Abstract
This paper evaluates the response of trout exposed to acute hypoxia between 8.7 mgO2/l (controls) and 1.4 mgO2/l. Temperature, pH, NH4, oxygen consumption rate and spleen-somatic index (SSI) were evaluated. Blood cell counts, oxidative radicals (ORs) production and immature erythrocytes were assessed to evaluate their relationship with the degree of hypoxia. Acute hypoxia induced a decrease in water pH (p < 0.05), oxygen consumption rate (60% less), SSI (55% less) and a significant increase of water ammonium concentration (p < 0.05). Haematocrit increased significantly starting at 4.8 mgO2/l, as well as an increase in the total number of leukocytes (up to 50% in some fish). Starting at 2 mgO2/l, swelling of erythrocytes was induced and a decrease in the potential production of ORs, showing a negative correlation to immature erythrocyte numbers. These results suggest that lower than normal oxygen concentrations may jeopardize ORs production and hence non-specific defence mechanisms in trout. High percentages of immature erythrocytes can be used as a simple and inexpensive indicator of both hypoxic events and impairment of ORs production in the absence of bleeding, haemolysis, anti-anaemia treatments and/or increased temperature.
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D.B. Allen J.J. Maguire M. Mahdavian C. Wicke L. Marcocci H. Scheuenstuhl M. Chang A.X. Le H.W. Hopf T.K. Hunt (1997) ArticleTitleWound hypoxia and acidosis limit neutrophil bacterial killing mechanisms Arch. Surg. 132 991–996 Occurrence Handle1:CAS:528:DyaK2sXmsVantL8%3D Occurrence Handle9301612
R.S. Anderson L.L. Brubacher L.R. Calvo M.A. Unger E.M. Burreson (1998) ArticleTitleEffects of tributyl and hypoxia on the progression of Perkinsus marinum infections and host defence mechanisms in oyster, Crassostrea virginica (Gmelin) J. Fish Dis. 21 371–379 Occurrence Handle10.1046/j.1365-2761.1998.00128.x Occurrence Handle1:CAS:528:DyaK1cXntFGhs78%3D
D.P. Anderson A.K. Siwicki (1993) Measuring the effects of contaminants on fish by hematolgucal and serological methods J. Stolen D.P. Anderson J. Selikoff L. Twerdok Kaattari (Eds) Modulators of Fish Immune Response SOS Publications Fair Haeven, NJ 97–116
B.M. Babior (1999) ArticleTitleNADPH Oxidase: An Update Blood 93 IssueID5 1464–1476 Occurrence Handle1:CAS:528:DyaK1MXhsFertbg%3D Occurrence Handle10029572
Beck, W. 1981. Hematopoyesis an Introduction to the anemias in Haematology Edited by William S. Beck, 3rd Edition.
Blanco, C.C. 1995. La trucha, cría industrial. 2da Edición. Ediciones Mundi-Prensa. Madrid.
K.A. Boleza L.E. Burnett K.G. Burnett (2001) ArticleTitleHypercapnic hypoxia compromises bactericidal activity of fish anterior kidney cells against opportunistic environmental pathogens Fish Shellfish Immunol. 11 593–610 Occurrence Handle10.1006/fsim.2001.0339 Occurrence Handle1:STN:280:DC%2BD3MrksFGgtA%3D%3D Occurrence Handle11592587
J.N. Boyd L.E. Burnett (1999) ArticleTitleReactive oxygen intermediate production by oyster haemocytes exposed to hypoxia J. Exp. Biol. 202 3135–3143 Occurrence Handle1:CAS:528:DC%2BD3cXjvFKkuw%3D%3D Occurrence Handle10539962
M.L. Burleson B.D. Wilhelm N.J. Smatresk (2001) ArticleTitleThe influence of fish size on the avoidance of hypoxia and oxygen selection by largemouth bass J. Fish Biol. 59 1336–1349
L.E. Burnett (1997) ArticleTitleThe challenges of living in hypoxic and hypercapnic aquatic environments Am. Zool. 37 633–640
T.W. Campbell F. Murru (1990) ArticleTitleAn introduction to fish haematology Compendium Continuing Edu. Vet. Sci. 12 525–533
S. Chung C.J. Secombes (1988) ArticleTitleAnalysis of events occurring within teleost macrophages during the respiratory burst Comp. Biochem. Physiol. 89B 539–544 Occurrence Handle1:CAS:528:DyaL1cXhs1Kjsr8%3D
H. Groot ParticleDe A. Littauer (1989) ArticleTitleHypoxia. Reactive oxygen and cell injury Free. Radic. Biol. Med. 6 541–551 Occurrence Handle2663666
W. Dröge (2002) ArticleTitleFree radicals in the physiological control of cell function Physiol Rev. 82 48–95
