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Physiological effects of salinity on Delta Smelt, Hypomesus transpacificus

Abstract

Abiotic factors like salinity are relevant to survival of pelagic fishes of the San Francisco Bay Estuary. We tested the effects of 4 parts per thousand (ppt) salinity increases on Delta Smelt (DS) in a laboratory experiment simulating salinity increases that might occur around the low-salinity zone (LSZ) (<6 ppt). Adult DS, fed 2 % body mass per day, starting at 0.5 ppt [freshwater (FW)], were exposed to weekly step-increases of 4 ppt to a maximum of 10 ppt saltwater (SW) over 19 days, and compared to FW controls. DS (n = 12/treatment per sampling) were sampled at 24, 72, and 96 h (1, 3, and 4 days) post-salinity increase for analyses of hematocrit, plasma osmolality, muscle water content, gill chloride cell (CC) Na+/K+-ATPase (NKA) and apoptosis after being weighed and measured (n = 3 tanks per treatment). No apparent increase in length or weight occurred nor did a difference in survival. Following step-increases in SW, hematocrit increased over time. Other fish responses generally showed a pattern; specifically plasma osmolality became elevated at 1 day and diminished over 4 days in SW. Percent muscle water content (%) did not show significant changes. CCs showed increased NKA, cell size and apoptosis over time in SW, indicating that CCs turnover in DS. The cell renewal process takes days, at least over 19 days. In summary, DS are affected by salinities of the LSZ and ≤10 ppt, though they employ physiological strategies to acclimate.

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References

  • Allen PJ, Cech JJ, Kültz D (2009) Mechanisms of seawater acclimation in a primitive, anadromous fish, the green sturgeon. J Comp Physiol B 179(7):903–920

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Baskerville-Bridges B, Lindberg JC, Doroshov SI (2005) Manual for the intensive culture of Delta Smelt (Hypomesus transpacificus). University of California—Davis, Report to CALFED Bay-Delta Program, ERP-02-P31

  • Bennett WA (2005) Critical Assessment of the Delta Smelt population in the San Francisco Estuary, California. San Franc Estuary Watershed Sci 3(2):1–71. http://escholarship.org/uc/item/0725n5vk

  • Bennett WA, Kimmerer WJ, Burau JR (2002) Plasticity in vertical migration by native and exotic estuarine fishes in a dynamic low-salinity zone. Limnol Oceanogr 47(5):1496–1507

    Article  Google Scholar 

  • Brown LR, Bennett WA, Wagner RW, Morgan-King T, Knowles N, Feyrer F, Schoellhamer DH, Stacey MT, Dettinger M (2013) Implications for future survival of Delta Smelt from four climate change scenarios for the Sacramento–San Joaquin Delta, California. Estuaries Coasts 36:754–774

    Article  CAS  Google Scholar 

  • Cloern JE, Jassby AD (2012) Drivers of change in estuarine–coastal ecosystems: discoveries from four decades of study in San Francisco Bay. Rev Geophys 50(4):4001–4033

    Google Scholar 

  • Cloern JE, Nichols FH (1985) Timescales and mechanisms of estuarine variability, a synthesis from studies of San Francisco Bay. Hydrobiologia 129:229–237

    Article  Google Scholar 

  • Daborn K, Cozzi RRF, Marshall WS (2001) Dynamics of pavement cell-chloride cell interactions during abrupt salinity change in Fundulus heteroclitus. J Exp Biol 204:1889–1899

    CAS  PubMed  Google Scholar 

  • Dege M, Brown L (2004) Effect of outflow on spring and summertime distribution and abundance of larval and juvenile fishes in the Upper San Francisco Estuary. Am Fish Soc Symp 39:49–65

    Google Scholar 

  • Dimaggio MA, Ohs CL, Grabe SW, Petty BD, Rhyne AL (2010) Osmoregulatory evaluation of the Seminole Killifish after gradual seawater acclimation. N Am J Aquac 72:124–131

    Article  Google Scholar 

  • Evans DH, Claiborne JB (eds) (2006) The physiology of fishes, 3rd edn. Taylor and Francis Group, Boca Raton

