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Hyposmoregulatory ability and ion- and water-regulatory mechanisms during the leptocephalus stages of Japanese eel Anguilla japonica

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Abstract

We explored osmoregulatory ability and mechanisms of ion and water regulation in Japanese eel leptocephali. Tissue osmolality of leptocephali ranged from 360 to 540 mOsm/kg·H2O. Immunocytochemical observations revealed that Na+/K+-ATPase-immunoreactive mitochondrion-rich (MR) cells were distributed over the entire body surface of leptocephali. Using a fluorescent sodium indicator and the chloride test, we localized Na+ and Cl− secreting sites at the apical region of cutaneous MR cells. To further examine drinking behavior and water absorption in the intestine, leptocephali were exposed to seawater containing dextran labeled with Alexa Fluor. To calculate relative water absorption, fluorescent intensity was measured along the digestive tract. Whereas water was hardly absorbed in the stomach and intestine, water absorption predominantly took place in the rectum. Our findings indicate that Japanese eel exert hyposmoregulatory ability as early as during leptocephalus stages, secreting Na+ and Cl− through cutaneous MR cells and primarily absorbing water from ingested seawater in the rectum.

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References

  1. Tsukamto K (1992) Discovery of the spawning area for Japanese eel. Nature 356:789–791

    Article  Google Scholar 

  2. Tsukamto K (2006) Spawning of eels near a seamount. Nature 439:929

    Article  Google Scholar 

  3. Schmidt J (1922) The breeding places of the eel. Philos Trans R Soc Lond B 211:179–208

    Article  Google Scholar 

  4. Kimura S, Tsukamoto K, Sugimoto T (1994) A model for the larval migration of the Japanese eel: roles of the trade winds salinity front. Mar Biol 119:185–190

    Article  Google Scholar 

  5. Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177

    Article  PubMed  CAS  Google Scholar 

  6. Marshall WS, Grosell M (2006) Ion transport, osmoregulation and acid-base balance. In: Evans DH, Claiborne JB (eds) The physiology of fishes. CRC Press, Boca Raton, pp 177–230

    Google Scholar 

  7. Evans DH, Claiborne JB (2009) Osmotic and ionic regulation in fishes. In: Evans DH (ed) Osmotic and ionic regulation: cells and animals. CRC Press, Boca Raton, pp 295–366

    Google Scholar 

  8. Hirose S, Kaneko T, Naito N, Takei Y (2003) Molecular biology of major components of chloride cells. Comp Biochem Physiol B 136:593–620

    Article  PubMed  Google Scholar 

  9. Kaneko T, Watanabe S, Lee KM (2008) Functional morphology of mitochondrion-rich cells in euryhaline and stenohaline teleosts. Aqua-Biosci Monogr 1:1–62

    Google Scholar 

  10. Karnaky KJ Jr, Kinter LB, Kinter WB, Stirling CE (1976) Teleost chloride cell. II. Autoradiographic localization of gill Na, K-ATPase in killifish Fundulus heteroclitus adapted to low and high salinity environments. J Cell Biol 70:157–177

    Article  PubMed  CAS  Google Scholar 

  11. Philpott CW (1980) Tubular system membranes of teleost chloride cells: osmotic response and transport sites. Am J Physiol 238:R171–R184

    PubMed  CAS  Google Scholar 

  12. McCormick SD (1995) Hormonal control of gill Na+, K+-ATPase and chloride cell function. In: Wood CM, Shuttleworth TJ (eds) Cellular and molecular approaches to fish ionic regulation. Academic Press, New York, pp 285–315

    Google Scholar 

  13. Evans DH (1993) Osmotic and ionic regulation. In: Evans DH (ed) The physiology of fishes. CRC Press, Boca Raton, pp 315–341

    Google Scholar 

  14. Maetz J, Skadhauge E (1968) Drinking rate and gill ionic turnover in relation to external salinities in the eel. Nature 217:371–373

    Article  PubMed  CAS  Google Scholar 

  15. Hirano T (1974) Some factors regulating water intake by the eel, Anguilla japonica. J Exp Biol 61:737–747

    PubMed  CAS  Google Scholar 

  16. Hirano T, Mayer-Gostan N (1976) Eel esophagus as an osmoregulatory organ. Proc Natl Acad Sci USA 73:1348–1350

    Article  PubMed  CAS  Google Scholar 

  17. Alderdice DF (1988) Osmotic and ionic regulation in teleost eggs and larvae. In: Hoar WS, Randall DJ (eds) Fish physiology, vol. 11a. Academic Press, New York, pp 163–251

  18. Kaneko T, Hiroi J (2008) Osmo- and ionoregulation. In: Finn RN, Kapoor BG (eds) Fish larval physiology. Science Publisher, Enfield, pp 163–183

  19. Kaneko T, Hasegawa S, Takagi Y, Tagawa M, Hirano T (1995) Hypoosmoregulatory ability of eyed-stage embryos of chum salmon. Mar Biol 122:165–170

    Article  Google Scholar 

  20. Kaneko T, Shiraishi K, Katoh F, Hasegawa S, Hiroi J (2002) Chloride cells during early life stages of fish and their functional differentiation. Fish Sci 68:1–9