S.W. Edwards M.B. Hallett A.K. Campbell (1984) ArticleTitleOxygen radicals production may be limited by oxygen concentration Biochem. J. 217 851–854 Occurrence Handle1:CAS:528:DyaL2cXms1WksQ%3D%3D Occurrence Handle6712601
G.M. Feldman A.M. Dannenberg J.L. Seed (1990) ArticleTitlePhysiologic oxygen tensions limit oxidant-mediated killing of schistosome eggs by inflammatory cells and isolated granulomas J. Leukoc. Biol. 47 344–354 Occurrence Handle1:CAS:528:DyaK3cXitlerurY%3D Occurrence Handle2319208
Y. Fukuda M. Maita K. Satoh N. Okamoto (1997) ArticleTitleInfluence of dissolved oxygen concentration on the mortality of Yellowtail experimentally infected with Enterococcus seriolicida Fish Pathol. 32 129–130
T.G. Gabig B.M. Babior (1981) ArticleTitleThe killing of pathogens by phagocytes Annu. Rev. Med. 32 313–326 Occurrence Handle10.1146/annurev.me.32.020181.001525 Occurrence Handle1:CAS:528:DyaL3MXhslanu7c%3D Occurrence Handle7013670
D.J. Hackam S. Grinstein A. Nathens W.G. Watson J.C. Marshall O.D. Rotstein (1996) ArticleTitleExudative neutrophils show impaired pH regulation compared with circulating neutrophils Arch Surg. 131 1296–1301 Occurrence Handle1:STN:280:ByiC3MrjslQ%3D Occurrence Handle8956771
J.W. Kiceniuk E. Colbourne (1997) ArticleTitleRelating oxygen levels in the Newfoundland offshore waters to the physiology of Atlantic cod (Gadus morhua) Can. J. Fish Aquat. Sci. 54 IssueID1 81–87 Occurrence Handle10.1139/cjfas-54-S1-81
J. Kita Y. Itazawa (1989) ArticleTitleRelease of erythrocytes from the spleen during exercise and splenic constriction by adrenaline infusion in the rainbow trout Jpn. J. Ichthyol. 36 IssueID1 48–52
J. Kita Y. Itazawa (1990) ArticleTitleEffects of adrenaline on the blood flow through the spleen of rainbow trout (Salmo gairdneri) Comp. Biochem. Physiol. 95A IssueID4 591–595 Occurrence Handle1:CAS:528:DyaK3cXktVemsLw%3D
G.W. Klontz (1994) Fish hematology J.D. Stolen A.F. Rowley J.T. Zelikoff S.L. Kaatari S.A. Smith (Eds) Techniques in Fish Immunology SOS Publications Fair Haven, USA
T. Leklin M. Nikinmaa (1999) ArticleTitleSeasonal and temperature effects on the adrenergic responses on the Artic charr (Salvelinus alpinus) erythrocytes J. Exp. Biol. 202 2233–2238
T. Leklin A. Tuominen M. Nikinmaa (2000) ArticleTitleThe adrenergic volume changes of immature and mature rainbow trout (Oncorhynchus mykiss) erythrocytes J. Exp. Biol. 203 3025–3031
G.C. Moullac ParticleLe C. Soyez D. Ansquer C. Saulnier D. Christophe P. Levy (1999) ArticleTitleEffect of hypoxic stress on the immune response and the resistance to Vibriosis of the shrimp Penaeus stylirostris Fish Shellfish Immunol. 8 621–629
J. López-Barneo R. Pardal P. Ortega-Sáenz (2001) ArticleTitleCellular mechanisms Of Oxygen Sensing Annu. Rev. Physiol. 63 259–87 Occurrence Handle11181957
J.B. Miale (1982) Laboratory Medicine. Haematology EditionNumber6 The C. V. Mosley Company USA 1084
M. Nikinmaa (1997) ArticleTitleOxygen and carbon dioxide transport in vertebrate erythrocytes: an evolutionary change in the role of membrane transport J. Exp. Biol. 200 369–380 Occurrence Handle1:CAS:528:DyaK2sXhslOnsbk%3D Occurrence Handle9050246
M. Nikinmaa A. Soivio (1982) ArticleTitleBlood oxygen transport of hypoxic Salmo gairdneri J. Exp. Zool. 219 173–178 Occurrence Handle10.1002/jez.1402190206 Occurrence Handle1:CAS:528:DyaL38XhtVWht7g%3D Occurrence Handle7061970
W.W. Nixon (1995) ArticleTitleCoastal marine eutrophication: a definition, social causes, and future concerns Ophelia 41 199–219
H.W. Paerl J.L. Pinckney J.M. Fear B.L. Peierls (1999) ArticleTitleEcosystem responses to internal and watershed organic matter loading-consequences for hypoxia in the eutrophying Neuse River estuary, NC Mar. Ecol. Prog. Ser. 166 17–25
S.F. Perry S.D. Reid (1992) ArticleTitleRelationship between blood O2 content and catecholamines levels during hypoxia in rainbow trout and American eel Am. J. Physiol. Regul. Integr. Comp. Physiol. 263 240–249