    Google Scholar 

  • Ferrari MC, Ranaker L, Weinersmith KL, Young MJ, Sih A, Conrad JL (2014) Effects of turbidity and an invasive waterweed on predation by introduced largemouth bass. Environ Biol Fish 97(1):79–90

    Article  Google Scholar 

  • Feyrer F, Nobriga ML, Sommer TR (2007) Multidecadal trends for three declining fish species: habitat patterns and mechanisms in the San Francisco Estuary, California, USA. Can J Fish Aquat Sci 64:723–734

    Article  Google Scholar 

  • Feyrer F, Nobriga ML, Sommer TR (2011) Modeling the effects of future outflow on the abiotic habitat of an imperiled estuarine fish. Estuaries Coasts 34:120–128

    Article  Google Scholar 

  • Frenkel V, Goren M (2000) Factors affecting growth of killifish, Aphanius dispar, a potential biological control of mosquitoes. Aquaculture 184:255–265

    Article  Google Scholar 

  • Galvez F, Reid SD, Hawkings G, Goss G (2002) Isolation and characterization of mitochondria-rich cell types from the fill of freshwater rainbow trout. Am J Regul Integr Comp Physiol 282:R658–R668

    Article  CAS  Google Scholar 

  • Goss GG, Adamia S, Galvez F (2001) Peanut lectin binds to a subpopulation of mitochondria-rich cells in the Rainbow Trout gill epithelium. Am J Regul Integr Comp Physiol 281:R1718–R1725

    CAS  Google Scholar 

  • Grimaldo LF, Sommer T, Van Ark N, Jones G, Holland E, Moyle PB, Herbold B, Smith P (2009) Factors affecting fish entrainment into massive water diversions in a tidal freshwater estuary: Can fish losses be managed? N Am J Fish Manag 29(5):1253–1270

    Article  Google Scholar 

  • Hasenbein M, Komoroske LM, Connon RE, Geist J, Fangue N (2013) Turbidity and salinity affect feeding performance and physiological stress in the endangered Delta Smelt. Integr Comp Biol 53(4):620–634

    Article  CAS  PubMed  Google Scholar 

  • Hiroi J, Miyazaki H, Katoh F, Ohtani-Kaneko R, Kaneko T (2005) Chloride turnover and ion transporting activities of yolk-sac preparations (yolk balls) separated from Mozambique tilapia embryos and incubated in freshwater and seawater. J Exp Biol 208:3851–3858

    Article  CAS  PubMed  Google Scholar 

  • Hobbs JA, Bennett WA, Burton J (2007) Classification of larval and adult Delta Smelt to nursery areas by use of trace elemental fingerprinting. Trans Am Fish Soc 136:518–527

    Article  CAS  Google Scholar 

  • Hwang PP, Sun CM, Wu SM (1989) Changes of plasma osmolality, chloride concentration and gill Na–K-ATPase activity in tilapia Oreochromis mossambicus during seawater acclimation. Mar Biol 100:295–299

    Article  Google Scholar 

  • Jassby AJ, Kimmerer WJ, Monismith SG, Armor C, Cloern JE, Powell TM, Schubel JR, Vendlinski TJ (1995) Isohaline position as a habitat indicator for estuarine populations. Ecol Appl 5(1):272–289

    Article  Google Scholar 

  • Kammerer BD, Heppell S (2012) Individual condition indicators of thermal habitat quality in field populations of redband trout (Oncorhynchus mykiss gairdneri). Environ Biol Fish 96(7):823–835

    Article  Google Scholar 

  • Kammerer BD, Heppell SA (2013) The effects of semichronic thermal stress on physiological indicators in steelhead. Trans Am Fish Soc 142:1299–1307

    Article  CAS  Google Scholar 

  • Kammerer BD, Kültz D (2009) Prolonged apoptosis in mitochondria-rich cells of tilapia (Oreochromis mossambicus) exposed to elevated salinity. J Comp Physiol B 179:535–542

