Advertisement

Fish Physiology and Biochemistry

, Volume 38, Issue 6, pp 1741–1751 | Cite as

Physiological short-term response to sudden salinity change in the Senegalese sole (Solea senegalensis)

  • Marcelino Herrera
  • Cláudia Aragão
  • Ismael Hachero
  • Ignacio Ruiz-Jarabo
  • Luis Vargas-Chacoff
  • Juan Miguel Mancera
  • Luis E. C. Conceição
Article

Abstract

The physiological responses of Senegalese sole to a sudden salinity change were investigated. The fish were first acclimated to an initial salinity of 37.5 ppt for 4 h. Then, one group was subjected to increased salinity (55 ppt) while another group was subjected to decreased salinity (5 ppt). The third group (control group) remained at 37.5 ppt. We measured the oxygen consumption rate, osmoregulatory (plasma osmolality, gill and kidney Na+,K+-ATPase activities) and stress (plasma cortisol and metabolites) parameters 0.5 and 3 h after transfer. Oxygen consumption at both salinities was higher than for the control at both sampling times. Gill Na+,K+-ATPase activity was significantly higher for the 55 ppt salinity at 0.5 h. Plasma osmolality decreased in the fish exposed to 5 ppt at the two sampling times but no changes were detected for high salinities. Plasma cortisol levels significantly increased at both salinities, although these values declined in the low-salinity group 3 h after transfer. Plasma glucose at 5 ppt salinity did not vary significantly at 0.5 h but decreased at 3 h, while lactate increased for both treatments at the first sampling time and returned to the control levels at 3 h. Overall, the physiological response of S. senegalensis was immediate and involved a rise in oxygen consumption and plasma cortisol values as well as greater metabolite mobilization at both salinities.

Keywords

Senegalese sole Osmoregulation Stress Oxygen consumption Physiology 

Notes

Acknowledgments

This work has been funded by the project INTERREG 0251_ECOAQUA_5_E and Proyecto de Excelencia PO7-RNM-02843 (Junta de Andalucía) to J.M. Mancera. Cláudia Aragão acknowledges financial support by Fundação para a Ciência e Tecnologia, Portugal, through grant SFRH/BPD/37197/2007. The experiments described complied with the Guidelines of European Union Council (86/609/EU) for the use of animals in research.

