Abstract
Antarctica is considered a thermally stable ecosystem; however, climate studies point to increases in water temperatures in this region. These thermal changes may affect the biological processes and promote metabolic changes in the adapted organisms that live in this region, rendering the animals more vulnerable to oxidative damage. This study assessed the effect of acclimation temperature on the levels of stress response markers in plasma, kidney, gill, liver, and brain tissues of Notothenia rossii subjected to gradual temperature changes of 0.5 °C/day until reaching temperatures of 2, 4, 6, and 8 °C. Under the effect of the 0.5 °C/day acclimation rate, gill tissue showed increased glutathione-S-transferase (GST) activity; kidney tissue showed increased H+-ATPase activity. In the liver, there was also an increase in GSH. In plasma, gradual decreases in the concentrations of total proteins and globulins were observed. These responses indicate a higher production of reactive oxygen species ROS, an imbalance in energy demand, and a lack in protein synthesis. Gradual increase in temperature may cause opposite responses to the thermal shock model in N. rossii.
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References
Abele D, Puntarulo S (2004) Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp Biochem Physiol A 138:405–415. https://doi.org/10.1016/j.cbpb.2004.05.013
Abele D, Burlango B, Viarengo A, Pörtner HO (1988) Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna. Comp Biochem Physiol B 120:425–435. https://doi.org/10.1016/S0305-0491(98)10028-7
Adamu KM, Kori-SIakpere O (2011) Effects of sublethal concentrations of tobacco (Nicotiana tobaccum) leaf dust on some biochemical parameters of hybrid catfish (Clarias gariepinus and Heterobranchus bidorsalis). Braz Arch Biol Technol 54:183–196. https://doi.org/10.1590/S1516-89132011000100023
Almroth BC, Asker N, Wassmur B, Rosengre M, Jutfele F, Gräns A, Sundell K, Axelsson M, Sturve J (2015) Warmer water temperature results in oxidative damage in an Antarctic fish, the bald notothen. J Exp Mar Biol Ecol 468:130–137. https://doi.org/10.1016/j.jembe.2015.02.018
Anderson M (2011) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Andreeva AM (2010) The role of structural organization of blood plasma proteins in the stabilization of water metabolism in bony fish (Teleostei). J Ichthyol 50:552–558. https://doi.org/10.1134/S0032945210070076
Ansaldo M, Luquet CM, Evelson PA, Polo JA, Llesuy S (2000) Antioxidant levels from different Antarctic fish caught around South Georgia Island and Shag Rocks. Polar Biol 23:160–165. https://doi.org/10.1007/s003000050022
Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525. https://doi.org/10.1093/icb/42.3.517
Beers JM, Jayasundara N (2015) Antarctic notothenioid fish: what are the future consequences of ‘losses’ and ‘gains’ acquired during long-term evolution at cold and stable temperatures? J Exp Biol 218:1834–1845. https://doi.org/10.1242/jeb.116129
Begg K, Pankhurst NW (2004) Endocrine and metabolic responses to stress in laboratory population of the tropical damshelfish Acanthochromis polyacanthus. J Fish Biol 64:133–145. https://doi.org/10.1111/j.1095-8649.2004.00290.x
Beutler E (1975) Red cell metabolism: a manual of biochemical methods. Grune & Stratton, New York, p 160
Bilyk KT, De Vries AL (2011) Heat tolerance and its plasticity in Antarctic fishes. Comp Biochem Physiol A 158:382–390. https://doi.org/10.1016/j.cbpa.2010.12.010
Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999