    Article  CAS  PubMed  Google Scholar 

  • 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 Part A 311A(2):80–90

    Article  Google Scholar 

  • Kammerer BD, Cech JJ Jr, Kültz D (2010) Rapid changes in plasma cortisol, osmolality, and respiration in response to salinity stress in tilapia (Oreochromis mossambicus). Comp Biochem Physiol Pt A 157:260–265

    Article  Google Scholar 

  • Kang CK, Tsai S-C, Lee T-H, Hwang P-P (2008) Differential expression of branchial Na+/K+-ATPase of two medaka species, Oryzias latipes and Oryzias dancena, with different salinity tolerances acclimated to fresh water, brackish water and seawater. Comp Biochem Physiol A 151:566–575

    Article  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Kiiskinen P, Hyvärinen H, Piironen J (2002) Smolting and seasonal variation in the smolt characteristics of one- and two-year-old Saimaa landlocked salmon under fish farm conditions. J Fish Biol 60:1015–1030

    Article  Google Scholar 

  • Kimmerer WJ (2002) Effects of freshwater flow on abundance of estuarine organisms: physical effects or trophic linkages? Mar Ecol Prog Ser 243:39–55

    Article  Google Scholar 

  • Kimmerer WJ (2011) Modeling Delta Smelt losses at the South Delta export facilities. San Franc Estuary Watershed Sci 9(1):1–11. http://escholarship.org/uc/item/0rd2n5vb?query=kimmerer

  • Kimmerer WJ, Nobriga ML (2008) Investigating particle transport and fate in the Sacramento–San Joaquin Delta using a particle transport model. San Franc Estuary Watershed Sci 6(1):1–28

    Google Scholar 

  • Kimmerer WJ, Gross ES, MacWilliams ML (2009) Is the response of estuarine nekton to freshwater flow in the San Francisco estuary explained by variation in habitat volume? Estuaries Coasts 32:375–389

    Article  Google Scholar 

  • Kimmerer WJ, MacWilliams ML, ES Gross (2013) Variation of fish habitat and extent of the low-salinity zone with freshwater flow in the San Francisco Estuary. San Franc Estuary Watershed Sci 11(4):1–18. http://escholarship.org/uc/item/3pz7x1x8?query=kimmerer

  • Knowles N, Cayan DR (2002) Potential effects of global warming on the Sacramento/San Joaquin watershed and the San Francisco Estuary. Geophys Res Lett 29:31–34

    Article  Google Scholar 

  • Knowles N, Cayan DR (2004) Elevational dependence of projected hydrologic changes in the San Francisco Estuary and Watershed. Clim Change 62:319–336

    Article  CAS  Google Scholar 

  • Komoroske L, Connon RE, Lindberg J, Cheng BS, Castillo G, Hasenbein M, Fangue NA (2014) Ontogeny influences sensitivity to climate change stressors in an endangered fish. Conserv Physiol 2:1–13

    Article  Google Scholar 

  • Kültz D (2005) Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 67:225–257

    Article  PubMed  Google Scholar 

  • Lima RN, Kültz D (2004) Laser scanning cytometry and tissue microarray analysis of salinity effects on killifish chloride cells. J Exp Biol 207:1729–1739

    Article  CAS  PubMed  Google Scholar 

  • Lehman PW, Teh SJ, Boyer GL, Nobriag ML, Bass E, Hogle C (2010) Initial impacts of Microcystis aeruginosa blooms on the aquatic food web in the San Francisco Estuary. Hydrobiologia 637:229–248

  • Lindberg J, Tigan G, Ellison L, Rettinghouse T, Nagel MM, Fisch KM (2013) Aquaculture methods for a genetically managed population of endangered Delta Smelt. N Am J Aquac 75(2):186–196

    Article  Google Scholar 

  • Loboschefsky E, Benigno G, Sommer T, Rose K, Ginn T, Massoudieh A, Loge F (2012) Individual-level and population-level historical prey demand of San Francisco Estuary Striped Bass using a bioenergetics model. San Franc Estuary Watershed Sci 10(1):1–23. http://escholarship.org/uc/item/1c788451?query=loboschefsky