    Article  CAS  Google Scholar 

  21. Hiroi J, Kaneko T, Seikai T, Tanaka M (1998) Developmental sequence of chloride cells in the body skin and gills of Japanese flounder (Paralichthys olivaceus) larvae. Zool Sci 15:455–460

    PubMed  CAS  Google Scholar 

  22. Hiroi J, Kaneko T, Uchida K, Hasegawa S, Tanaka M (1998) Immunolocalization of vacuolar-type H+-ATPase in the yolk-sac membrane of tilapia (Oreochromis mossambicus) larvae. Zool Sci 15:447–453

    PubMed  CAS  Google Scholar 

  23. Sasai S, Kaneko T, Tsukamoto K (1998) Extrabranchial chloride cells in early life stages of the Japanese eel, Anguilla japonica. Ichthyol Res 45:95–98

    Article  Google Scholar 

  24. Katoh F, Shimizu A, Uchida K, Kaneko T (2000) Shift of chloride cell distribution during early life stages in seawater-adapted killifish, Fundulus heteroclitus. Zool Sci 17:11–18

    Article  PubMed  CAS  Google Scholar 

  25. Varsamos S, Diaz JP, Charmantier G, Blasco C, Connes R, Flik G (2002) Location and morphology of chloride cells during the post-embryonic development of European sea bass, Dicentrarchus labrax. Anat Embryol 205:203–213

    Article  PubMed  Google Scholar 

  26. Yanagie R, Lee KM, Watanabe S, Kaneko T (2009) Ontogenic change in tissue osmolality and developmental sequence of mitochondria-rich cells in Mozambique tilapia developing in freshwater. Comp Biochem Physiol A 154:263–269

    Article  Google Scholar 

  27. Hullet WH, Fischer J, Rietberg BJ (1972) Electrolyte composition of anguilliform leptocephali from the straits of Florida. Bull Mar Sci 22:432–448

    Google Scholar 

  28. Horie N, Utoh T, Mikawa N, Yamada Y, Okamura A, Tanaka S, Tsukamoto K (2008) Influence of artificial fertilization methods of the hormone-treated Japanese eel Anguilla japonica upon the quality of eggs and larvae: comparison between stripping-insemination and spontaneous spawning methods (in Japanese). Nippon Suisan Gakkaishi 74:26–35

    Article  Google Scholar 

  29. Kagawa H, Tanaka H, Ohta H, Unuma K, Nomura N (2005) The first success of glass eel production in the world: basic biology on fish reproduction advances new applied technology in aquaculture. Fish Physiol Biochem 31:193–199

    Article  PubMed  CAS  Google Scholar 

  30. Ohta H, Kagawa H, Tanaka H, Okuzawa K, Linuma N (1997) Artificial induction of maturation and fertilization in the Japanese eel, Anguilla japonica. Fish Physiol Biochem 17:163–169

    Article  CAS  Google Scholar 

  31. Dou SZ, Yamada Y, Okamura A, Tanaka S, Shinoda A, Tsukamoto K (2008) Temperature influence on the spawning performance of artificially-matured Japanese eel, Anguilla japonica, in captivity. Environ Biol Fish 82:151–164

    Article  Google Scholar 

  32. Okamura A, Yamada Y, Horie N, Utoh T, Mikawa N, Tanaka S, Tsukamto K (2007) Effects of water temperature on early development of Japanese eel Anguilla japonica. Fish Sci 73:1241–1248

    CAS  Google Scholar 

  33. Uchida K, Kaneko T, Miyazaki H, Hasegawa S, Hirano T (2000) Excellent salinity tolerance of Mozambique tilapia (Oreochromis mossambicus): elevated chloride cell activity in the branchial and opercular epithelia of the fish adapted to concentrated seawater. Zool Sci 17:149–160

    Article  Google Scholar 

  34. Sasai S, Katoh F, Kaneko T, Tsukamoto K (2007) Ontogenic change of gill chloride cells in leptocephalus and glass eel stages of the Japanese eel Anguilla japonica. Mar Biol 150:487–496

    Article  Google Scholar 

  35. Kaneko T, Shiraishi K (2001) Evidence for chloride secretion from chloride cells in the yolk-sac membrane of Mosambique tilapia larvae adapted to seawater. Fish Sci 67:541–543

    Article  CAS  Google Scholar 

  36. Hullet WH, Robins CR (1989) The evolutionary significance of the leptocephalus larva. In: Bohike EB (ed) Fishes of the western North Atlantic, part 9, vol. 2. Sears Foundation for Marine Research, New Haven, pp 669–677

  37. Ura K, Soyano K, Omoto N, Adachi S, Yamauchi K (1996) Localization of Na+, K+-ATPase in tissues of rabbit and teleosts using an antiserum directed against a partial sequence of the α-subunit. Zool Sci 13:219–227

    Article  PubMed  CAS  Google Scholar 

  38. Hootman SR, Philpott DW (1979) Ultracytochemical localization of Na+, K+-activated ATPase in chloride cells from the gills of a euryhaline teleost. Anat Rec 193:99–130