Breton S, Brown D (2000) New insights into the regulation of V-ATPase-dependent proton secretion. Am J Physiol Renal Physiol 292:1–10. https://doi.org/10.1152/ajprenal.00340.2006
Brodte E, Graeve M, Jacob U, Knust R, Pörtner HO (2008) Temperature-dependent lipid levels and components in polar and temperate eelpout (Zoarcidae). Fish Physiol Biochem 34:261–274. https://doi.org/10.1007/s10695-007-9185-y
Buckley BA, Place SP, Hofmann GE (2004) Regulation of heat shock genes in isolated hepatocytes froman Antarctic fish, Trematomus bernacchii. J Fish Biol 207:3649–3656. https://doi.org/10.1242/jeb.01219
Carlberg I, Mannervik B (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250:5475–5480. https://doi.org/10.1016/S0021-9258(19)41206-4
Cheng CH, Ye CX, Guo ZX, Wang AL (2017) Immune and physiological responses of pufferfish (Takifugu obscurus) under cold stress. Fish Shellfish Immunol 64:137–145. https://doi.org/10.1016/j.fsi.2017.03.003
Crouch RK, Gandy SC, Kinsey G (1981) The inhibition of islet superoxide dismutase by diabetogenic drugs. Diabetes 30:235–241. https://doi.org/10.2337/diab.30.3.235
De Vries AL, Cheng CHC (2005) Antifreeze proteins and organismal freezing avoidance in polar fishes. Fish Physiol 22:155–201. https://doi.org/10.1016/S1546-5098(04)22004-090
Do TD, Mai NT, Khoa TND, Abol-Munafi AB, Liew HJ, Kim CB, Wong LL (2019) Molecular characterization and gene expression of glutathione peroxidase 1 in Tor tambroides exposed to temperature stress. Evol Bioinform 15:1–8. https://doi.org/10.1177/116934319853580
Donatti L, Fanta E (2002) Influence of photoperiod on visual prey detection in the Antarctic fish Notothenia neglecta Nybelin. Antarct Sci 14:146–150. https://doi.org/10.1017/S0954102002000706
Duarte RM, Ferreira MS, Wood CM, Val AL (2013) Effect of low pH on Na+ regulation in two cichlid fish species of the Amazon. Comp Biochem Physiol A Mol Integr Physiol 166:441–448. https://doi.org/10.1016/j.cbpa.2013.07.022
Enzor LA, Place SP (2014) Is warmer better? Decreased oxidative damage in notothenioid fish after long-term acclimation to multiple stressors. J Exp Biol 217:3301–3310. https://doi.org/10.1242/jeb.108431
Federici G, Shaw BJ, Handy RD (2007) Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 84:415–430. https://doi.org/10.1016/j.aquatox.2007.07.009
Forgati M, Kandalski PK, Herrerias T, Zaleski T, Machado C, Souza MRDP, Donatti L (2017) Effects of heat stress on the renal and branchial carbohydrate metabolism and antioxidant system of Antarctic fish. J Comp Physiol B 187:1137–1154. https://doi.org/10.1007/s00360-017-1088-3
Gibbs A, Somero GN (1989) Pressure adaptations of Na+ /K+ -ATPase in gills of marine teleosts. J Exp Biol 143:475–492. https://doi.org/10.1242/jeb.143.1.475
Gieseg SP, Cuddihy S, Hill JV, Davison WA (2000) Comparison of plasma vitamin C and E levels in two Antarctic and two temperate water fish species. Comp Biochem Physiol B 125:371–378. https://doi.org/10.1016/S0305-0491(99)00186-8
Gonzalez-Cabrera PJ, Dowd F, Pedibhotla VK, Rosario R, Stanley-Samuelson D, Petzel D (1995) Enhanced hypo-osmoregulation induced by warm-acclimation in antarctic fish is mediated by increased gill and kidney Na+ /K+ -ATPase activities. J Exp Biol 198:2279–2291. https://doi.org/10.1242/jeb.198.11.2279
Guderley H, St-Pierre J (2002) Going with the flow or life in the fast lane: contrasting mitochondrial responses to thermal change. J Exp Biol 205:2237–2249. https://doi.org/10.1242/jeb.205.15.2237
