Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-03T00:38:15.573Z Has data issue: false hasContentIssue false
  • English
  • Français

Maintenance of ionic gradients and tissue hydration in the intertidal sea cucumber Holothuria grisea under hypo- and hyper-salinity challenges

Published online by Cambridge University Press:  19 September 2016

Giovanna C. Castellano ,
Ivonete Aparecida Santos  and
Carolina A. Freire
Giovanna C. Castellano
Affiliation:
Graduate Programme in Zoology, Universidade Federal do Paraná, Curitiba, PR, Brazil
Ivonete Aparecida Santos
Affiliation:
Graduate Programme in Molecular and Cell Biology, Universidade Federal do Paraná, Curitiba, PR, Brazil
Carolina A. Freire*
Affiliation:
Department of Physiology, Universidade Federal do Paraná, Caixa Postal 19031, CEP 81531-980 Curitiba, PR, Brazil
*
Correspondence should be addressed to: Dr C.A. Freire Graduate Program in Zoology, Universidade Federal do Paraná, Curitiba, PR, Brazil email: [email protected] or [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Echinoderms are exclusively marine, osmoconformer invertebrates. Their distribution patterns are strongly influenced by salinity. Nevertheless, several species of the phylum inhabit the challenging intertidal zone, characterized by steep and fast salinity fluctuations. This study evaluated the response of coelomic fluid ionic concentrations (sodium, chloride, magnesium and potassium) of the intertidal sea cucumber Holothuria grisea to hypo- and hypersaline challenges. A stepwise protocol was performed for the whole animal exposure to both anisosmotic conditions: from 35 to 15 psu along 8 h, and from 35 to 45 psu along 6 h, to simulate intertidal conditions. Tissue water regulation by the longitudinal muscle, oesophagus and posterior intestine was also evaluated, upon hypo- and hyper-osmotic shocks of 20 and 50% of intensity with respect to the isosmotic control. Ionic gradients were observed between coelomic fluid and external water, mainly for potassium and magnesium, but also sodium, and in a greater extent under hyposaline conditions than under hypersaline exposure. Consistently, H. grisea shows retracted tube feet in 15 psu, but a more relaxed appearance and exposed tube feet in 45 psu. In addition, H. grisea showed greater capacity for tissue water maintenance during hyper- than in hyposmotic conditions. Holothuria grisea shows an avoidance behaviour in low salinity (thus sustaining ionic gradients), preventing its tissues from intense swelling. This strategy allows it to dwell in the intertidal region.

Keywords

chloridecoelomic fluidechinodermoesophagusintestinelongitudinal musclemagnesiumpotassiumsodium
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 2 , March 2018 , pp. 325 - 332
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Amado, E.M., Freire, C.A. and Souza, M.M. (2006) Osmoregulation and tissue water regulation in the freshwater red crab Dilocarcinus pagei (Crustacea, Decapoda), and the effect of waterborne inorganic lead. Aquatic Toxicology 79, 1–8.CrossRefGoogle ScholarPubMed
Barker, M.F. and Russell, M.P. (2008) The distribution and behaviour of Patiriella mortenseni and P. regularis in the extreme hyposaline conditions of the Southern New Zealand Fiords. Journal of Experimental Marine Biology and Ecology 35, 76–84.CrossRefGoogle Scholar
Binyon, J. (1962) Ionic regulation and mode of adjustment to reduced salinity of the starfish Asterias rubens . Journal of the Marine Biological Association of the United Kingdom 42, 49–69.CrossRefGoogle Scholar
Binyon, J. (1966) Salinity tolerance and ionic regulation. In Boolootian, R.A. (ed.) Physiology of Echinodermata. New York, NY: Interscience, pp. 359–377.Google Scholar