  • Lougee LA, Bollens SM, Avent SR (2002) The effects of haloclines on the vertical distribution and migration of zooplankton. J Exp Biol Ecol 278:111–134

    Article  Google Scholar 

  • Lüthi AU, Martin SJ (2007) The CASBAH: a searchable database of caspase substrates. Cell Death Differ 14:641–650

    Article  PubMed  Google Scholar 

  • Marshall W (2002) Na+, Cl, Ca2+, and Zn2+ transport by fish gills: retrospective review and prospective synthesis. J Exp Zool 293:264–283

    Article  CAS  PubMed  Google Scholar 

  • Marshall WS, Emberley TR, Singer TD, Bryson SE, McCormick SD (1999) Time course of salinity adaptation in a strongly euryhaline estuarine teleost, Fundulus heteroclitus: a multivariable approach. J Exp Biol 202:1535–1544

    PubMed  Google Scholar 

  • Marshall WS, Cozzi RRF, Pelis RM, McCormick SD (2005) Cortisol receptor blockade and seawater adaptation in the euryhaline teleost Fundulus heteroclitus. J Exp Biol 303A:132–142

    CAS  Google Scholar 

  • McCormick S (ed) (1995) Hormonal control of gill Na+ K+-ATPase and chloride cell function. Academic Press, New York

    Google Scholar 

  • McCormick S, Regish AM, Christensen AK (2009) Distinct freshwater and seawater isoforms of Na+/K+-ATPase in gill chloride cells of Atlantic Salmon. J Exp Biol 212(24):3994–4001

    Article  CAS  PubMed  Google Scholar 

  • Meffe GK, Carroll CR (eds) (1997) Conservation biology. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Meng L, Matern SA (2001) Native and introduced larval fishes of Suisun Marsh California: the effects of freshwater flow. Trans Am Fish Soc 130(5):750–765

    Article  Google Scholar 

  • Morgan JD, Iwama GK (1991) Effects of salinity on growth, metabolism, and ionic regulation in juvenile rainbow trout and steelhead trout (Oncorhynchus mykiss) and fall Chinook Salmon (Onchornynchus tshawytscha). Can J Aquat Sci 48:2083–2094

    Article  Google Scholar 

  • Morgan JD, Sakamoto T, Grau EG, Iwama GK (1997) Physiological and respiratory responses of the Mozambique tilapia (Oreochromis mossambicus) to salinity acclimation. Comp Biochem Physiol A 117(3):391–398

    Article  Google Scholar 

  • Moyle PB (ed) (2002) Inland Fishes of California. University of California Press, Oakland

    Google Scholar 

  • Moyle PB, Cech JJ Jr (2004) Fishes: an introduction to ichthyology, 5th edn. Pearson Benjamin Cummings, San Francisco

    Google Scholar 

  • Moyle PB, Herbold B, Stevens DE, Miller LW (1992) Life history and status of delta smelt in the Sacramento–San Joaquin Estuary, California. Trans Am Fish Soc 121:67–77

    Article  Google Scholar 

  • Moyle PB, Bennett WA, Fleenor WE, Lund JR (2010) Habitat variability and complexity in the Upper San Francisco Estuary. San Franc Estuary Watershed Sci 8(3):1–24. http://escholarship.org/uc/item/0kf0d32x?query=moyle

  • Nobriga ML, Sommer TR, Feyrer F, Fleming K (2008) Long-term trends in summertime habitat suitability or Delta Smelt (Hypomesus transpacificus). San Franc Estuary Watershed Sci 6(1):1–13. http://escholarship.org/uc/item/5xd3q8tx?query=nobriga

  • Nordlie FG (2009) Environmental influences on regulation of blood plasma/serum components in teleost fishes: a review. Rev Fish Biol Fish 19:481–564

    Article  Google Scholar 

  • Ogoshi M, Kanoko K, Takahashi H, Ikeuchi T, Abe T, Sakamoto T (2012) Growth, energetic and the cortisol-hepatic glucocorticoid receptor axis of medaka (Oryzias latipes) in various salinities. Gen Comp Endocrinol 178:175–179