Guillen AC, Borges ME, Herrerias T, Kandalski PK, Marins EA, Viana D, Souza MRDP, Daloski LOC, Donatti L (2019) Effect of gradual temperature increase on the carbohydrate energy metabolism responses of the Antarctic fish Notothenia rossii. Mar Environ Res 150:104779. https://doi.org/10.1016/j.marenvres.2019.104779
Guynn S, Dowd F, Petzel D (2002) Characterization of gill Na/K-ATPase activity and ouabain binding in Antarctic and New Zealand nototheniid fishes. Comp Biochem Physiol A Mol Integr Physiol 131:363–374. https://doi.org/10.1016/S1095-6433(01)00488-3
Halliwell B, Gutteridge J (2007) Free radicals in biology and medicine. Oxford University Press, Oxford
Harrower JR, Brown CH (1972) Blood lactic acid. A micromethod adapted to field collection of microliter samples. J Appl Physiol 32:224–228. https://doi.org/10.1152/jappl.1972.32.5.709
Heise K, Puntarulo S, Portner HO, Abele D (2003) Production of reactive oxygen species by isolated mitochondria of the Antarctic bivalve Laternula elliptica (King and Broderip) under heat stress. Comp Biochem Physiol C 134:79–90. https://doi.org/10.1016/s1532-0456(02)00212-0
Heise K, Estevez MS, Puntarulo S, Galleano M, Nikinmaa M, Portner HO, Abele D (2007) Effects of seasonal and latitudinal cold on oxidative stress parameters and activation of hypoxia inducible factor (HIF-1) in zoarcid fish. J Comp Physiol B 177:765–777. https://doi.org/10.1007/s00360-007-0173-4
Hofmann GE, Buckley BA, Airaksinen S, Keen JE, Somero GN (2000) Heatshock protein expression is absent in the Antarctic fish Trematomus bernacchii (family Nototheniidae). J Exp Biol 203:2331–2339. https://doi.org/10.1242/jeb.203.15.2331
Hudson HA, Brauer PR, Scofield MA, Petzel DH (2008) Effects of warm acclimation on serum osmolality, cortisol and hematocrit levels in the Antarctic fish, Trematomus Bernacchii. Polar Biol 31:991–997. https://doi.org/10.1007/s00300-008-0438-8
Huey RB, Stevenson RD (1979) Integrating thermal physiology and ecology of ectotherms: a Discussion of Approaches. Am Zool 19:357–366. https://doi.org/10.1093/icb/19.1.357
Jayasundara N, Healy TM, Somero GN (2013) Effects of temperature acclimation on cardiorespiratory performance of the Antarctic notothenioid Trematomus bernacchii. Polar Biol 36:1047–1057. https://doi.org/10.1007/s00300-013-1327-3
Jin Y, De Vries AL (2006) Antifreeze glycoprotein levels in Antarctic notothenioid fishes inhabiting different thermal environments and the effect of warm acclimation. Comp Biochem Physiol B 144:290–300. https://doi.org/10.1016/j.cbpb.2006.03.006
Johansen K, Pettersson K (1981) Gill O2 consumption in a teleost fish, Gadus Morhua. Respir Physiol 44:277–284. https://doi.org/10.1016/0034-5687(81)90023-2
Johnson TP, Bennett AF (1995) The thermal acclimation of burst escape performance in fish: an integrated study of molecular and cellular physiology and organismal performance. J Exp Biol 198:2165–2175. https://doi.org/10.1242/jeb.198.10.2165
Kandalski PK, Souza MRDP, Herrerias T, Machado C, Zaleski T, Forgati M, Guillen AC, Viana D, Moura M, Donatti L (2018) Effects of short-term thermal stress on the plasma biochemical profiles of two Antarctic nototheniid species. Rev Fish Biol Fish 28:925–940. https://doi.org/10.1007/s11160-018-9535-0
Keen JH, Habig WH, Jakoby WB (1976) Mechanism for several activities of the glutathione S transferases. J Biol Chem 251:6183–6188. https://doi.org/10.1016/S0021-9258(20)81842-0
Keller M, Sommer AM, Portner HO, Abele D (2004) Seasonality of energetic functioning and production of reactive oxygen species by lugworm (Arenicola marina) mitochondria exposed to acute temperature changes. J Exp Biol 207:2529–2538. https://doi.org/10.1242/jeb.01050
