Marine Biology

, Volume 153, Issue 4, pp 661–671 | Cite as

Interaction of short-term testosterone treatment with osmotic acclimation in the gilthead sea bream Sparus auratus

  • Francisco J. Arjona
  • Susana Sangiao-Alvarellos
  • Sergio Polakof
  • Angel García-López
  • María P. Martín del Río
  • Gonzalo Martínez-Rodríguez
  • José L. Soengas
  • Juan M. Mancera
Research Article

Abstract

To assess the interaction between testosterone (T) treatment and acclimation to different salinities, seawater-acclimated gilthead sea bream (Sparus auratus) were implanted with slow-release coconut oil implants alone (control) or containing T (5 μg/g body mass). After 5 days, eight fish of control and T-treated groups were sampled. The same day, eight fish of each group were transferred to low salinity water (LSW, 6 ppt, hypoosmotic test), seawater (SW, 38 ppt, control test) and high salinity water (HSW, 55 ppt, hyperosmotic test) and sampled 9 days later. Gill Na+, K+-ATPase activity increased in HSW-acclimated fish with respect to SW- and LSW-acclimated fish in both control and T-treated groups. Kidney Na+, K+-ATPase activity was also enhanced in HSW-acclimated fish, but only in T-treated group. From a metabolic point of view, most of the changes observed can be attributed to the action of salinity and T treatment alone, since few interactions between T treatment and osmotic acclimation to different salinities were observed. Those interactions included in treated fish: in the liver, decreased capacity in using glucose in fish acclimated to extreme salinities; in the gills, decreased capacity in using amino acids in HSW; in the kidneys increased capacity in using amino acids in extreme salinities; and in the brain, decreased glycogen and acetoacetate levels of fish in LSW.

Abbreviations

Ala-AT

Alanine aminotransferase (EC. 2.6.1.2.)

Asp-AT

Aspartate aminotransferase (EC. 2.6.1.1.)

HK

Low Km hexokinase (EC. 2.7.1.11.)

G6Pase

Glucose 6-phosphatase (EC. 3.1.3.9.)

G3PDH

α-Glycerophosphate dehydrogenase (EC. 1.1.1.8.)

G6PDH

Glucose 6-phosphate dehydrogenase (EC. 1.1.1.49)

GDH

Glutamate dehydrogenase (EC. 1.4.1.2.)

GK

Glucokinase (EC. 2.7.1.2.)

HOAD

3-Hydroxiacil-CoA-dehydrogenase (EC. 1.1.1.35.)

LDH-O

Lactate dehydrogenase-oxidase (EC. 1.1.1.27.)

PFK

6-Phosphofructo 1-kinase (EC. 2.7.1.11.)

PK

Pyruvate kinase (EC. 2.7.1.40.)

Notes

Acknowledgments

This study was partly supported by grants VEM2003-20062 (Ministerio de Ciencia y Tecnología and FEDER, Spain) and PGIDT04PXIC31208PN (Xunta de Galicia, Spain) to J.L.S., and grant BOS2004-04439-C02-01B (Ministerio de Educación y Ciencia and FEDER, Spain) to J.M.M. The authors wish to thank Planta de Cultivos Marinos (CASEM, Universidad de Cádiz, Puerto Real, Cádiz, Spain) for providing the experimental fish. The experiments described comply with the European Union Council (86/609/EU) and the Spanish Government (RD 1201/2005) guidelines for the use of animals in research (Consejería de Agricultura y Pesca de la Junta de Andalucía animal facilities refs. CA/3/U and CA/4/CS).