References

  1. Arias AM, Drake P (1999) Fauna acuática de las salinas del Parque Natural Bahía de Cádiz. Empresa de Gestión Medioambiental S.A. (EGMASA), SevillaGoogle Scholar
  2. Arjona FJ, Vargas-Chacoff L, Ruiz-Jarabo I, Martín del Río MP, Mancera JM (2007) Osmoregulatory response of Senegalese sole (Solea senegalensis) to changes in environmental salinity. Comp Biochem Phys 148A:413–421CrossRefGoogle Scholar
  3. Arjona FJ, Vargas-Chacoff L, Ruiz-Jarabo I, Gonçalves O, Páscoa I, Martín del Río MP, Mancera JM (2009) Tertiary stress responses in Senegalese sole (Solea senegalensis Kaup, 1858) to osmotic challenge: implications for osmoregulation, energy metabolism and growth. Aquaculture 287:419–426CrossRefGoogle Scholar
  4. Barton BA, Schreck CB, Barton LD (1987) Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow trout. Dis Aquat Organ 2:173–185CrossRefGoogle Scholar
  5. Bayarri MJ, Muñoz-Cueto JA, López-Olmeda JF, Vera LM, Rol de Lama MA, Madrid JA, Sánchez-Vázques FJ (2004) Daily locomotor activity and melatonin rhythms in Senegalese sole (Solea senegalensis). Physiol Behav 51:553–573Google Scholar
  6. Beyenbach KW (1995) Secretory electrolyte transport in renal proximal tubules of fish. In: Wood CM, Shuttleworth TJ (eds) Fish Physiology, vol 14. Academic Press, San Diego, CA, pp 85–106Google Scholar
  7. Burrows MT, Gibson RN, Maclean A (1994) Effects of endogenous rhythms and light conditions on foraging and predator-avoidance in juveniles plaice. J Fish Biol 45:171–180CrossRefGoogle Scholar
  8. Cabral H, Costa MJ (1999) Differential use of nursery areas within the Tagus Estuary by sympatric soles Solea solea and Solea senegalensis. Environ Biol Fish 56:389–397CrossRefGoogle Scholar
  9. Dantzler WH (2003) Regulation of renal proximal an distal tubule transport: sodium, chloride and organic anions. Comp Biochem Phys 136A:453–478CrossRefGoogle Scholar
  10. Dinis MT, Ribeiro L, Soares F, Sarasquete C (1999) A review on the cultivation potential of Solea senegalensis in Spain and in Portugal. Aquaculture 176:27–38CrossRefGoogle Scholar
  11. Establier R, Lubián LM, Blasco J, Gómez A (1984) Estudio de las variaciones fisicoquímicas de salinas de Cádiz dedicadas al cultivo extensivo de peces. Inf Téc Inv Pesq 112Google Scholar
  12. Evans DH (2010) Co-ordination of osmotic stress responses through osmosensing and signal transduction events in fishes. J Fish Biol 76:1903–1925CrossRefGoogle Scholar
  13. 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 85:97–177CrossRefGoogle Scholar
  14. Ewart HS, Klip A (1995) Hormonal regulation of the Na + -K + , ATPase: mechanisms underlying rapid and sustained changes in pump activity. Am J Physiol 269:C295–C311CrossRefGoogle Scholar
  15. Fabbri E, Capuzzo A, Moon TW (1998) The role of circulating catecholamines in the regulation of fish metabolism: an overview. Comp Biochem Phys 120C:177–192Google Scholar
  16. Herrera M, Hachero I, Prado MA, Márquez JM, Navas JI (2005) Resultados preliminares sobre aclimatación y mantenimiento en cautividad de reproductores de lenguado (Solea senegalensis), parracho (Scophthalmus rhombus) y acedía (Dicologoglossa cuneata) en el CICEM Agua del Pino, Huelva. In: Actas del IX Congreso Nacional de Acuicultura. Cádiz, Mayo 2003. Consejería de Agricultura y Pesca. Junta de Andalucía, pp 291–295Google Scholar
  17. Herrera M, Vargas-Chacoff L, Hachero I, Ruiz-Jarabo I, Rodiles A, Navas JI, Mancera JM (2009) Osmoregulatory changes in wedge sole (Dicologoglossa cuneata Moreau, 1881) after acclimation to different environmental salinities. Aquac Res 40:762–771CrossRefGoogle Scholar
