Abstract
The objective of the present study was to assess the effect of short-term (2–144 h) heat stress (8 °C) on energy production processes and antioxidant defense systems in the kidneys and gills of Notothenia rossii and Notothenia coriiceps. Heat stress affected energy metabolism and oxidative stress parameters in a time-, tissue-, and species-dependent manner, and gills were more sensitive than kidneys to heat stress. N. rossii kidneys were able to stabilize carbohydrate metabolism after 12 h of heat stress, whereas the glycogen levels in N. coriiceps kidneys fluctuated in response to varying glucose-6-phosphatase (G6Pase) levels. The gills of N. rossii were able to stabilize their energy demand and aerobic metabolism under heat stress, whereas in the gills of N. coriiceps, changes in carbohydrate metabolic pathways depended on the exposure time: initially, anaerobiosis was activated after 6 h; the energy demand, characterized by glycogen consumption, increased after 72 h, and aerobic metabolism was activated within 144 h. With regard to the antioxidant defenses of the N. rossii kidney, it was found that levels of antioxidant enzymes were reduced during the first hours of heat stress, contributing to increased lipid peroxidation, whereas N. coriiceps kidneys did not show signs of oxidative damage. The gills of N. rossii exhibited more pronounced oxidative damage in response to heat stress than those of N. coriiceps despite the presence of increasing levels of antioxidants, likely due to tissue hypoxia.
Similar content being viewed by others
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. doi:10.1016/j.cbpb.2004.05.013
Almroth BC, Asker N, Wassmur B, Rosengren M, Jutfelt L, 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. doi:10.1016/j.jembe.2015.02.018
Bagnyukova TV, Storey KB, Lushchak VI (2003) Induction of oxidative stress in Rana ridibunda during recovery from winter hibernation. J Therm Biol 28(1):21–28. doi:10.1016/S0306-4565(02)00031-1
Baldwin J, Elias JP, Wells RMG, Donovan DA (2007) Energy metabolism in the tropical abalone, Haliotis asinina Linné: comparisons with temperate abalone species. J Exp Mar Biol Ecol 342:213–225. doi:10.1016/j.jembe.2006.09.005
Barrera-Oro ER (2002) Review: the role of fish in the Antarctic marine food web: differences between inshore and offshore waters in the southern Scotia Arc and west Antarctic Peninsula. Antartct Sci 14:293–309
Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42(3):517–525. doi:10.1093/icb/42.3.517
Beutler E (1975) Red cell metabolism: a manual of biochemical and methods. Grune & Stratton, New York
Bidinotto PM, Souza RHS, Moraes G (1997) Hepatic glycogen in eight tropical freshwater teleost fish: Procedure for field determinations of microsamples. B Téc CEPTA 0:53–60
Bilyk KT, DeVries AL (2011) Heat tolerance and its plasticity in Antarctic fishes. Comp Biochem Physiol A 158:382–390. doi:10.1016/j.cbpa.2010.12.010
Blasco J, Gutiérrez J, Fernández J, Planas J (1988) The effect of temperature on immunoreactive glucagon plasma level in carp Cyprinus carpio. Rev Esp Fisiol 44:157–162
Boyce SJ, Clarke A (1997) Effect of body size and ration on specific dynamic action in the Antarctic plunderfish,Harpagifer antarcticusNybelin 1947. Physiol Zool 70(6):679–690.
Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of rotein-dye binding. Anal Biochem 72:248–254
Burchett MS (1983) Food, feeding and behavior of Notothenia rossii nearshore at South Georgia. Bull Br Antarct Surv 61:45–51
Campbell HA, Fraser KPP, Bishop CM, Peck LS, Egginton S (2008) Hibernation in an Antarctic fish: on ice for winter. PLoS ONE 3(3):e1743. doi:10.1371/journal.pone.0001743
Carlberg I, Mannervik B (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250:5475–5480
Chien LT, Hwang DF (2001) Effects of thermal stress and vitamin C on lipid peroxidation and fatty acid composition in the liver of thornfish Terapon jarbua. Comp Biochem Physiol B 128:91–97. doi:10.1016/S1096-4959(00)00299-2
Childress JJ, Somero GN (1979) Depth-related enzymic activities in muscle, brain and heart of deep-living pelagic marine teleosts. Mar Biol 52:273–283. doi:10.1007/BF00398141
Ciardello M, Camardella L, di Prisco G (1995) Glucose-6-phosphate dehydrogenase from the blood cells of two Antarctic teleosts: correlation with cold adaptation. Biochim Biophys Acta 1250:76–82. doi:10.1016/0167-4838(95)00046-W
Corbisier TN, Petti MAV, Skowronski RSP, Brito TAS (2004) Trophic relationships in the nearshore zone of Martel Inlet (King George Island, Antarctica): d13C stableisotope analysis. Polar Biol 27(2):75–82. doi:10.1007/s00300-003-0567-z
Crouch RK, Gandy SC, Kinsey G (1981) The inhibition of islet superoxide dismutase by diabetogenic drugs. Diabetes 30:235–241. doi:10.2337/diab.30.3.235
Das TA, Pal K, Chakraborty SK, Manush SM, Chatterjee N, Mukherjee SC (2004) Thermal tolerance and oxygen consumption of Indian Major Carps acclimated to four different temperatures. J Therm Biol 29:157–163. doi:10.1016/j.jtherbio.2004.02.001
Donatti L, Fanta E (2002) Influence of photoperiod on visual prey detection in the Antarctic fish Notothenia neglecta Nybelin. Antarct Sci 14(2):146–150
Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350–358. doi:10.1021/ac60111a017
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. doi:10.1242/jeb.108431
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 85:97–177. doi:10.1152/physrev.00050.2003
Fathi AR, Krautheim A, Lucke S, Becker K, Steinfelde RHJ (2002) Nonradioactive technique to measure protein phosphatase 2A-like activity and its inhibition by drugs in cell extracts. Anal Biochem 310:208–214. doi:10.1016/S0003-2697(02)00377-9
Gieseg SP; Cuddihy S; Hill JV; Davison W (2000) A comparison of plasma vitamin C and E levels in two Antarctic and two temperate water fish species. Comp Biochem Physiol Part B 125:371–378
Girotti A (1998) Lipid hydroperoxide generation, turnover, and effector action in biological systems. J Lipid Res 39:1529–1642
Grim JM, Simonik EA, Semones MC, Kuhn DE, Crockett EL (2013) The glutathione-dependent system of antioxidant defense is not modulated by temperature acclimation in muscle tissues from striped bass, Morone saxatilis. Comp Biochem Physiol A 164(2):383–390. doi:10.1016/j.cbpa.2012.11.018
Halliwell B, JMC Gutteridge (2007) Free radicals in biology and medicine. 4. Clarendon, Oxford
Harrower JR, Brown CH (1972) Blood lactic acid. A micromethod adaptes to field collection of microliter samples. J Appl Physiol 32:224–228
Heise K, Estevez MS, Puntarulo S, Galeano M, Nikinmaa M, Pörtner 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. doi:10.1007/s00360-007-0173-4
Hochachka PW, Lutz PL (2001) Mechanism, origin and evolution of anoxia tolerance in animals. Comp Biochem Physiol B 130:435–459. doi:10.1016/S1096-4959(01)00408-0
Hochachka PW, Somero GN (2002) Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford University Press, New York
Hunt BM, Hoefling K, Cheng CHC (2003) Annual warming episodes in seawater temperatures in McMurdo Sound in relationship to endogenous ice in notothenioid fish. Antarct Sci 15(3):333–338. doi:10.1017/S0954102003001342
Hwang PP, Lee TH, Lin LY (2011) Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. Am J Physiol Regul Integr Comp Physiol 301:R28–R47. doi:10.1152/ajpregu.00047.2011
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. doi:10.1007/s00300-013-1327-3