Bishop, D., Lee, K.J. and Watts, S.A. (1994) A comparison of osmolality and specific ion concentrations in the fluid compartments of the regular sea urchin L. variegatus Lamarck (Echinodermata: Echinoidea) in varying salinities. Comparative Biochemistry and Physiology, Part A 108, 497–502.CrossRefGoogle Scholar
Boolootian, R.A. (1966) Physiology of Echinodermata. New York, NY: Interscience.Google Scholar
Calil, P., Rocha, R.M.D., Freire, C.A. and Roper, J.J. (2009) The role of Asterina stellifera (Echinodermata: Asteroidea) as a predator in a rocky intertidal community in southern Brazil. Zoologia 26, 279–287.CrossRefGoogle Scholar
D'Andrea-Winslow, L., Strohmeier, G.R., Rossi, B. and Hofman, P. (2001) Identification of a sea urchin Na+/K+/2Cl− cotransporter (NKCC): microfilament-dependent surface expression is mediated by hypotonic shock and cyclic AMP. Journal of Experimental Biology 204, 147–156.CrossRefGoogle ScholarPubMed
Diehl, W.J. (1986) Osmoregulation in echinoderms. Comparative Biochemistry and Physiology, Part A 84, 199–205.CrossRefGoogle Scholar
Diehl, W.J. and Lawrence, J.M. (1984) The effect of salinity on coelomic fluid osmolyte concentration and intracellular water content in Luidia clathrata (Say) (Echinodermata: Asteroidea). Comparative Biochemistry and Physiology, Part A 79, 19–126.Google Scholar
Diehl, W.J. and Lawrence, J.M. (1985) Effect of salinity on the intracellular osmolytes in the pyloric caeca and tube feet of Luidia clathrata (Say) (Echinodermata: Asteroidea). Comparative Biochemistry and Physiology, Part A 82, 559–566.CrossRefGoogle Scholar
Dong, Y., Dong, S. and Meng, X. (2008) Effects of thermal and osmotic stress on growth, osmoregulation and Hsp70 in sea cucumber (Apostichopus japonicas Selenka). Aquaculture 276, 179–186.CrossRefGoogle Scholar
Eylers, J.P. (1982) Ion-dependent viscosity of holothurian body wall and its implications for the functional morphology of echinoderms. Journal of Experimental Biology 99, 1–8.CrossRefGoogle Scholar
Foglietta, L.M. and Herrera, F.C. (1996) Ionosmotic response of respiratory trees of the holothurian Isostichopus badionotus Selenka preincubated in hyper-, iso-and hypo-osmotic sea water. Journal of Experimental Marine Biology and Ecology 202, 151–164.CrossRefGoogle Scholar
Foster, C., Amado, E.M., Souza, M.M. and Freire, C.A. (2010) Do osmoregulators have lower capacity of muscle water regulation than osmoconformers? A study on decapod crustaceans. Journal of Experimental Zoology A 313, 80–94.CrossRefGoogle Scholar
Freire, C.A., Santos, I.A. and Vidolin, D. (2011) Osmolality and ions of the perivisceral coelomic fluid of the intertidal sea urchin Echinometra lucunter (Echinodermata: Echinoidea) upon salinity and ionic challenges. Zoologia 28, 479–487.CrossRefGoogle Scholar
García-Franco, M. (1992) Anaesthetics for the squid Sepioteuthis sepioidea (Mollusca: Cephalopoda). Comparative Biochemistry and Physiology, Part A 103, 121–123.CrossRefGoogle Scholar
Häussinger, D. (1996) The role of cellular hydration in the regulation of cell function. Biochemical Journal 313, 697–710.CrossRefGoogle ScholarPubMed
Hayashi, Y. and Motokawa, T. (1986) Effects of ionic environment on viscosity of catch connective tissue in holothurian body wall. Journal of Experimental Biology 125, 71–84.CrossRefGoogle Scholar
Hendler, G., Miller, J.E., Pawson, D.L. and Kier, P.M. (1995) Sea stars, sea urchins, and allies. Echinoderms of Florida and the Caribbean. Washington, DC: Smithsonian Institution Press.Google Scholar
Hidaka, M. (1982) Effects of certain physico-chemical agents on the mechanical properties of the catch apparatus of the sea urchin spine. Journal of Experimental Biology 103, 15–29.CrossRefGoogle Scholar