    Article  CAS  PubMed  Google Scholar 

  • Ott HC, Matthiesen TS, Goh S-K, Black LD, Kren SM, Netoff TI, Taylor DA (2007) Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med 14(2):213–221

    Article  Google Scholar 

  • Paltiel L, Ronningen K, Meltzer HM, Baker SV, Hoppin JA (2008) Evaluation of freeze thaw cycles on stored plasma in the Biobank of the norwegian mother and child cohort study. Cell Preserv Technol 6(3):223–230

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Pasupuleti N, Leon L, Carraway KL III, Gorin F (2013) 5-Benzylglycinyl-Amiloide kills proliferating and nonproliferating malignant glioma cells through Caspase-Independent necrosis mediated by apoptotis-inducing factor. J Pharmacol Exp Ther 344:600–615

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Paulsen M, Ussat S, Jakob M, Scherer G, Lepenies I, Schultze S, Kabelitz D, Adam-Klages S (2008) Interaction with XIAP prevents full Caspase 3/7 activation in proliferating human T lymphocytes. Eur J Immunol 38:1–9

    Article  Google Scholar 

  • Pearson MP, Stevens ED (1991) Size and hematological impact of the splenic erythrocyte reservoir in Rainbow Trout. Fish Physiol Biochem 9:39–50

    Article  CAS  PubMed  Google Scholar 

  • Pisam M, Prunet P, Boeuf G, Rambourg A (1988) Ultrastructural features of chloride cells in the gill epithelium of the Atlantic Salmon, Salmo salar, and their modifications during smoltification. Am J Anat 183:235–244

    Article  CAS  PubMed  Google Scholar 

  • Salman NA, Eddy FB (1988) Effect of dietary sodium chloride on growth, food intake and conversion efficiency in Rainbow Trout (Salmo gairdneri Richardson). Aquaculture 70:131–144

    Article  CAS  Google Scholar 

  • Salman NA, Eddy FB (1990) Increased sea-water adaptability of non-smolting rainbow trout by salt feeding. Aquaculture 86:259–270

    Article  Google Scholar 

  • Sardella BA, Cooper J, Gonzalez RJ, Brauner CJ (2004a) The effect of temperature on juvenile Mozambique tilapia hybrids (Oreochromis mossambicus x O. urolepis hornorum) exposed to full-strength and hypersaline seawater. Comp Biochem Physiol A 132:621–629

    Article  Google Scholar 

  • Sardella BA, Matey V, Cooper J, Gonzalez RJ, Brauner CJ (2004b) Physiological, biochemical, and morphological indicators of osmoregulatory stress in ‘California’ Mozambique tilapia (Oreochromis mossambicus O. urolepis hornorum) exposed to hypersaline water. J Exp Biol 207:1399–1413

    Article  CAS  PubMed  Google Scholar 

  • Sardella BA, Kültz D, Cech JJ Jr (2008a) Salinity-dependent changes in Na+/K+-ATPase content of mitochondria-rich cells contribute to differences in thermal tolerances of Mozambique tilapia. J Comp Physiol B 178:249–256

    Article  CAS  PubMed  Google Scholar 

  • Sardella BA, Sanmarti E, Kültz D (2008b) The acute temperature tolerance of green sturgeon (Acipenser medirostris) and the effect of environmental salinity. J Exp Zool 309A:477–483

    Article  Google Scholar 

  • Seifarth CC, Miertshcischk J, Hahn EG, Hensen J (2004) Measurement of serum and plasma osmolality in healthy young humans—influence of time and storage conditions. Clin Chem Lab Med 42(8):927–932

    Article  CAS  PubMed  Google Scholar 

  • Slater S, Baxter R (2014) Diet, prey selection, and body condition of age-0 Delta Smelt Hypomesus transpacificus in the Upper San Francisco Estuary. San Franc Estuary Watershed Sci J 12(3):1–24. http://escholarship.org/uc/item/52k878sb?query=slaterandbaxter