Johnston IA, Battram J (1993) Feeding energetics and metabolism in demersal fish species from Antarctic, temperate and tropical environments. Mar Biol 115:7–14
Johnston IA, Dunn J (1987) Temperature acclimation and metabolism in ectotherms with particular reference to teleost fish. Symp Soc Exp Biol 41:67–93
Keen JH, Habig WH, Jakoby WB (1976) Mechanism for several activities of the glutathione S transferases. J Biol Chem 251:6183–6188
King JC, Harangozo SA (1998) Climate change in the western Antarctic Peninsula since 1945: observations and possible causes. Ann Glaciol 27:571–575. doi:10.3198/1998AoG27-1-571-575
Knox GA (1994) The biology of the Southern Ocean. Cambridge University Press, Cambridge, p 444
Lannig G, Storch D, Pörtner HO (2005) Aerobic mitochondrial capacities in Antarctic and temperate eelpout (Zoarcidae) subjected to warm versus cold acclimation. Polar Biol 28:575–584. doi:10.1007/s00300-005-0730-9
Leggatt RA, Brauner CJ, Schulte PM, Iwama GK (2007) Effects of acclimation and incubation temperature on the glutathione antioxidant system in killifish and RTH 149 cells. Comp Biochem Physiol A 146:322–328. doi:10.1016/j.cbpa.2006.10.033 doi
Levine RL, Williams JA, Stadtman EP, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357. doi:10.1016/S0076-6879(94)33040-9
Lu GD (1939) The metabolism of piruvic acid in normal and vitamin B-deficient state. I. A rapid specific and sensitive method for the estimation of blood piruvate. Biochem J 33:249–254
Lushchak VI, Bagnyukova TV (2006a) Temperature increase results in oxidative stress in goldfish tissues. 1. Indices of oxidative stress. Comp Biochem Physiol C 143:30–35. doi:10.1016/j.cbpc.2005.11.017
Lushchak VI, Bagnyukova TV (2006b) Temperature increase results in oxidative stress in goldfish tissues: 2. Antioxidant and associated enzymes. Comp Biochem Physiol C 143:36–41. doi:10.1016/j.cbpc.2005.11.018
Lushchak VI, Lushchak LP, Mota AA, Hermes-Lima M (2001) Oxidative stress and antioxidant defenses in goldfish Carassius auratus during anoxia and reoxygenation. Am J Physiol Regulatory Integrative Comp Physiol 280(1):R100–R107
Lushchak VI, Bagnyukova TV, Lushchak OV, Storey JM, Storey KB (2005) Hypoxia and recovery perturb free radical processes and antioxidant potential in common carp (Cyprinus carpio) tissues. Int J Biochem Cell Biol 37:1319–1330. doi:10.1016/j.biocel.2005.01.006
Machado C, Zaleski T, Rodrigues E, Carvalho CDS, Cadena SMSC, Gozzi GJ, Krebsbach P, Rios FSA, 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 172–173:21–28. doi:10.1016/j.cbpb.2014.02.003
Madeira D, Narciso L, Cabral HN, Vinagre C, Diniz MS (2013) Influence of temperature in thermal and oxidative stress responses in estuarine fish. Comp Biochem Physiol A 166:237–243. doi:10.1016/j.cbpa.2013.06.008
Mark FC, Bock C, Pörtner HO (2002) Oxygen-limited thermal tolerance in Antarctic fish investigated by MRI and 31P-MRS. Am J Physiol Regul Integr Comp Physiol 283:R1254–R1262. doi:10.1152/ajpregu.00167.2002
Mark FC, Lucassen M, Pörtner HO (2006) Thermal sensitivity of uncoupling protein expression in polar and temperate fish. Comp Biochem Physiol D 1:365–374. doi:10.1016/j.cbd.2006.08.004
Méton I, Caseras A, Fernández F, Baanante IV (2004) Molecular cloning of hepatic glucose-6-phosphatase catalytic subunit from gilthead sea bream (Sparus aurata): response of its mRNA levels and glucokinase expression to refeeding and diet composition. Comp Biochem Physiol B 138:145–153
Mintenbeck K, Barrera-Oro ER, Brey T, Jacob U, Knust R, Mark FC, Moreira E, Strobel A, Arntz WE (2012) Impact of climate change on fishes in complex Antarctic ecosystems. Adv Ecol Res 46:351–426. doi:10.1016/B978-0-12-396992-7.00006-X
Mueller IA, Devor DP, Grim JM, Beers JM, Crockett EL, O’Brien KM (2012) Exposure to critical thermal maxima increases oxidative stress in hearts of whitebut not red-blooded Antarctic notothenioid fishes. J Exp Biol 215(20):3655–3664. doi:10.1242/jeb.071811
Navarro I, Rojas P, Capilla E, Albalat A, Castillo J, Montserrat N, Codina M, Gutiérrez J (2002) Insights into insulin and glucagon responses in fish. Fish Physiol Biochem 27:205–216. doi:10.1023/B:FISH.0000032726.78074.04