Hoffmann, E.K. and Dunham, P.B. (1995) Membrane mechanisms and intracellular signaling in cell volume regulation. International Review of Cytology 161, 173–262.CrossRefGoogle ScholarPubMed
Hoffmann, E.K., Lambert, I.H. and Pedersen, S.F. (2009) Physiology of cell volume regulation in vertebrates. Physiological Reviews 89, 193–277.CrossRefGoogle ScholarPubMed
Lange, R. (1964) The osmotic adjustment in the echinoderm Strongylocentrotus droebachiensis . Comparative Biochemistry and Physiology 13, 205–216.CrossRefGoogle Scholar
Leong, P.K.K. and Manahan, D.T. (1997) Metabolic importance of Na+/K+-ATPase activity during sea urchin development. Journal of Experimental Biology 200, 2881–2892.CrossRefGoogle ScholarPubMed
Leong, P.K.K. and Manahan, D.T. (1999) Na+/K+-ATPase activity during early development and growth of an antartic sea urchin. Journal of Experimental Biology 202, 2051–2058.CrossRefGoogle Scholar
Madrid, E., Zanders, I.P. and Herrera, F.C. (1976) Changes in coelomic fluid and intracellular ionic composition in holothurians exposed to diverse sea water concentrations. Comparative Biochemistry and Physiology, Part A 54, 167–174.CrossRefGoogle Scholar
Mendes, F.M., Marenzi, A.W.C. and Di Domenico, M. (2006) Population patterns and seasonal observations on density and distribution of Holothuria grisea (Holothuroidea: Aspidochirotida) on the Santa Catarina coast, Brazil. SPC Beche-de-mer Information Bulletin 23, 5–10.Google Scholar
Meng, X.L., Dong, Y.W. and Dong, S.L. (2015) Large-scale mortality and limited expression of heat shock proteins of aestivating sea cucumbers Apostichopus japonicus after acute salinity decrease. Aquaculture Research 46, 1573–1581.CrossRefGoogle Scholar
Meng, X.L., Dong, Y.W., Dong, S.L., Yu, S.S. and Zhou, X. (2011) Mortality of the sea cucumber, Apostichopus japonicas Selenka, exposed to acute salinity decrease and related physiological responses: osmoregulation and heat shock protein expression. Aquaculture 316, 88–92.CrossRefGoogle Scholar
Mercier, A., Battaglene, S.C. and Hamel, J.F. (1999) Daily burrowing cycle and feeding activity of juvenile sea cucumbers Holothuria scabra in response to environmental factors. Journal of Experimental Marine Biology and Ecology 239, 125–156.CrossRefGoogle Scholar
Mosher, C. (1980) Distribution of Holothuria arenicola Semper in the Bahamas with observations on habitat, behavior, and feeding activity (Echinodermata: Holothuroidea). Bulletin of Marine Sciences 30, 1–12.Google Scholar
Motokawa, T. (1984) Connective tissue catch in echinoderms. Biological Reviews 59, 255–270.CrossRefGoogle Scholar
Motokawa, T. (1994) Effects of ionic environment on viscosity of triton-extracted catch connective tissue of a sea cucumber body wall. Comparative Biochemistry and Physiology 109B, 613–622.Google Scholar
Pagett, R.M. (1980) Distribution of sodium, potassium and chloride in the ophiuroid, Ophiocomina nigra (Abildgaard). Journal of the Marine Biological Association of the United Kingdom 60, 163–170.CrossRefGoogle Scholar
Pierce, S.K. (1982) Invertebrate cell volume control mechanisms: a coordinated use of intracellular amino acids and inorganic ions as osmotic solute. Biological Bulletin 163, 405–419.CrossRefGoogle Scholar
Prosser, C.L. (1973) Comparative animal physiology. Philadelphia, PA: WB Saunders Co.Google Scholar
Prusch, R.D. (1977) Solute secretion by the tube foot epithelium in the starfish Asterias forbesi . Journal of Experimental Biology 68, 35–43.CrossRefGoogle Scholar
Prusch, R.D. and Whoriskey, F. (1976) Maintenance of fluid volume in the starfish water vascular system. Nature 262, 577–578.CrossRefGoogle ScholarPubMed
