Reviews in Fish Biology and Fisheries

, Volume 28, Issue 4, pp 925–940 | Cite as

Effects of short-term thermal stress on the plasma biochemical profiles of two Antarctic nototheniid species

  • Priscila Krebsbach Kandalski
  • Maria Rosa Dmengeon Pedreiro de Souza
  • Tatiana Herrerias
  • Cintia Machado
  • Tania Zaleski
  • Mariana Forgati
  • Angela Carolina Guillen
  • Douglas Viana
  • Maurício Osvaldo Moura
  • Lucélia DonattiEmail author
Research Paper


Thermal elevation records in the Austral Ocean have raised questions about the physiological impacts on Antarctic organisms which have evolved under cold and stable water temperatures. Some notothenioid fishes exhibit species-specific responses to elevated temperature, yet the mechanisms involved in restoring homeostasis are unclear. Our study focused on the physiological effects of short-term (2–144 h) exposure to water temperatures of 8 °C on the plasma biochemical profiles of Notothenia coriiceps and Notothenia rossii, species that are abundant in Admiralty Bay, King George Island, Antarctic Peninsula, a region where increasing temperatures have been detected. Despite being phylogenetically similar, these species responded differently to thermal stress. N. rossii showed no changes in cortisol levels, and transient hyperglycemia was likely triggered by elevated catecholamine levels; conversely, metabolic and antioxidant defense parameters were unaffected. Increased gill Na+/K+-ATPase activity was observed only in N. rossii after 24 h at 8 °C, which assists in maintaining ionic homeostasis. In N. coriiceps, cortisol accurately indicated thermal stress. Increased cortisol levels in N. coriiceps additionally resulted in transient secondary responses such as hyperglycemia and hyperlactemia, as well as reduced levels of total protein, globulins and triglycerides. Unlike in N. rossii, catalase activity in N. coriiceps was modulated at 8 °C, and this parameter is thus considered a good biomarker of thermal stress. Results suggest that N. coriiceps is more sensitive to thermal stress than is N. rossii and that the former is a potential bioindicator for Admiralty Bay.


Admiralty bay Antarctic fishes Biochemical bioindicators Metabolism Temperature 



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); the Secretariat of the Inter-Ministerial Commission for the Resources of the Sea (SeCIRM); and the Ethics Committee on Animal Experimentation of the Federal University of Paraná (process numbers, 496/2010 and 840/2014). 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 execution 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). We would like to thank the editor and reviewer for providing valuable comments and suggestions.