  18. Hiroi J, McCormick SD, Ohtani-Kaneko R, Kaneko T (2005) Functional classification of mitochondrion-rich cells in euryhaline Mozambique tilapia (Oreochromis mossambicus) embryos, by means of triple immunofluorescence staining for Na/K + -ATPase, Na +/K +/2Cl(-) cotransporter and CFTR anion channel. J Exp Biol 208:2023–2036CrossRefGoogle Scholar
  19. Hossler FE (1980) Gill arch of the mullet, Mugil cephalus, III: rate of response to salinity change. Am J Physiol 238:R160–R164CrossRefGoogle Scholar
  20. Hwang PP, Sun CM, Wu SM (1989) Changes of plasma osmolality, chloride concentration and gill Na-K-ATPases activity in tilapia Oreochromis mossambicus during seawater acclimation. Mar Biol 100:295–299CrossRefGoogle Scholar
  21. Imsland AK, Foss A, Conceicao LEC, Dinis MT, Delbare D, Schram E, Kamstra A, Rema P, White P (2003) A review of the culture of Solea solea and S. senegalensis. Rev Fish Biol Fisher 13:379–407CrossRefGoogle Scholar
  22. Kadri S, Metcalfe NB, Huntingford FA, Thorpe JE (1997a) Daily feeding rhythms in Atlantic salmon I: feeding and aggression in part under ambient environmental conditions. J Fish Biol 50:267–272CrossRefGoogle Scholar
  23. Kadri S, Metcalfe NB, Huntingford FA, Thorpe JE (1997b) Daily feeding rhythms in Atlantic salmon II: size-related variation in feeding patterns of post-smolts under constant environmental conditions. J Fish Biol 50:273–279CrossRefGoogle Scholar
  24. Kammerer BD, Sardella BA, Kültz D (2009) Salinity stress results in rapid cell cycle changes of tilapia (Oreochromis mossambicus) gill epithelial cells. J Exp Zool 311A:80–90CrossRefGoogle Scholar
  25. Kammerer BD, Cech JJ, Kültz D (2010) Rapid changes in plasma cortisol, osmolality, and respiration in response to salinity stress in tilapia (Oreochromis mossambicus). Comp Biochem Phys A 157:260–265CrossRefGoogle Scholar
  26. Kidder GW III, Petersen CW, Preston RL (2006) Energetics of Osmoregulation: I. Oxygen Consumption by Fundulus heteroclitus. J Exp Zool 305A:309–317CrossRefGoogle Scholar
  27. Laiz-Carrión R, Sangiao-Alvarellos S, Guzmán JM, Martín del Río MP, Mínguez J, Soengas JL, Mancera JM (2002) Energy metabolism in fish tissues related to osmoregulation and cortisol action. Fish Physiol Biochem 27:179–188CrossRefGoogle Scholar
  28. Madsen SS, Naamansen ET (1989) Plasma ionic regulation and gill Na +/K + -ATPase changes during rapid transfer to sea water of yearling rainbow trout, Salmo gairdneri: time course and seasonal variation. J Fish Biol 34:829–840CrossRefGoogle Scholar
  29. Mancera JM, McCormick SD (2000) Rapid activation of gill Na + , K + -ATPase in the euryhaline teleost Fundulus heteroclitus. J Exp Zool 287:263–274CrossRefGoogle Scholar
  30. Marshall WS (2002) Na+, Cl, Ca2+ and Zn2+ transport by fish gills: retrospective review and prospective synthesis. J Exp Zool 293:264–283CrossRefGoogle Scholar
  31. 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, FL, pp 177–231Google Scholar
  32. McCormick SD (1993) Methods for nonlethal gill biopsy and measurement of Na + , K + -ATPase activiy. Can J Fish Aquat Sci 50:656–658CrossRefGoogle Scholar
  33. McCormick SD (1995) Hormonal control of gill Na + , K + -ATPase and chloride cell function. In: Wood CM, Shuttlewoth TJ (eds) Fish Physiology, vol 14. Academic Press, New York, pp 285–315Google Scholar
  34. McCormick SD (2001) Endocrine Control of Osmoregulation in Teleost Fish. Am Zool 41:781–794Google Scholar
  35. Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fisher 9:211–268CrossRefGoogle Scholar
  36. Morgan JD, Iwama GK (1991) Effects of salinity on growth, metabolism, and ion regulation in juvenile rainbow and steelhead trout (Oncorhynchus mykiss) and fall Chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 48:2083–2094CrossRefGoogle Scholar
