similar content being viewed by others

References

  • Behnke RD, Busquets-Turner L, Ahearn GA (1998) Epithelial glucose transport by lobster antennal gland. J Exp Biol 201:3385–3393

    CAS  PubMed  Google Scholar 

  • Binns R (1969) The physiology of the antennal gland of Carcinus maenas. III. Glucose reabsorption. J Exp Biol 51:17–25

    CAS  Google Scholar 

  • Blanco G, Mercer RW (1998) Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function. Am J Physiol 275:F633–F650

    Google Scholar 

  • Charmantier G, Haond C, Lignot JH, Charmantier-Daures M (2001) Ecophysiological adaptation to salinity throughout a life cycle: a review in homarid lobsters. J Exp Biol 204:967–977

    CAS  PubMed  Google Scholar 

  • Chen JC, Lin MN, Ting YY, Lin JN (1995) Survival, haemolymph osmolality and tissue water of Penaeus chinensis juvenile acclimated to different salinity and temperature levels. Comp Biochem Physiol 110:253–258

    Article  Google Scholar 

  • Cieluch U, Anger K, Aujoulat F, Buchholz F, Charmantier-Daures M, Charmantier G (2004) Ontogeny of osmoregulatory structures and functions in the green crab Carcinus maenas (Crustacea, Decapoda). J Exp Biol 207:325–336

    Article  CAS  PubMed  Google Scholar 

  • Fambrough DM, Lemas MV, Takeyasu K, Renaud K, Inman EM (1994) Structural requirements for subunit assembly of the Na+/K+-ATPase. Curr Top Membr Trans 41:45–69

    CAS  Google Scholar 

  • Fuller EG, Highison GJ, Brown F, Bayer C (1989) Ultrastructure of the crayfish antennal gland revealed by scanning and transmission electron microscopy combined with ultrasonic microdissection. J Morphol 200:9–15

    Article  Google Scholar 

  • Harris RR, Santos MCF (1993) Sodium uptake and transport (Na++K+)ATPase changes following Na+ depletion and low salinity acclimation in the mangrove crab Ucides cordatus (L.). Comp Biochem Physiol 105:35–42

    Article  Google Scholar 

  • Holliday CW (1985) Salinity-induced changes in gill Na+/K+-ATPase activity in the mud fidder crab, Uca pugnax. J Exp Zool 233:199–208

    Article  CAS  Google Scholar 

  • Horisberger JD, Lemas V, Kraehenbuhl JP, Rossier BC (1991) Structure-function relationship of Na, K-ATPase. Annu Rev Physiol 53:565–584

    Article  CAS  PubMed  Google Scholar 

  • Khodabandeh S, Charmantier G, Blasco C, Grousset E, Charmantier-Daures M (2005a) Ontogeny of the antennal glands in the crayfish, Astacus leptodactylus (Crustacea, Decapoda): anatomical and cell differentiation. Cell Tissue Res 319:153–165

    Article  CAS  PubMed  Google Scholar 

  • Khodabandeh S, Charmantier G, Charmantier-Daures M (2005b) Ultrastructural studies and Na+/K+-ATPase immunolocalization in the antennal urinary glands of the lobster Homarus gammarus (Crustacea, Decapoda). J Histochem Cytochem 53:1203–1214

    Article  CAS  PubMed  Google Scholar 

  • Kumlu M, Eroldogan OT, Aktas M (1999) The effect of salinity on larval growth, survival and development of Penaeus semisulcatus (Decapoda: Penaeidae). Isr J Aquac-Bamidgeh 51:114–121

    Google Scholar 

  • Lemos D, Phan VN, Alvares G (2001) Growth, oxygen consumption, ammonia excretion, biochemical composition and energy content of Farfantepenaeus paulensis (Crustacea Decapoda: Penaeidae). Marine Biol 138:985–997

    Article  CAS  Google Scholar 

  • Lin SC, Liou CH, Cheng JH (2000) The role of the antennal glands in ion and body volume regulation of cannulated Penaeus monodon reared in various salinity conditions. Comp Biochem Physiol 127:121–129

    Article  CAS  Google Scholar 

  • Lucu C, Towle DW (2003) Na+/K+-ATPase in gills of aquatic crustacean. Comp Biochem Physiol 135A:195–214

    CAS  Google Scholar 

  • Mantel LH, Farmer LL (1983) Osmotic and ionic regulation. In: Bliss DE (ed) The biology of Crustacea, vol 5. Academic Press, New York

    Google Scholar 

  • Norfolk JRW, Craik JCA (1980) Investigation of the control of the urine production in the shore line crab, Carcinus maenas L. Comp Biochem Physiol 67A:141–148