Klein RD, Borges VD, Rosa CE, Colares EP, Robaldo RB, Martinez PE, Bianchini A (2017) Effects of increasing temperature on antioxidant defense system and oxidative stress parameters in the Antarctic fish Notothenia coriiceps and Notothenia rossii. J Therm Biol 68:110–118. https://doi.org/10.1016/j.jtherbio.2017.02.016
Koakoski G, Oliveira TA, Rosa JGS, Fagundes M, Kreutz LC, Barcellos LJG (2012) Divergent time course of cortisol response to stress in fish of different ages. Physiol Behav 106:129–132. https://doi.org/10.1016/j.physbeh.2012.01.013
Kreiss CM, Michael K, Lucassen M, Jutfeelt F, Motyka R, Dupont S, Portner HO (2015) Ocean warming and acidification modulated energy budget and gill ion regulatory mechanisms in Atlantic cod (Gadus morhua). J Comp Physiol B 185:767–781. https://doi.org/10.1007/s00360-015-0923-7
Kultz D, Somero GN (1995) Osmotic and thermal effects on in situ ATPase activity in permeabilized gill epithelial cells of the fish Gillichthys mirabilis. J Exp Biol 198:1883–1894. https://doi.org/10.1242/jeb.198.9.1883
Laborde E (2010) Glutathione transferases as mediators of signaling pathways involved in cell proliferation and cell death. Cell Death Difer 17:1373–1380. https://doi.org/10.1038/cdd.2010.80
Levine RL, Williams JA, Stadtman EP, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357. https://doi.org/10.1016/S0076-6879(94)33040-9
Lowe CJ, Davison W (2005) Plasma osmolarity, glucose concentration and erythrocyte responses of two Antarctic nototheniid fishes to acute and chronic thermal change. J Fish Biol 67:752–766. https://doi.org/10.1111/j.0022-1112.2005.00775.x
Machado C, Zaleski T, Rodrigues E, Carvalho CDS, Cadena SMSC, Gozzi GJ, Krebsbach P, Rios FS’A, Donatti L (2014) Effect of temperature acclimation on the liver antioxidant defence system of the Antarctic nototheniids Notothenia coriiceps and Notothenia rossii. Comp Biochem Physiol B Biochem Mol Biol 172–173:21–28. https://doi.org/10.1016/j.cbpb.2014.02.003
Mommsen TP (1984) Metabolism of the fish gill. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol XB. Academic Press, Orlando, pp 203–237
Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268. https://doi.org/10.1023/A:1008924418720
Mueller I, Hoffman M, Dullen K, O’Brien K (2014) Moderate elevations in temperature do not increase oxidative stress in oxidative muscles of Antarctic notothenioid fishes. Polar Biol 37:311–320. https://doi.org/10.1007/s00300-013-1432-3
Nish T, Forgac M (2002) The vacuolar (H+)-ATPases natures´s most versatile proton pumps. Nat Rev Mol Cell Biol 3:94–103. https://doi.org/10.1038/nrm729
Pankhurst NW (2011) The endocrinology of stress in fish: an environmental perspective. Gen Comp Endocrinol 170:265–275. https://doi.org/10.1016/j.ygcen.2010.07.017
Peck LS (2002) Ecophysiology of Antarctic marine ectotherms: limits to life. Polar Biol 25:31–40. https://doi.org/10.1007/s003000100308
Peres H, Costas B, Perez-Jimenez A, Guerreiro I, Oliva-Teles A (2015) Reference values for selected hematological and serum biochemical parameters of Senegalese sole (Solea senegalensis Kaup, 1858) juveniles under intensive aquaculture conditions. J Appl Ichthyol 31:65–71. https://doi.org/10.1111/jai.12641
Perry SF, Laurent P (1993) Environmental effects on fish gill structure and function. In: Rankin JC, Jensen FB (eds) Fish Ecophysiology. Chapman; Hall, London, pp 231–264
Perry SF, Beyers ML, Johnson DA (2000) Cloning and molecular characterisation of the trout (Oncorhynchus mykiss) vacuolar H+- ATPase B subunit. J Exp Biol 203:459–470. https://doi.org/10.1242/jeb.203.3.459