Near TJ, Pesavento JJ, Cheng CHC (2004) Phylogenetic investigations of Antarctic notothenioid fishes (Perciformes: Notothenioidei) using complete gene sequences of the mitochondrial encoded 16 S rRNA. Mol Phylogenet Evol 32:881–891. 10.1016/j.ympev.2004.01.002
O’Connor EA, Pottinger TG, Sneddon LU (2011) The effects of acute and chronic hypoxia on cortisol, glucose and lactate concentrations in different populations of three-spined stickleback. Fish Physiol Biochem 37:461–469. doi:10.1007/s10695-010-9447-y
Oliva M, Vicente JJ, Gravato C, Guilhermino L, Galindo-Riaňo MD (2012) Oxidative stress biomarkers in Senegal sole, Solea senegalensis, to assess the impact of heavy metal pollution in a Huelva estuary (SW Spain): seasonal and spatial variation. Ecotoxicol Environ Saf 75:151–162. doi:10.1016/j.ecoenv.2011.08.017
Omlin T, Weber JM (2010) Hypoxia stimulates lactate disposal in rainbow trout. J Exp Biol 213:3802–3809. doi:10.1242/jeb.048512
Podrabsky JE, Somero GN (2006) Inducible heat tolerance in Antarctic notothenioid fishes. Polar Biol 30:39–43. doi:10.1007/s00300-006-0157-y
Polakof S, Arjona FJ, Sangiao-Alvarellos S, Martín del Río MP, Mancera JM, Soengas JL (2006) Food deprivation alters osmoregulatory and metabolic responses to salinity acclimation in gilthead sea bream Sparus auratus. J Comp Physiol B 176:441–452
Polakof S, Míguez JM, Soengas JL (2007) Daily changes in parameters of energy metabolism in liver, white muscle, and gills of rainbow trout: dependence on feeding. Comp Biochem Physiol 147A:363–374
Pörtner HO (2002) Climate change and temperature dependent biogeography: systemic to molecular hierarchies of thermal tolerance in animals. Comp Biochem Physiol A 132:739–761. doi:10.1007/s001140100216
Pörtner HO (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213:881–893. doi:10.1242/jeb.037523
Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692. doi:10.1126/science.1163156
Pörtner HO, Mark FC, Bock C (2004) Oxygen limited thermal tolerance in fish? Answers obtained by nuclear magnetic resonance techniques. Respir Physiol Neurobiol 141:243–260. doi:10.1016/j.resp.2004.03.011
Pörtner HO, Langenbuch M, Michaelidis B (2005) Synergistic effects of temperature extremes, hypoxia and increases in CO2 on marine animals: from Earth history to global change. J Geophys Res 110:C09S10. doi:10.1029/2004JC002561
Qiu J (2012) Climate change. winds of change. Science 338:879–881. doi:10.1126/science.338.6109.879
Raga G, Pichler HA, Zaleski T, Silva FBV, Machado C, Rodrigues E, Kawall HG, Rios FS, Donatti L (2015) Ecological and physiological aspects of the antarctic fishes Notothenia rossii and Notothenia coriiceps in Admiralty Bay, Antarctic Peninsula. Environ Biol Fish 98(3):775–788. doi:10.1007/s10641-014-0311-2
Richardson MG (1844) The dietary composition of some Antarctic fish. Br Antarct Surv Bull 41(42):113–120
Robinson E (2008) Antarctic fish: thermal specialists or adaptable generalists? PhD Thesis, University of Canterbury
Robinson E, Davison W (2008) The Antarctic notothenioid fish Pagothenia borchgrevinki is thermally flexible: acclimation changes oxygen consumption. Polar Biol 31:317–326. doi:10.1007/s00300-007-0361-4
Robinson E, Egginton S, Davison W (2011) Warm-induced bradycardia and cold-induced tachycardia: mechanisms of cardiac and ventilatory control in a warm-acclimated Antarctic fish. Polar Biol 34:371. doi:10.1007/s00300-010-0891-z
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. doi: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(5):1205–1220. doi:10.1007/s10695-015-0080-7
Rodrigues E, Suda CNK, Rodrigues E Jr, de Oliveira MF, dos Santos Carvalho C, Vani GS (2011) Antarctic fish metabolic responses as potential biomarkers of environmental impact. Oecol Australis 15(1):124–149
Ryan SN (1995) The effect of chronic heat stress on cortisol levels in the Antarctic fish Pagothenia borchgrevinki. Experientia 51:768–774. doi:10.1007/BF01922428
Saborowski IR, Buchholz F (2002) Metabolic properties of Northern krill, Meganyctiphanes norvegica, from different climatic zones. II. Enzyme characteristics and activities. Mar Biol 140:557–565. doi:10.1007/s00227-001-0734-0
