Advertisement

Cell and Tissue Research

, Volume 353, Issue 1, pp 87–98 | Cite as

Adaptation to freshwater in the palaemonid shrimp Macrobrachium amazonicum: comparative ontogeny of osmoregulatory organs

  • Nesrine Boudour-BouchekerEmail author
  • Viviane Boulo
  • Catherine Lorin-Nebel
  • Camille Elguero
  • Evelyse Grousset
  • Klaus Anger
  • Mireille Charmantier-Daures
  • Guy Charmantier
Regular Article

Abstract

The ontogeny of osmoregulatory organs was studied in two geographically isolated populations of the palaemonid shrimp Macrobrachium amazonicum, one originating from the Amazon estuary (A) and the other from inland waters of the Pantanal (P) in northeastern and southwestern Brazil, respectively. A previous investigation had shown that the estuarine population is able to hypo-osmoregulate in seawater, whereas the hololimnetic inland population has lost this physiological function. In the present study, the structural development of the branchial chamber and excretory glands and the presence of Na+/K+-ATPase (NKA) were compared between populations and between larval and juvenile stages after exposure to two salinities representing hypo- and hypertonic environments. In the newly hatched zoea I stage of both populations, gills were absent and NKA was localized along the inner epithelium of the branchiostegite. In intermediate (zoea V) and late larval stages (decapodids), significant differences between the two populations were observed in gill development and NKA expression. In juveniles, NKA was detected in the gills and branchiostegite, with no differences between populations. At all developmental stages and in both populations, NKA was present in the antennal glands upon hatching. The strong hypo-osmoregulatory capacity of the early developmental stages in population A could be linked to ion transport along the inner side of the branchiostegite; this seemed to be absent or weak in population P. The presence of fully functional gills expressing NKA appears to be essential for efficient hyper-osmoregulation in late developmental stages during successful freshwater adaptation and colonization.

Keywords

Osmoregulation Immunolocalization Branchial chamber Antennal gland Na+/K+-ATPase Crustaceans Macrobrachium amazonicum 

Notes

Acknowledgments

The authors are grateful to Dr. Liliam Hayd, State Univertsity of Mato Grosso do Sul, Aqudauana, Brazil, for transporting live shrimp from Brazil to Helgoland, to IBAMA (Brasília) for the permit to export shrimps, to Uwe Nettelmann for help in maintaining shrimp cultures and to Maryline Bossus for her advice.