    Article  Google Scholar 

  • O’Brien CJ (1994) The effects of temperature and salinity on growth and survival of juvenile tiger prawn Penaeus esculentus (Haswall). J Exp Mar Biol Ecol 183:133–145

    Article  Google Scholar 

  • Palacios E, Bonilla A, Luna D, Racotta IS (2004) Survival, Na+/K+-ATPase and lipid responses to salinity challenge in fed and starved white Pacific shrimp (Litopenaeus vannamei) postlarvae. Aquaculture 234:497–511

    Article  CAS  Google Scholar 

  • Péqueux A (1995) Osmotic regulation in crustaceans. J Crust Biol 15:1–60

    Article  Google Scholar 

  • Peterson DR, Loizzi RF (1974) Ultrastructure of the crayfish kidney, coelomosac, labyrinth, and nephridial canal. J Morphol 142:241–264

    Article  CAS  PubMed  Google Scholar 

  • Ponce-Palafor J, Martinez-Palacios CA, Ross LG (1997) The effects of salinity and temperature on the growth and survival rates of juvenile white shrimp, Penaeus vannamei, Boone, 1931. Aquaculture 157:107–115

    Article  Google Scholar 

  • Riegel JA (1963) Micropuncture studies of chloride concentration and osmotic pressure in the crayfish antennal gland. J Exp Biol 40:487–492

    CAS  PubMed  Google Scholar 

  • Riegel JA, Cook MA (1975) Recent studies of excretion in crustaceans. Fortschr Zool 23:48–75

    CAS  Google Scholar 

  • Sang HM, Fotedar R (2004) Growth, survival, haemolymph osmolality and organosomatic indices of the western king prawn (Penaeus latisulcatus Kishinouye, 1896) reared at different salinities. Aquaculture 234:601–614

    Article  Google Scholar 

  • Sarver RG, Flynn MA, Holliday CW (1994) Renal Na, K-ATPase and osmoregulation in the crayfish, Procambarus clarkii. Comp Biochem Physiol 107:349–356

    Article  Google Scholar 

  • Schmidt-Nielsen B, Gertz KH, Davis LE (1968) Excretion and ultrastructure of the antennal gland of the fiddler crab Uca mordax. J Morphol 125:473–96

    Article  CAS  PubMed  Google Scholar 

  • Sesma P, Bayona C, Villaro AC, Vazquez JJ (1983) A microscopic study on the antennal gland of Antrapotamobius ballines (Crustacea Decapoda). Morf Normal Patolog 7:289–301

    Google Scholar 

  • Setiarto A, Strussmann CA, Takashima F, Watanabe S, Yokota M (2004) Short-term responses of adult kuruma shrimp Marsupenaeus japonicus (Bate) to environmental salinity: osmotic regulation, oxygen consumption and ammonia excretion. Aquacult Res 35:669–677

    Article  Google Scholar 

  • Towle DW (1990) Sodium transport systems in gills. In: Kinne RKH (ed) Comparative aspects of sodium cotransport system. Karger, Basel, pp 241–263

    Google Scholar 

  • Towle DW, Paulsen RS, Weihrauch D, Kordylewski M, Salvador C, Lignot JH, Spanings-Pierrot C (2001) Na++K+-ATPase in gills of the blue crab Callinectes sapidus: cDNA sequencing and salinity-related expression of α-subunit mRNA and protein. J Exp Biol 204:4005–4012

    CAS  PubMed  Google Scholar 

  • Ueno M, Inoue Y (1996) The fine structure of podocytes in crayfish antennal glands. J Electron Microsc 45:395–400

    Google Scholar 

  • Wheatly MG, Henry RP (1987) Branchial and antennal gland Na+/K+-dependent ATPase and carbonic anhydrase activity during salinity acclimation of the euryhaline crayfish Pacifastacus leniusculus. J Exp Biol 133:73–86

    CAS  Google Scholar 

  • Zhang S, Dang S, Wang F (1999) The effects of salinity and food on carbon budget of Penaeus chinensis. J Fish China 23:144–149

    Google Scholar 

Download references

Acknowledgements

The authors thank Prof. Perter Hanna, Deakin University, Geelong, Australia, for his valuable suggestions and proofreading this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Somluk Asuvapongpatana.

Additional information

This study was supported by an Initiative Grant from Mahidol University and the Thailand Research Fund (TRF).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buranajitpirom, D., Asuvapongpatana, S., Weerachatyanukul, W. et al. Adaptation of the black tiger shrimp, Penaeus monodon, to different salinities through an excretory function of the antennal gland. Cell Tissue Res 340, 481–489 (2010). https://doi.org/10.1007/s00441-010-0971-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-010-0971-y

Keywords

Navigation