  37. Morgan JD, Iwama GK (1998) Salinity effects on oxygen consumption, gill Na + , K + -ATPase and ion regulation in juvenile coho salmon. J Fish Biol 53:1110–1119Google Scholar
  38. Rodríguez L, Begtashi I, Zanuy S, Carrillo M (2000) Development and validation of an enzyme immunoassay 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
  39. Sangiao-Alvarellos S, Laíz-Carrión R, Guzmán JM, Martín del Río MP, Migues JM, Mancera JM, Soengas JL (2003) Acclimation of S. auratus to various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs. Am J Phys 285:R897–R907Google Scholar
  40. Sangiao-Alvarellos S, Arjona FJ, Martín del Río MP, Migues JM, Mancera JM, Soengas JL (2005) Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus. J Exp Biol 208:4291–4304CrossRefGoogle Scholar
  41. Sardella BA, Matey V, Cooper JC, Gonzalez RJ, Brauner CJ (2004) Physiological, biochemical and morphological indicators of osmoregulatory stress in ‘California’ Mozambique tilapia (Oreochromis mossambicus × O. urolepis hornorum) exposed to hypersaline water. J Exp Biol 207:1399–1413CrossRefGoogle Scholar
  42. Soengas JL, Sangiao-Alvarellos S, Laiz-Carrión R, Mancera JM (2007) Energy metabolism and osmotic acclimation in teleost fish. In: Baldisserotto B, Mancera JM, Kapoor BG (eds) Fish Osmoregulation. Science Publishers Inc., Enfield, NH, pp 278–307Google Scholar
  43. Thetmeyer H (1997) Diel rhythms of swimming activity and oxygen consumption in Gobiusculus flavescens (Fabricius) and Pomatoschistus (Pallas) (Teleostei: Gobiidae). J Exp Mar Biol Ecol 218:187–198CrossRefGoogle Scholar
  44. Tipsmark CK, Madsen SS (2001) Rapid modulation of Na+/K+-ATPase activity in osmoregulatory tissues of a salmonid fish. J Exp Biol 204:701–709PubMedGoogle Scholar
  45. Vargas-Chacoff L, Arjona FJ, Polakof S, Martín del Río MP, Soengas JL, Mancera JM (2009) Interactive effects of environmental salinity and temperature on metabolic responses of gilthead sea bream Sparus aurata. Comp Biochem Phys 154(3):417–424CrossRefGoogle Scholar
  46. Via JD, Villani P, Gasteiger E, Niederstätter H (1998) Oxygen consumption in sea bass fingerlings Dicentrarchus labrax exposed to acute salinity and temperature changes: metabolic basis for maximum stocking density estimations. Aquaculture 169:303–313CrossRefGoogle Scholar
  47. Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 7:591–625CrossRefGoogle Scholar
  48. Wendelaar Bonga SE, van der Meij CJM (1989) Degeneration and death, by apoptosis and necrosis, of the pavement and chloride cells in the gills of the teleost Oreochromis mossambicus. Cell Tissue Res 255:235–243CrossRefGoogle Scholar
  49. Yoon SJ, Kim CK, Myoung JG, Kim WS (2003) Comparison of oxygen consumption patterns between wild and cultured black rockfish Sebastes schlegeli. Fish Sci 69:43–49CrossRefGoogle Scholar
  50. Zadunaisky JA, Cardona S, Au L, Roberts DM, Fisher E, Lowenstein B, Crague EJ, Spring KR (1995) Chloride transport activation by plasma osmolality during rapid adaptation to high salinity of Fundulus heteroclitus. J Membr Biol 143:207–217CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Marcelino Herrera
    • 1
  • Cláudia Aragão
    • 2
  • Ismael Hachero
    • 1
  • Ignacio Ruiz-Jarabo
    • 3
  • Luis Vargas-Chacoff
    • 3
    • 4
  • Juan Miguel Mancera
    • 3
  • Luis E. C. Conceição
    • 2
  1. 1.IFAPA Agua del PinoCtra. Cartaya-Punta UmbríaCartaya, HuelvaSpain
  2. 2.CCMARUniversidade do Algarve (Campus de Gambelas)FaroPortugal
  3. 3.Departamento de Biología, Facultad de Ciencias del Mar y AmbientalesUniversidad de CádizPuerto RealSpain
  4. 4.Instituto de Ciencias Marinas y Limnológicas, Facultad de CienciasUniversidad Austral de ChileValdiviaChile

Personalised recommendations