Robertson, J.D. (1949) Ionic regulation in some marine invertebrates. Journal of Experimental Biology 26, 182–200.CrossRefGoogle ScholarPubMed
Robertson, J.D. (1953) Further studies on ionic regulation in marine invertebrates. Journal of Experimental Biology 30, 277–296.CrossRefGoogle Scholar
Ruppert, E.E. and Fox, R.S. (2004) Invertebrate zoology: a functional evolutionary approach (of RD Barnes’ Invertebrate zoology). Belmont, CA: Brooks/Cole.Google Scholar
Russell, M.P. (2013) Echinoderm responses to variation in salinity. Advances in Marine Biology 66, 171–212.CrossRefGoogle ScholarPubMed
Santos, I.A., Castellano, G.C. and Freire, C.A. (2013) Direct relationship between osmotic and ionic conforming behavior and tissue water regulatory capacity in echinoids. Comparative Biochemistry and Physiology, Part A 164, 466–476.CrossRefGoogle ScholarPubMed
Santos-Gouvea, I.A. and Freire, C.A. (2007) Effects of hypo- and hypersaline seawater on the microanatomy and ultrastructure of epithelial tissues of Echinometra lucunter (Echinodermata: Echinoidea) of intertidal and subtidal populations. Zoological Studies 46, 221–233.Google Scholar
Sardini, A., Amey, J.S., Weylandt, K.H., Nobles, M., Valverde, M.A. and Higgins, C.F. (2003) Cell volume regulation and swelling-activated chloride channels. Biochimica et Biophysica Acta (BBA) – Biomembranes 1618, 153–162.CrossRefGoogle ScholarPubMed
Shumway, S.E. (1977) The effects of fluctuating salinities on four species of asteroid echinoderms. Comparative Biochemistry and Physiology, Part A 58, 177–179.CrossRefGoogle Scholar
Stancyk, S.E. and Shaffer, P.L. (1977) The salinity tolerance of Ophiothrix angulata (Say) (Echinodermata: Ophiuroidea) in latitudinally separate populations. Journal of Experimental Marine Biology and Ecology 29, 35–43.CrossRefGoogle Scholar
Stickle, W.B. and Ahokas, R. (1974) The effects of tidal fluctuation of salinity on the perivisceral fluid composition of several echinoderms. Comparative Biochemistry and Physiology 47, 469–476.CrossRefGoogle Scholar
Stickle, W.B. and Denoux, G.J. (1976) Effects of in situ tidal salinity fluctuations on osmotic and ionic composition of body fluid in Southeastern Alaska Rocky intertidal fauna. Marine Biology 37, 125–135.CrossRefGoogle Scholar
Stickle, W.B. and Diehl, W.J. (1987) Effects of salinity on echinoderms. In Jangoux, M. and Lawrence, J.M. (eds) Echinoderm studies II. Rotterdam: AA Balkema, pp. 235–285.Google Scholar
Vadas, R.L., Elner, R.W., Garwood, P.E. and Babb, I.G. (1986) Experimental evaluation of aggregation behavior in the sea urchin Strongylocentrotus droebachiensis . Marine Biology 90, 433–448.CrossRefGoogle Scholar
Vidolin, D., Santos-Gouvea, I.A. and Freire, C.A. (2002) Osmotic stability of the coelomic fluids of a sea cucumber (Holothuria grisea) and a starfish (Asterina stellifera) (Echinodermata) exposed to the air during low tide: a field study. Acta Biologica Paranaense 31, 113–121.Google Scholar
Vidolin, D., Santos-Gouvea, I.A. and Freire, C.A. (2007) Differences in ion regulation in the sea urchins Lytechinus variegatus and Arbacia lixula (Echinodermata: Echinoidea). Journal of the Marine Biological Association of the United Kingdom 87, 769–775.CrossRefGoogle Scholar
Wang, Q.L., Yu, S.S., Qin, C.X., Dong, S.L. and Dong, Y.W. (2014) Combined effects of acute thermal and hypo-osmotic stresses on osmolality and hsp70, hsp90 and sod expression in the sea cucumber Apostichopus japonicus Selenka. Aquaculture International 22, 1149–1161.CrossRefGoogle Scholar
Wehner, F., Olsen, H., Tinel, H., Kinne-Saffran, E. and Kinne, R.K.H. (2003) Cell volume regulation: osmolytes, osmolyte transport, and signal transduction. Reviews of Physiology, Biochemistry and Pharmacology 148, 1–80.CrossRefGoogle ScholarPubMed