  • Sommer T, Armor C, Baxter R, Breuer R, Brown L, Chotkowski M, Culberson S, Feyrer F, Gringas M, Herbold B, Kimmerer W, Mueller-Solger A, Nobriga M, Souza K (2007) The collapse of pelagic fishes in the Upper San Francisco Estuary. Fisheries 32(6):270–277

    Article  Google Scholar 

  • Sommer T, Mejia FH, Nobriga ML, Feyrer F, Grimaldo L (2011) The spawning migration of Delta Smelt in the Upper San Francisco Estuary. San Franc Estuary Watershed Sci 9(2):1–16. http://escholarship.org/uc/item/86m0g5sz?query=sommer,nobriga

  • Swanson C, Mager RC, Doroshov SI, Cech JJ Jr (1996) Use of salts, anesthetics, and polymers to minimize handling and transport mortality in Delta Smelt. Trans Am Fish Soc 125(2):326–329

    Article  CAS  Google Scholar 

  • Swanson C, Young PS, Cech JJ Jr (1998) Swimming performance of Delta Smelt: maximum performance, and behavioral and kinematic limitations on swimming at submaximal velocities. J Exp Biol 201:333–345

    PubMed  Google Scholar 

  • Swanson C, Reid T, Young PS, Cech JJ Jr (2000) Comparative environmental tolerances of threatened Delta Smelt (Hypomesus transpacficus) and introduced wakasagi (Hypomesus nipponensis) in an altered California estuary. Oecologia 123:384–390

    Article  Google Scholar 

  • Thrall MA, Weiser G, Allison RW, Campbell TW (2012) Veterinary hematology and clinical chemistry, 2nd edn. Wiley, Hobeken, pp 608–609

    Google Scholar 

  • Vermeij GJ (ed) (1987) Evolution and escalation: an ecological history of life. Princeton University Press, Princeton

    Google Scholar 

  • Wang JS (2007) Spawning, early life stages, and early life histories of the Osmerids found in the Sacramento–San Joaquin Delta of California. Tracy Fish Facility Studies. Bureau of Reclamation, pp 1–72. http://www.usbr.gov/mp/TFFIP/tracyreports/TracyReportsVolume38.pdf

  • Wendelaar Bonga SE, Vander Meij SA (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 255:235–243

    Article  Google Scholar 

  • Whitehead A, Roach JL, Zhang S, Galvez F (2012) Salinity- and population-dependent genome regulatory response during osmotic acclimation in the killifish (Fundulus heteroclitus) gill. J Exp Biol 215:1293–1305

    Article  PubMed  Google Scholar 

  • Yang M, Huang WT, Tsai MJ, Jiang IF, Weng CF (2009) Transient response of brain heat shock protein 70 and 90 to acute osmotic stress in tilapia (Oreochromis mossambicus). Zool Stud 48(6):723–736

    CAS  Google Scholar 

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Acknowledgments

This project was supported by California SeaGrant/Delta Science (grant #2053, Project # R/SF-55) to the University of California, Davis (UC D). All work was conducted in compliance with the Institutional Care and Use Committee Protocol #17332 at UC Davis. Thank you to the Fish Conservation and Culture Laboratory at UC D, Byron, CA for supplying Delta Smelt and equipment. This work was carried out in the Aquatic Health Program, UC Davis, at CABA of whom we would like to thank. Thanks is due also to CABA staff, Stephen Bennett, Professors Silas Hung, Dietmar Kültz and Pam Lein for technical support and also Dr. Bruce Hammock for his editorial comments.

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Kammerer, B.D., Hung, TC., Baxter, R.D. et al. Physiological effects of salinity on Delta Smelt, Hypomesus transpacificus . Fish Physiol Biochem 42, 219–232 (2016). https://doi.org/10.1007/s10695-015-0131-0

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Keywords

  • Delta Smelt
  • Fluorescent confocal microscopy
  • Salinity
  • Na+/K+-ATPase
  • Apoptosis
  • Chloride cells
  • Physiology
  • Low-salinity zone