References

  1. Anger K (2001) The biology of decapod crustacean larvae. Crustacean issues 14. Balkema, LisseGoogle Scholar
  2. Anger K (2013) Neotropical Macrobrachium (Caridea: Palaemonidae): on the biology, origin, and radiation of freshwater-invading shrimp. J Crust Biol (in press)Google Scholar
  3. Anger K, Hayd L (2010) Feeding and growth in early larval shrimp Macrobrachium amazonicum from the Pantanal, southwestern Brazil. Aquatic Biol 9:251–261CrossRefGoogle Scholar
  4. Anger K, Hayd L, Knott J, Nettelmann U (2009) Patterns of larval growth and chemical composition in the Amazon River prawn, Macrobrachium amazonicum. Aquaculture 287:341–348CrossRefGoogle Scholar
  5. Augusto A, Greene LJ, Laure HJ, McNamara JC (2007) The ontogeny of isosmotic intracellular regulation in the diadromous, freshwater Palaemonid shrimps, Macrobrachium amazonicum and M. olfersi (Decapoda). J Crust Biol 27:626–634CrossRefGoogle Scholar
  6. Augusto A, Pinheiro AS, Greene LJ, Laure HJ, McNamara JC (2009) Evolutionary transition to freshwater by ancestral marine palaemonids: evidence from osmoregulation in a tide pool shrimp. Aquatic Biol 7:113–122CrossRefGoogle Scholar
  7. Bauer R (2004) Remarkable shrimps: adaptations and natural history of the Carideans. University of Oklahoma Press, NormanGoogle Scholar
  8. Belli NM, Faleiros RO, Firmino KCS, Masui DC, Leone FA, McNamara JC, Furriel RPM (2009) Na+/K+-ATPase activity and epithelial interfaces in gills of the freshwater shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). Comp Biochem Physiol A 152:431–439CrossRefGoogle Scholar
  9. Bouaricha N, Charmantier-Daures M, Thuet P, Trilles J-P, Charmantier G (1994) Ontogeny of osmoregulatory structures in the shrimp Penaeus japonicus (Crustacea, Decapoda). Biol Bull 186:29–40CrossRefGoogle Scholar
  10. Charmantier G, Anger K (2011) Ontogeny of osmoregulatory patterns in the South American shrimp Macrobrachium amazonicum: loss of hypo-osmoregulation in a land-locked population indicates phylogenetic separation from estuarine ancestors. J Exp Marine Biol Ecol 396:89–98CrossRefGoogle Scholar
  11. Charmantier G, Charmantier-Daures M, Towle DW (2009) Osmotic and ionic regulation in aquatic arthropods. In: Evans DH (ed) Osmotic and ionic regulation: cells and animals. Taylor & Francis Group, London, pp 165–208Google Scholar
  12. 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 207:325–336PubMedCrossRefGoogle Scholar
  13. Cieluch U, Charmantier G, Grousset E, Charmantier-Daures M, Anger K (2005) Osmoregulation, immunolocalization of Na+/K+-ATPase, and ultrastructure of branchial epithelia in the developing brown shrimp, Crangon crangon (Decapoda, Caridea). Physiol Biochem Zool 78:1017–1025PubMedCrossRefGoogle Scholar
  14. Cieluch U, Anger K, Charmantier-Daures M, Charmantier G (2007) Osmoregulation and immunolocalization of Na+/K+-ATPase during the ontogeny of the mitten crab Eriocheir sinensis (Decapoda, Grapsoidea). Mar Ecol Progr Ser 329:169–178CrossRefGoogle Scholar
  15. Faleiros RO, Goldman MHS, Furriel RPM, McNamara JC (2010) Differential adjustment in gill Na+/K+- and V-ATPase activities and transporter mRNA expression during osmoregulatory acclimation in the cinnamon shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). J Expl Biol 213:3894–3905CrossRefGoogle Scholar
  16. Felder J, Felder D, Hand S (1986) Ontogeny of osmoregulation in the estuarine ghost shrimp Callianassa jamaicense var louisianensis Schmitt (Decapoda, Thalassinidae). J Exp Mar Biol 99:91–105CrossRefGoogle Scholar
  17. Freire CA, Cavassin F, Rodrigues EN, Torres AH, McNamara JC (2003) Adaptive patterns of osmotic and ionic regulation, and the invasion of fresh water by the palaemonid shrimps. Comp Biochem Physiol A 136:771–778CrossRefGoogle Scholar
  18. Freire CA, Onken H, McNamara JC (2008) A structure-function analysis of ion transport in crustacean gills and excretory organs. Comp Biochem Physiol A 151:272–304CrossRefGoogle Scholar
  19. 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 200:9–15CrossRefGoogle Scholar
  20. Haond C, Flik G, Charmantier G (1998) Confocal laser scanning and electron microscopical studies on osmoregulatory epithelia in the branchial cavity of the lobster Homarus gammarus. J Exp Biol 201:1817–1833PubMedGoogle Scholar
  21. Harris RR, Santos MCF (1993) Ionoregulatory and urinary responses to emersion in the mangrove crab Ucides cordatus and the intertidal crab Carcinus maenas. J Comp Physiol B 163:18–27CrossRefGoogle Scholar
  22. Hayd L, Anger K (2013) Reproductive and morphometric traits of Macrobrachium amazonicum (Decapoda: Palaemonidae) from the Pantanal, Brazil, suggests initial speciation. Revista Biol Trop (Int J Trop Biol) 61:39-57Google Scholar