Sangiao Alvarellos S, Guzmán JM, Láiz-Carrión R, Míguez JM, Martín Del Río MP, Mancera JM, Soengas JL (2005) Interactive effects of the high stocking density and food deprivation on carbohydrate metabolismo in several tissues of gilthead sea bream Sparus auratus. J Exp Zool 303:761–775
Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56. doi:10.1007/s00360-008-0283-7
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
Sidell BD (1998) Intracellular oxygen diffusion: the roles of myoglobin and lipid at cold body temperature. J Exp Biol 201:1118–1127
Silveira US, Logato PVR, Pontes EC (2009) Fatores estressantes em peixes. Revista Eletrônica Nutritime 6(4):1001–1017
Strobel A, Benneck S, Leo E, Mintenbeck K, Pörtner HO, Mark FC (2012) Metabolic shifts in the Antarctic fish Notothenia rossii in response to rising temperature and PCO2. Front Zool 9:28. doi:10.1186/1742-9994-9-28
Strobel A, Leo E, Pörtner HO, Mark FC (2013) Elevated temperature and PCO2 shift metabolic pathways in differentially oxidative tissues of Notothenia rossii. Comp Biochem Physiol B 166:48–57. doi:10.1016/j.cbpb.2013.06.006
Suarez RK, Mallet MD, Daxboeck C, Hochachka PW (1986) Enzymes of energy metabolism and gluconeogenesis in the Pacific blue marlin, Makaira nigricans. Can J Zool 64:694–697. doi:10.1139/z86-102
Subudhi AW, Davis, SL, Kipp RW, Askew EW (2001) Antioxidant status and oxidative stress in elite alpine ski racers. Int J Sport Nutr Exerc Metab 11(1):32–41
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 Ass U K 85:603–611. doi:10.1017/S0025315405011537
Tseng YC, Lee JR, Chang JCH, Kuo CH, Lee SJ, Hwang PP (2008) Regulation of lactate dehydrogenase in tilapia (Oreochromis mossambicus) gills during acclimation to salinity challenge. Zool Stud 47:473–480
Van Dijk PLM, Tesch C, Hardewig I, Pörtner HO (1999) Physiological disturbances at critically high temperatures: a comparison between stenothermal Antarctic and eurythermal temperate eelpouts (Zoarcidae). J Exp Biol 202:3611–3621
Vanella FA, Boy CC, Lattuca ME, Calvo J (2010) Temperature influence on post-prandial metabolic rate of sub-Antartic teleost fish. Comp Biochem Physiol A Mol Integr Physiol 156(2):247–254. doi:10.1016/j.cbpa.2010.02.006
Vinagre C, Madeira D, Narciso L, Cabral HN, Diniz M (2012) Effect of temperature on oxidative stress in fish: Lipid peroxidation and catalase activity in the muscle of juvenile seabass, Dicentrarchus labrax. Ecol Indic 23:274–279. doi:10.1016/j.ecolind.2012.04.009
Wendel A (1981) Glutathione peroxidase. Method Enzymol 77:325–333
Windisch HS, Frickenhaus S, John E, Knust R, Pörtner HO (2014) Stress response or beneficial temperature acclimation: transcriptomic signatures in Antarctic fish (Pachycara brachycephalum). Mol Ecol 23:3469–3482. doi:10.1111/mec.12822
Woody CA, Nelson J, Ramstad K (2002) Clove oil as an anaesthetic for adult sockeye salmon: field trials. J Fish Biol 60(340–347):2002. doi:10.1111/j.1095-8649.2002.tb00284.x
Acknowledgements
We are grateful to the following for their support: the Brazilian Ministry of the 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 Inter-Ministerial Commission for the Resources of the Sea (SeCIRM). The authors would like to thank Dr. Edith Susana Elisabeth Fanta (in memoriam) and Dr. Yocie Yoneshigue Valentin, coordinator of the National Institute of Antarctic Science and Technology of Environmental Research (INCT-APA), for providing help and encouragement during the performance of the present work. This study was supported by CAPES and CNPq through the projects CAPES/PNPD 2443/2011, CNPq 52.0125/2008-8, 30.5562/2009-6, 30.5969/2012-9, and INCT-APA (CNPq 574.018/2008-5, FAPERJ E-26/170.023/2008).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by I.D. Hume.
Rights and permissions
About this article
Cite this article
Forgati, M., Kandalski, P.K., Herrerias, T. et al. Effects of heat stress on the renal and branchial carbohydrate metabolism and antioxidant system of Antarctic fish. J Comp Physiol B 187, 1137–1154 (2017). https://doi.org/10.1007/s00360-017-1088-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-017-1088-3