    Article  PubMed  CAS  Google Scholar 

  39. Kaneko T, Hasegawa S, Sasai S (2003) Chloride cells in Japanese eel (Anguilla japonica) during their early life stages and downstream migration. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel biology. Springer, Tokyo, pp 457–468

    Chapter  Google Scholar 

  40. Varsamos S, Nebel C, Charmantier G (2005) Ontogeny of osmoregulation in postembryonic fish: review. Comp Biochem Physiol A 141:401–429

    Article  Google Scholar 

  41. Guggino WB (1980) Water balance in embryos of Fundulus heteroclitus and F. bermudae in seawater. Am J Physiol 238:R36–R41

    PubMed  CAS  Google Scholar 

  42. Pisam M, Massa F, Jammet C, Prunet P (2000) Chronology of the appearance of β, A, and α mitochondria-rich cells in the gill epithelium during ontogenesis of the brown trout (Salmo trutta). Anat Rec 259:301–311

    Article  PubMed  CAS  Google Scholar 

  43. Li J, Eygensteyn J, Lock RAC, Verbost PM, van der Heijden AJH, Wendelaar Bonga SE, Flik G (1995) Branchial chloride cells in larvae and juveniles of freshwater tilapia Oreochromis mossambicus. J Exp Biol 198:2177–2184

    PubMed  Google Scholar 

  44. Shen WP, Horng JL, Lin LY (2011) Functional plasticity of mitochondrion-rich cells in the skin of euryhaline medaka larvae (Oryzias latipes) subjected to salinity changes. Am J Physiol Regul Integr Comp Physiol 300:R858–R868

    Article  PubMed  CAS  Google Scholar 

  45. Sasai S, Kaneko T, Hasegawa S, Tsukamoto K (1998) Morphological alteration in two types of gill chloride cells in Japanese eel (Anguilla japonica) during catadromous migration. Can J Zool 76:1480–1487

    Google Scholar 

  46. Okamura A, Yamada Y, Mikawa N, Horie N, Utoh T, Kaneko T, Tanaka S, Tsukamto K (2009) Growth and survival of eel leptocephali (Anguilla japonica) in low-salinity water. Aquaculture 296:367–372

    Article  CAS  Google Scholar 

  47. Mangor-Jensen A, Adoff GR (1987) Drinking activity of the newly hatched larvae of cod Gadus morhua L. Fish Physiol Biochem 3:99–103

    Article  Google Scholar 

  48. Tytler P, Blaxter JHS (1988) The effects of external salinity on the drinking rates of the larvae of herring, plaice and cod. J Exp Biol 138:1–15

    Google Scholar 

  49. Brown JA, Tytler P (1993) Hypoosmoregulation of larvae of the turbot, Scophthalamus maximus: drinking and gut function in relation to environmental salinity. Fish Physiol Biochem 10:475–483

    Article  Google Scholar 

  50. Tytler P, Ireland J (1994) Drinking and water absorption by the larvae of herring (Clupea harengus) and turbot (Scophthalmus maximus). J Fish Biol 44:103–116

    Article  Google Scholar 

  51. Miyazaki H, Kaneko T, Hasegawa S, Hirono T (1998) Developmental changes in drinking rate and ion water permeability during early life stages of euryhaline tilapia, Oreochromis mossambicus, reared in fresh water and seawater. Fish Physiol Biochem 18:277–284

    Article  CAS  Google Scholar 

  52. Tytler P, Blaxter JHS (1988) Drinking in yolk-sac stage larvae of the halibut, Hippoglossus hippoglossus (L.). J Fish Biol 32:493–494

    Article  Google Scholar 

  53. Kaneko T, Hasegawa S (1999) Application of laser scanning microscopy to morphological observations on drinking in freshwater medaka larvae and those exposed to 80 % seawater. Fish Sci 65:492–493

    CAS  Google Scholar 

  54. Kim YK, Ideuchi H, Watanabe S, Park SI, Huh MD, Kaneko T (2008) Rectal water absorption in seawater-adapted Japanese eel Anguilla japonica. Comp Biochem Physiol A 151:533–541

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo, 113-8657, Japan

    Kyung Mi Lee & Toyoji Kaneko

  2. IRAGO Institute, Tahara, Aichi, 441-3605, Japan

    Yoshiaki Yamada, Akihiro Okamura & Katsumi Tsukamoto

  3. Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba, 277-8564, Japan

    Katsumi Tsukamoto

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  1. Kyung Mi Lee
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  2. Yoshiaki Yamada
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  4. Katsumi Tsukamoto
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  5. Toyoji Kaneko
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Correspondence to Toyoji Kaneko.

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Lee, K.M., Yamada, Y., Okamura, A. et al. Hyposmoregulatory ability and ion- and water-regulatory mechanisms during the leptocephalus stages of Japanese eel Anguilla japonica . Fish Sci 79, 77–86 (2013). https://doi.org/10.1007/s12562-012-0576-3

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  • DOI: https://doi.org/10.1007/s12562-012-0576-3

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