References

  1. Arias A (1976) Sobre la biología de la dorada, Sparus aurata L., de los esteros de la provincia de Cádiz. Inv Pesq 40:201–222Google Scholar
  2. Chaves-Pozo E, Liarte S, Vargas-Chacoff L, Garcia-Lopez A, Mulero V, Meseguer J, Mancera JM, Garcia-Ayala A (2007) 17β-Estradiol ttriggers postspawning in spermatogenically active gilthead seabream (Sparus aurata L.) males. Biol Reprod 6:142–148CrossRefGoogle Scholar
  3. Gothilf Y, Meiri I, Elizur A, Zohar Y (1997) Preovulatory changes in the levels of three gonadotropin-releasing hormone-encoding messenger ribonucleic acids (mRNAs), gonadotropin beta-subunit mRNAs, plasma gonadotropin, and steroids in the female gilthead seabream, Sparus aurata. Biol Reprod 57:1145–1154PubMedCrossRefGoogle Scholar
  4. Guzmán JM, Sangiao-Alvarellos S, Laiz-Carrión R, Míguez JM, Martín del Río MP, Soengas JL, Mancera JM (2004) Osmoregulatory action of 17β-estradiol in the gilthead sea bream Sparus auratus. J Exp Zool 301A:828–836CrossRefGoogle Scholar
  5. Haddy JA, Pankhurst NW (2000) The effects of salinity on reproductive development, plasma steroid levels, fertilisation and egg survival in black bream Acanthopagrus butcheri. Aquaculture 188:115–131CrossRefGoogle Scholar
  6. Haux C, Norberg B (1985) The influence of estradiol-17β on the liver content of protein, lipids, glycogen, and nucleic acids in juvenile rainbow trout, Salmo gairdneri. Comp Biochem Physiol 81B:275–279Google Scholar
  7. Ince BW, Lone KP, Matty AJ (1982) Effect of dietary protein level, and an anabolic steroid, ethylestrenol on the growth, food conversion efficiency and protein efficiency ratio of rainbow trou (Salmo gairdneri). Br J Nutr 47:615–624PubMedCrossRefGoogle Scholar
  8. Jakobsson S, Mayer I, Borg B (1997) Androgen binding in the gills of atlantic salmon, Salmo salar, mature male parr, and immature male smolts. J Exp Zool 278:391–394CrossRefGoogle Scholar
  9. Jensen MK, Madsen SS, Kristiansen K (1998) Osmoregulation and salinity effects on the expression and activity of Na+, K+-ATPase in gills of European sea bass, Dicentrarchus labrax (L.). J Exp Zool 282:290–300PubMedCrossRefGoogle Scholar
  10. Kelly SP, Woo NYS (1999) Cellular and biochemical characterization of hypoosmotic adaptation in a marine teleost, Sparus sarba. Zool Sci 16:505–514CrossRefGoogle Scholar
  11. Kelly SP, Chow INK, Woo NYS (1999) Haloplasticity of black seabream (Mylio macrocephalus): hypersaline to freshwater acclimation. J Exp Zool 283:226–241CrossRefGoogle Scholar
  12. Keppler D, Decker K (1974) Glycogen. determination with amyloglucosidase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Academic, New York, pp 1127–1131Google Scholar
  13. Laiz-Carrión R, Guerreiro PM, Fuentes J, Martín del Río MP, Canario AVM, Mancera JM (2005) Branchial osmoregulatory response to environmental salinities in the gilthead sea bream, Sparus auratus. J Exp Zool 303A:563–576CrossRefGoogle Scholar
  14. Laiz-Carrión R, Martín del Río MP, Míguez JM, Mancera JM, Soengas JL (2003) Influence of cortisol on osmoregulation and energy metabolism in gilthead sea bream Sparus aurata. J Exp Zool 298A:105–118CrossRefGoogle Scholar
  15. Le François N, Blier P (2000) Branchial Na+, K+-ATPase activity in brook charr (Salvelinus fontinalis): effect of gonadal development in hypo- and hyperosmotic environmentes. J Exp Zool 286:647–655PubMedCrossRefGoogle Scholar
  16. Le François NR, Lamarre SG, Blier PU (2004) Tolerance, growth and haloplasticity of the Atlantic wolfish (Anarhichas lupus) exposed to various salinities. Aquaculture 236:659–675CrossRefGoogle Scholar
  17. Mancera JM, Laiz-Carrión R, Martín del Río MP (2002) Osmoregulatory action of PRL, GH and cortisol in the gilthead seabream (Sparus auratus L.). Gen Comp Endocrinol 129:95–103CrossRefGoogle Scholar
  18. Mancera JM, Smolenaars M, Laiz-Carrión R, Martin del Rio MP, Wendelaar Bonga SE, Flik G (2004) 17β-estradiol affects osmoregulation in Fundulus heteroclitus. Comp Biochem Physiol 139B:183–191Google Scholar
  19. McCormick SD (1993) Methods for nonlethal gill biopsy and measurement of Na+, K+-ATPase activity. Can J Fish Aquat Sci 50:656–658CrossRefGoogle Scholar
  20. McCormick SD (1995) Hormonal control of gill Na+, K+-ATPase and chloride cell function. In: Wood CM, Shuttleworth TJ (eds) Hormonal control of gill Na+, K+ATPase and chloride cell function. Academic, San Diego, pp 285–315Google Scholar
  21. McCormick SD (1996) Effect of growth hormone and insulin-like factor I on salinity tolerance and gill Na+, K+-ATPase in atlantic salmon (Salmo salar): interaction with cortisol. Gen Comp Endocrinol 101:3–11PubMedCrossRefGoogle Scholar