Petzel D (2005) Drinking in Antarctic fishes. Polar Biol 28:763–768. https://doi.org/10.1007/s00300-005-0005-5
Place SP, Hofmann GE (2005) Constituve expression of a stress-inducible heat shock protein gene, hsp70, in phylogenetically distant Antartic fish. Polar Biol 28:261–267. https://doi.org/10.1007/s00300-004-0697-y
Podrabsky JE, Somero GN (2006) Inducible heat tolerance in Antarctic notothenioid fishes. Polar Biol 30:39–43. https://doi.org/10.1007/s00300-006-0157-y
Portner HO (2002) Physiological basis of temperature-dependent biogeography: trade-offs in muscle design and performance in polar ectotherms. J Exp Biol 205:2217–2230. https://doi.org/10.1242/jeb.205.15.2217
Portner HO, Peck MA (2010) Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. J Fish Biol 77:1745–1779. https://doi.org/10.1111/j.1095-8649.2010.02783x
R: Development Core Team (2013) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3–90051–07–0. R-Project.org
Rodrigues E Jr, Feijó-Oliveira M, Vani GS, Suda CNK, Carvalho CS, Donatti L, Lavrado HP, Rodrigues E (2013) Interaction of warm acclimation, low salinity, and trophic fluoride on plasmatic constituents of the Antarctic fish Notothenia rossii Richardson, 1844. Fish Physiol Biochem 39:1591–1601. https://doi.org/10.1007/s10695-013-9811-9
Rodrigues E Jr, Feijó-Oliveira M, Suda CNK, Vani GS, Donatti L, Rodrigues E, Lavrado HP (2015) Metabolic responses of the Antarctic fishes Notothenia rossii and Notothenia coriiceps to sewage pollution. Fish Physiol Biochem 41:1205–1220. https://doi.org/10.1007/s10695-015-0080-7
Saber TH (2011) Histological adaptation to thermal changes in gills of common carp fishes Cyprinus carpio L. Rafidain. J Sci 22:1–16. https://doi.org/10.33899/rjs.2011.32464
Sedilak J, Lindsay RHC (1968) Estimation of total, protein bound and nonprotein sulfhydryl groups in tissue with Ellmann’s reagent. Anal Biochem 25:192–205. https://doi.org/10.1016/0003-2697(68)90092-4
Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferases: implications for classifications of non-mammalian members of na ancient enzyme superfamily. Biochem J 360:1–16. https://doi.org/10.1042/0264-6021:3600001
Sidell BD (1998) Intracellular oxygen diffusion: the roles of myoglobin and lipid at cold body temperature. J Exp Biol 201:1118–1127. https://doi.org/10.1242/jeb.201.8.1119
Sidell BD, Driedzic R, Stowe B, Johnston A (1987) Biochemical correlations of power development and metabolic fuel preferenda in fish hearts. Physiol Zool 60:221–232. https://doi.org/10.1086/physzool.60.2.30158646
Sk UH, Bhattacharya S (2006) Prevention of cadmium induced lipid peroxidation, depletion of some antioxidative enzymes and glutathione by series of novel organoselenocyanates. Environ Toxicol Pharmacol 22:298–308. https://doi.org/10.1016/j.etap.2006.04.004
Somero GN, De Vries AL (1967) Temperature tolerance of some antarctic fishes. Science 156:257–258. https://doi.org/10.1126/science.156.3772.257
Souza MRDP, Herrerias T, Zaleski T, Forgati M, Kandalski PK, Machado C, Silva DT, Piechnik CA, Moura MO, Donati L (2018) Heat stress in the heart and muscle of the Antarctic fishes Notothenia rossii and Notothenia coriiceps: carbohydrate metabolism and antioxidant defence. Biochimie 146:43–55. https://doi.org/10.1016/j.biochi.2017.11.010
Stastna V (2010) Spatio-temporal changes in surface air temperature in the region of the northern Antarctic Peninsula and south Shetland islands during 1950–2003. Polar Sci 4:18–33. https://doi.org/10.1016/j.polar.2010.02.001