  23. 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 319:153–165PubMedCrossRefGoogle Scholar
  24. Khodabandeh S, Kutnik M, Aujoulat F, Charmantier G, Charmantier-Daures M (2005b) Ontogeny of the antennal glands in the crayfish Astacus leptodactylus (Crustacea, Decapoda): immunolocalization of Na+/K+-ATPase. Cell Tissue Res 319:167–174PubMedCrossRefGoogle Scholar
  25. Lee CE, Bell MA (1999) Invasion of fresh waters by saltwater animals. Trends Ecol Evol 14:449PubMedCrossRefGoogle Scholar
  26. Lignot J-H, Charmantier G (2001) Immunolocalization of Na+/K+-ATPase in the branchial cavity during the early developement of the European lobster Homarus gammarus (Crustacea, Decapoda). J Histochem Cytochem 49:1013–1023PubMedCrossRefGoogle Scholar
  27. Lignot J-H, Charmantier-Daures M, Charmantier G (1999) Immunolocalization of Na+/K+-ATPase in the organs of the branchial cavity of the European lobster Homarus gammarus (Crustacea, Decapoda). Cell Tissue Res 296:417–426PubMedCrossRefGoogle Scholar
  28. Lignot J-H, Susanto GN, Charmantier-Daures M, Charmantier G (2005) Immunolocalization of Na+/K+-ATPase in the branchial cavity during the early development of the crayfish Astacus leptodactylus (Crustacea, Decapoda). Cell Tissue Res 319:331–339PubMedCrossRefGoogle Scholar
  29. Lucu C (1990) Ionic regulatory mechanisms in crustacean gill epithelia. Comp Biochem Physiol 97:297–306CrossRefGoogle Scholar
  30. Lucu C, Towle DW (2003) Na+/K+-ATPase in gills of aquatic crustacean. Comp Biochem Physiol A 135:195–214CrossRefGoogle Scholar
  31. Maciel CR, Valenti WC (2009) Biology, fisheries, and aquaculture of the Amazon River prawn Macrobrachium amazonicum: a review. Nauplius 17:61–79Google Scholar
  32. Magalhães C (1985) The larval development of palaemonids from Amazon region reared in the laboratory. I. Macrobrachium amazonicum (Heller, 1862) (Crustacea, Decapoda). Amazoniana 9:247–274Google Scholar
  33. Magalhães C, Walker I (1988) Larval development and ecological distribution of central Amazonian palaemonid shrimps (Decapoda, Caridea). Crustaceana 55:279–292CrossRefGoogle Scholar
  34. Mantel LH, Farmer LL (1983) Osmotic and ionic regulation. In: Mantel LH (ed) The biology of Crustacea. Academic Press, New York, pp 53–161Google Scholar
  35. Martinez AS, Charmantier G, Compère P, Charmantier-Daures M (2005) Branchial chamber tissues in two caridean shrimps: the epibenthic Palaemon adspersus and the deep-sea hydrothermal Rimicaris exoculata. Tissue Cell 37:153–165PubMedCrossRefGoogle Scholar
  36. McNmara JC, Lima AG (1997) The route of ion and water movements across the gill epithelium of the freshwater shrimp Macrobrachium olfersii (Decapoda, Palaemonidae): evidence from ultrastructural changes induced by acclimation to saline media. Biol Bull 192:321–331CrossRefGoogle Scholar
  37. Odinetz Collart O (1991) Stratégie de reproduction de Macrobrachium amazonicum en Amazonie Centrale (Decapoda, Caridea, Palaemonidae). Crustaceana 61:253–270CrossRefGoogle Scholar
  38. Péqueux A (1995) Osmotic regulation in crustaceans. J Crust Biol 15:536–536CrossRefGoogle Scholar
  39. Peterson DR, Loizzi RF (1974) Ultrastructure of the crayfish kidney, coelomosac, labyrinth, and nephridial canal. J Morphol 142:241–264PubMedCrossRefGoogle Scholar
  40. Talbot P, Clark WH, Lawrence AL (1972) Ultrastructural observations of muscle insertion and modified branchiostegite epidermis in larval brown shrimp, Penaeus aztecus. Tissue Cell 4:613–628PubMedCrossRefGoogle Scholar
  41. Towle DW, Kays WT (1986) Basolateral localization of Na+/K+-ATPase in gill epithelium of two osmoregulating crabs, Callinectes sapidus and Carcinus maenas. J Exp Zool 239:311–318CrossRefGoogle Scholar
  42. Vergamini FG, Pileggi LG, Mantelatto FL (2011) Genetic variability of the Amazon River prawn Macrobrachium amazonicum (Decapoda, Caridea, Palaemonidae). Contrib Zool 80:67–83Google Scholar
  43. Vogt G (2002) Functional anatomy. In: Holdich DM (ed) Biology of freshwater crayfish. Blackwell Science, Oxford, pp 53–151Google Scholar
  44. Ziegler A (1997) Immunocytochemical localization of Na+/K+-ATPase in the calcium-transporting sternal epithelium of the terrestrial isopod Porcellio scaber L (Crustacea). J Histochem Cytochem 45:437–446PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Nesrine Boudour-Boucheker
    • 1
    Email author
  • Viviane Boulo
    • 1
  • Catherine Lorin-Nebel
    • 1
  • Camille Elguero
    • 1
  • Evelyse Grousset
    • 1
  • Klaus Anger
    • 2
  • Mireille Charmantier-Daures
    • 1
  • Guy Charmantier
    • 1
  1. 1.Université Montpellier 2, Equipe Adaptation Ecophysiologique et OntogénèseUMR5119 EcoSyM, UM1-2-CNRS-IRD-IfremerMontpellier cedex 05France
  2. 2.Alfred-Wegener-Institut, Biologische Anstalt HelgolandHelgolandGermany

Personalised recommendations