  22. McCormick SD, Naiman RJ (1985) Hypoosmoregulation in an anadromous teleost: influence of sex and maduration. J Exp Zool 234:193–198PubMedCrossRefGoogle Scholar
  23. Moore S (1968) Amino acid analysis: aqueous dimethyl sulfoxide as solvent for the nynhidrin reaction. J Biol Chem 1242:6281–6283Google Scholar
  24. Nakano K, Tagawa M, Takemura A, Hirano T (1998) Temporal changes in liver carbohydrate metabolism associated with seawater transfer in Oreochromis mossambicus. Comp Biochem Physiol 119B:721–728Google Scholar
  25. Peter MCS, Oommen OV (1989) Oxidative metabolism in a teleost, Anabas testudineus Bloch: effect of testosterone and estradiol-17β on hepatic enzyme activities. Fish Physiol Biochem 6:377–385CrossRefGoogle Scholar
  26. Reshkin SJ, Grover ML, Howerton RD, Grau EG, Ahearn GA (1989) Dietary hormonal modification of growth, intestinal ATPase, and glucose transport in tilapia. Am J Physiol 256:E610–E618PubMedGoogle Scholar
  27. Rodríguez L, Begtashi I, Zanuy S, Carrillo M (2000) Development and validation of an enzyme inmunoassay for testosterone: effects of photoperiod on plasma testosterone levels and gonadal development in male sea bass (Dicentrarchus labrax, L.) at puberty. Fish Physiol Biochem 23:141–150CrossRefGoogle Scholar
  28. Ros AFH, Becker K, Canario AVM, Oliveira RF (2004) Androgen levels and energy metabolism in Oreochromis mossambicus. J Fish Biol 65:895–905CrossRefGoogle Scholar
  29. Sangiao-Alvarellos S, Laiz-Carrión R, Guzmán JM, Martín del Río MP, Míguez JM, Mancera JM, Soengas JL (2003) Acclimation of S. aurata to various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs. Am J Physiol 285:R897–R907Google Scholar
  30. Sangiao-Alvarellos S, Arjona FJ, Martín del Río MP, Míguez JM, Mancera JM, Soengas JL (2005a) Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus. J Exp Biol 208:4291–4304PubMedCrossRefGoogle Scholar
  31. Sangiao-Alvarellos S, Guzmán JM, Laiz-Carrión R, Míguez JM, Martín del Río MP, Mancera JM, Soengas JL (2005b) Actions of 17β-estradiol on carbohydrate metabolism in liver, gills, and brain of gilthead sea bream Sparus auratus during acclimation to different salinities. Mar Biol 146:607–617CrossRefGoogle Scholar
  32. Sangiao-Alvarellos S, Polakof S, Arjona FJ, García-López A., Martín del Río MP, Martínez-Rodríguez G, Míguez JM, Mancera JM, Soengas JL (2006) Influence of testosterone administration on osmoregulation and energy metabolism of gilthead seabream Sparus auratus. Gen Comp Endocrinol 149:30–41PubMedCrossRefGoogle Scholar
  33. Singh C, Gupta RC (2002) Influence of testosterone propionate and methyl testosterone on RNA, DNA, glycogen and protein contents in liver and ovary of fresh water catfish, Clarias batrachus (Bloch). J Exp Zool India 5:41–44Google Scholar
  34. Sparks R, Shepherd BS, Ron B, Richman III NH, Riley LG, Iwama GK, Hirano T, Grau EG (2003) Effects of environmental salinity and 17α-methyltestosterone on growth and oxygen consumption in the tilapia, Oreochromis mossambicus. Comp Biochem Physiol 136B:657–665Google Scholar
  35. Sunny F, Oommen OV (2000) Steroid hormones regulate enzymes of osmoregulation in a freshwater fish Oreochromis (tilapia) mossambicus. J Endocrinol Reprod 4:63–73Google Scholar
  36. Sunny F, Oommen OV (2002) Rapid action of testosterone and diethylstilbestrol on enzymes of osmoregulation in a freshwater fish Oreochromis mossambicus. Endocrine Res 28:69–81CrossRefGoogle Scholar
  37. Sunny F, Jacob A, Oommen OV (2002) Sex steroids regulate intermediary metabolism in Oreochromis mossambicus. Endocrine Res 28:175–188CrossRefGoogle Scholar
  38. Vijayan MM, Takemura A, Mommsen TP (2001) Estradiol impairs hypoosmoregulatory capacity in the euryhaline tilapia, Oreochromis mossambicus. Am J Physiol 281:R1161–R1168Google Scholar
  39. Woo NYS, Chung ASB, Ng TB (1993) Influence of oral administration of estradiol-17β and testosterone on growth, digestion, food conversion and metabolism in the underyearling red sea bream, Chrysophrys major. Fish Physiol Biochem 10:377–387CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Francisco J. Arjona
    • 1
  • Susana Sangiao-Alvarellos
    • 2
  • Sergio Polakof
    • 2
  • Angel García-López
    • 3
  • María P. Martín del Río
    • 1
  • Gonzalo Martínez-Rodríguez
    • 3
  • José L. Soengas
    • 2
  • Juan M. Mancera
    • 1
  1. 1.Departamento de BiologíaFacultad de Ciencias del Mar y Ambientales, Universidad de CádizCádizSpain
  2. 2.Laboratorio de Fisioloxía Animal, Departamento de Bioloxía Funcional e Ciencias da Saúde, Facultade de BioloxíaUniversidade de VigoVigoSpain
  3. 3.Instituto Ciencias Marinas de AndalucíaCSICCádizSpain

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