Strobel A, Bennecke S, Leo E, Mintenbeck K, Portner HO, Mark FC (2012) Metabolic shifts in the Antarctic fish Notothenia rossii in response to rising temperature and PCO2. Front Zool 9:28. https://doi.org/10.1186/1742-9994-9-28
Tapiero H, Tew KD (2003) The importance of glutathione in human disease. Biomed Pharmacother 57:145–155. https://doi.org/10.1016/s0753-3322(03)00043-x
Thorne MAS, Burns G, Fraser KPP, Hillyard G, Clark MS (2010) Transcription profiling of acute temperature stress in the Antarctic plunderfish Harpagifer antarcticus. Mar Genom 3:35–44. https://doi.org/10.1016/j.margen.2010.02.002
Thuesen EV, Mccullough KD, Childress JJ (2005) Metabolic enzyme activities in swimming muscle of medusae: is the scaling of glycolytic activity related to oxygen availability? J Mar Biol Assoc UK 85:603–611. https://doi.org/10.1017/S0025315405011537
Trefts E, Gannon M, Waseerman DH (2017) The liver. Curr Biol 27:1147–1151. https://doi.org/10.1016/j.cub.2017.09.019
Turner J, Colwell SR, Marshall GJ, Lachlan-Cope TA, Carleton AM, Jones PD, Lagun V, Reid PA, Iagovkina AS (2005) Antarctic climate change during the last 50 years. Int J Climatol 25:279–294. https://doi.org/10.1002/joc.1130
Turner J, Barrand NE, Bracegirdle TJ, Convey P, Hodgson DA, Jarvis M, Jenkins A, Marshall G, Meredith MP, Roscoe H, Shanklin (2014) Antarctic climate change and the environment: an update. Polar Record (Gr Brit) 50:237–259. https://doi.org/10.1017/S0032247413000296
Wendel A (1981) Glutathione peroxidase. Methods Enzymol 77:325–333. https://doi.org/10.1016/s0076-6879(81)77046-0
Wilson RS, Kuchel LJ, Franklin CE, Davison W (2002) Turning up the heat on subzero fish: Thermal dependence of sustained swimming in an Antarctic notothenioid. J Therm Biol 27:381–386. https://doi.org/10.1016/S0306-4565(02)00006-2
Acknowledgements
We are grateful to Mariana Forgati, Tânia Zaleski, and Thaylise C.S. Przepiura for their help in the experimental design during the Antarctic expedition XXXIII. We are grateful to the following organizations for their support: the Brazilian Ministry of Environment (MMA), the Ministry of Science, Technology and Innovation (MCTI), the National Council for the Development of Scientific and Technological Research (CNPq), the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES), and the Secretariat of the Commission for the Resources of the Sea (SeCIRM). The authors would like to extend special acknowledgments to Dr. Edith Susana Elisabeth Fanta (in memoriam) and Dr. Yocie Yoneshigue Valentin, for the help and support provided during the present study.
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The study was funded by CAPES, CNPq, and FAPERJ through projects PNPD (CAPES process Auxpe N. 2443/2011), research productivity granted to L. Donatti (CNPq Process N.305969/2012–9 and 304208/2016–6), and INCT-APA (CNPq Process N. 574018/2008–5 and FAPERJ E-26/170.023/2008).
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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by AC Guillen, PK Krebsbach, MRDP Souza, T Herrerias, L Donatti, and ME Borges. The first draft of the manuscript was written by AC Guillen and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Guillen, A.C., Borges, M.E., Herrerias, T. et al. Gradual increase of temperature trigger metabolic and oxidative responses in plasma and body tissues in the Antarctic fish Notothenia rossii. Fish Physiol Biochem 48, 337–354 (2022). https://doi.org/10.1007/s10695-021-01044-2
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DOI: https://doi.org/10.1007/s10695-021-01044-2