S.F. Perry S.G. Reid E. Wankiewicz V. Iyer K.M. Gilmour (1996) ArticleTitlePhysiological responses of rainbow trout (Oncorhynchus mykiss) to prolonged exposure to softwater Physiol. Zool. 69 1419–1441
P.M. Pierson A. Lamers G. Flik N. Mayer-Gostan (2004) ArticleTitleThe stress axis, stanniocalcin, and ion balance in rainbow trout Gen. Comp. Endocrinol. 137 263–271 Occurrence Handle10.1016/j.ygcen.2004.03.010 Occurrence Handle1:CAS:528:DC%2BD2cXkvVKmtLg%3D Occurrence Handle15201064
M.D. Powell S.F. Perry (1997) ArticleTitleRespiratory and acid-base disturbances in rainbow trout blood during exposure to chloramine-T under hypoxia and hyperoxia J. Fish Biol. 50 418–428 Occurrence Handle1:CAS:528:DyaK2sXhvV2iu7g%3D
N.N. Rabalais W.J. Wiseman SuffixJr R.E. Turner (1994) ArticleTitleComparison of continuous records of near-bottom dissolved oxygen from the hypoxia zone along the Louisiana coast Estuaries 17 850–861 Occurrence Handle1:CAS:528:DyaK2MXltlGmsbc%3D
S.G. Reid S.F. Perry (1991) ArticleTitleThe effects and physiological consequences of raised levels of cortisol on rainbow trout (Oncorhynchus mykiss) erythrocyte β-adrenoceptors J. Exp. Biol. 158 217–240 Occurrence Handle1:CAS:528:DyaK3MXlsFGmsr8%3D Occurrence Handle1680955
C. Swallow S. Grinstein R. Sudsberg O.D. Rostein (1993) ArticleTitleRelative roles of Na+/H+ exchange and vacuolar-type H+-ATPases in regulating cytoplasmic pH and function in murine peritoneal macrophages J. Cell Physiol. 157 453–460 Occurrence Handle10.1002/jcp.1041570304 Occurrence Handle1:CAS:528:DyaK2cXivVamuw%3D%3D Occurrence Handle8253856
J.L. Taft W.R. Taylor E.O. Hartwig R. Loftus (1980) ArticleTitleSeasonal oxygen depletion in the Chesapeake Bay Estuaries 3 242–247
J.C. Taylor J.M. Miller (2001) ArticleTitlePhysiological performance of juvenile southern flounder, Paralichthys lethostigma (Jordan and Gilbert, 1884), in chronic and episodic hypoxia J. Exp. Mar. Biol. Ecol 258 195–214 Occurrence Handle10.1016/S0022-0981(01)00215-5 Occurrence Handle11278010
R.E. Turner W.W. Schroeder W.J. Wiseman SuffixJr. (1987) ArticleTitleThe role of stratification in the deoxygenation of Mobile Bay and the adjacent shelf bottom waters Estuaries 10 13–19 Occurrence Handle1:CAS:528:DyaL2sXlvVaqurc%3D
Vogelbein, W.K., Zwerner, D.E., Kator, H., Rhodes, M. and Cardinal, J. 1999. Epizootic mycobacteriosis in Chesapeake Bay striped bass. In: Proceedings of the 24th Annual Eastern Fish Health Workshop, 8–11 March 1999, National Fish Health Research Laboratory, Atlantic Beach, NC. West Virginia.
G.A. Wedemeyer B.A. Barton D.J. McLeay (1990) Stress and acclimation C.B. Schreck P.B. Moyle (Eds) Methods for Fish Biology American Fisheries Society Bethesda, Maryland 451–489
J. Wojtaszek D. Dziewulska-Szwajkowska M. Lozinska-Gabska A. Adamowicz A. Dzugaj (2002) ArticleTitleHematological effects of high dose of cortisol on the carp (Ciprinus carpio L.): Cortisol effect on the Carp Blood Gen. Comp. Endocrinol. 125 176–183 Occurrence Handle10.1006/gcen.2001.7725 Occurrence Handle1:CAS:528:DC%2BD38Xhs1yrtrs%3D Occurrence Handle11884063
R.N. Winn D.M. Knott (1992) ArticleTitleAn overview of environmental health in populations exposed to hypoxia in the Savannah River estuary Mar. Ecol. Prog. Ser. 88 161–179
J.H. Zar (1994) Biostatistical Analysis Englewood Cliffs NJ 662
J.J. Zulueta F.S. Yu V.J. Thannickal P.M. Hassoun (1995) ArticleTitleRelease of hydrogen peroxide in response to hypoxiareoxygenation: role of an NAD(P)H oxidase-like enzyme in endothelial cell plasma membrane Am. J. Resp. Cell Mol. Biol. 12 41–49 Occurrence Handle1:CAS:528:DyaK2MXksFCrtL0%3D
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Valenzuela, A., Silva, V., Tarifeño, E. et al. Effect of Acute Hypoxia in Trout (Oncorhynchus mykiss) on Immature Erythrocyte Release and Production of Oxidative Radicals. Fish Physiol Biochem 31, 65–72 (2005). https://doi.org/10.1007/s10695-005-5288-5
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DOI: https://doi.org/10.1007/s10695-005-5288-5