Compliance with ethical standards

This study was approved by the Ethics Committee on Animal Experimentation of the Federal University of Paraná (UFPR) under applications number 496/2010 and 840/2014.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. 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 Mol Integr Physiol 138:405–415. CrossRefPubMedGoogle Scholar
  2. 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). Brazilian Arch Biol Technol 54:183–196. CrossRefGoogle Scholar
  3. Akhtar MS, Pal AK, Sahu NP et al (2013) Thermal tolerance, oxygen consumption and haemato-biochemical variables of Tor putitora juveniles acclimated to five temperatures. Fish Physiol Biochem 39:1387–1398. CrossRefPubMedGoogle Scholar
  4. Almeida JR, Gravato C, Guilhermino L (2015) Effects of temperature in juvenile seabass (Dicentrarchus labrax L.) biomarker responses and behaviour: implications for environmental monitoring. Estuar Coast 38(1):45–55CrossRefGoogle Scholar
  5. 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. CrossRefGoogle Scholar
  6. Arigony-Neto J, Simões JC, Bremer UF (2004) Implementation of the Admiralty Bay geographic information system, King George Island, Antarctica. Pesqui Antárt Bras 4:187–190Google Scholar
  7. Baldissera MD, Souza CF, Júnior GB, Verdi CM, Moreira KLS, Da Rocha MIUM, Da Veiga ML, Santos RCV, Vizzotto BS, Baldisserotto B (2017) Aeromonas caviae alters the cytosolic and mitochondrial creatine kinase activities in experimentally infected silver catfish: impairment on renal bioenergetics. Microb Path 110:439–443CrossRefGoogle Scholar
  8. Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525. CrossRefPubMedGoogle Scholar
  9. Beers JM, Sidell BD (2011) Thermal tolerance of Antarctic notothenioid fishes correlates with level of circulating hemoglobin. Physiol Biochem Zool 84:353–362. CrossRefPubMedGoogle Scholar
  10. Beutler E (1975) Red cell metabolism: a manual of biochemical methods. Grune & Stratton, New York, p 160Google Scholar
  11. Booth DJ, Bond N, Macreadie P (2011) Detecting range shifts among Australian fishes in response to climate change. Mar Freshw Res 62:1027–1042CrossRefGoogle Scholar
  12. Braun M, Simões JC, Vogt S, Bremer UF, Blindow N, Pfender M, Saurer H, Aquino FE, Ferron FA (2001) An improved topographic database for King George Island: compilation, application and outlook. Antarct Sci 13:41–52CrossRefGoogle Scholar
  13. Carney Almroth B, Asker N, Wassmur B et al (2015) Warmer water temperature results in oxidative damage in an antarctic fish, the bald notothen. J Exp Mar Bio Ecol 468:130–137. CrossRefGoogle Scholar
  14. Chen Z, Cheng CH, Zhang J, Cao L, Chen L, Zhou L, Jin Y, Ye H, Deng C, Dai Z, Xu Q, Hu P, Sun S, Shen Y, Chen L (2008) Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish. Proc Natl Acad Sci 105:12944–12949CrossRefGoogle Scholar
  15. 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. CrossRefPubMedGoogle Scholar
  16. Clarke A, Murphy EJ, Meredith MP, King JC, Peck LS, Barnes DKA, Smith RC (2007) Climate change and the marine ecosystem of the western Antarctic Peninsula. Philos Trans R Soc B 362:149–166CrossRefGoogle Scholar
  17. Cook AJ, Holland PR, Meredith MP et al (2016) Ocean forcing of glacier retreat in the western Antarctic Peninsula. Science 353:283–286. CrossRefPubMedGoogle Scholar
  18. Cowan JA (1995) Introduction to the biological chemistry of magnesium ion. In: Cowan JA (ed) The biological chemistry of magnesium. VCH Publishers, New York, pp 1–23Google Scholar
  19. Crouch RK, Gandy SC, Kinsey G (1981) The inhibition of islet superoxide dismutase by diabetogenic drugs. Diabetes 30:235–241CrossRefGoogle Scholar
  20. Davis KB (2004) Temperature affects physiological stress responses to acute confinement in sunshine bass (Morone chrysops × Morone saxatilis). Comp Biochem Physiol A Mol Integr Physiol 139:433–440CrossRefGoogle Scholar
  21. Devor DP, Kuhn DE, O’Brien KM, Crockett EL (2016) Hyperoxia does not extend critical thermal maxima (CT max) in white- or red-blooded Antarctic notothenioid fishes. Physiol Biochem Zool 89:1–9. CrossRefPubMedGoogle Scholar
  22. Di Marco P, Priori A, Finoia MG, Massari A, Mandich A, Marino (2008) Physiological responses of European sea bass Dicentrarchus labrax to different stocking densities and acute stress challenge. Aquaculture 275:319–328CrossRefGoogle Scholar
  23. Donatti L, Fanta E (2002) Influence of photoperiod on visual prey detection in the Antarctic fish Notothenia neglecta. Antarct Sci 14:146–150. CrossRefGoogle Scholar
  24. Dunn JF, Johnston IA (1986) Metabolic constraints on burst-swimming in the Antartic teleost Nothothenia neglecta. Mar Biol 91:433–440CrossRefGoogle Scholar
  25. Eastman JT (1993) Antarctic fish biology: evolution in a unique environment. Academic Press, San DiegoGoogle Scholar
  26. Egginton S (1997) A comparison of the response to induced exercise in red- and white-blooded Antarctic fishes. J Comp Physiol B 167:129–134. CrossRefGoogle Scholar
  27. Egginton S, Campbell HA (2016) Cardiorespiratory responses in an Antarctic fish suggest limited capacity for thermal acclimation. J Exp Biol 219:1283–1286. CrossRefPubMedGoogle Scholar
  28. Endres DB, Rude RK (1999) Mineral and bone metabolism. In: Burtis CA, Ashwwod ER (eds) Tietz textbook of clinical chemistry, 3rd edn. Saunders, Philadelphia, pp 1395–1457Google Scholar
  29. 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. CrossRefPubMedGoogle Scholar
  30. Enzor LA, Hunter EM, Place SP (2017) The effects of elevated temperature and ocean acidification on the metabolic pathways of notothenioid fish. Conserv Physiol. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Faggio C, Piccione G, Marafioti S, Arfuso F, Fortino G, Fazio F (2014) Metabolic response to monthly variations of Sparus aurata reared in Mediterranean on-shore tanks. Turk J Fish Aquat Sci 14:567–574. CrossRefGoogle Scholar
  32. Forgati M, Kandalski PK, Herrerias T et al (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. CrossRefPubMedGoogle Scholar
  33. Forster ME, Davison W, Axelsson M, Sundin L, Franklin CE, Gieseg S (1998) Catecholamine release in heat-stressed Antarctic fish causes proton extrusion by the red cells. J Comp Physiol B 168:345–352CrossRefGoogle Scholar
  34. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage Publications, CaliforniaGoogle Scholar
  35. Gamperl AK, Vijayan MM, Boutilier RG (1994) Experimental control of stress hormone levels in fishes: techniques and applications. Rev Fish Biol Fish 4:215–255. CrossRefGoogle Scholar
  36. Ghelichpour M, Mirghaed AT, Mirzargar SS, Joshaghani H, Mousavi HE (2017) Plasma proteins, hepatic enzymes, thyroid hormones and liver histopathology of Cyprinus carpio (Linnaeus, 1758) exposed to an oxadiazin pesticide, indoxacarb. Aquacult Res 48:5666–5676CrossRefGoogle Scholar
  37. Gibbs A, Somero GN (1989) Pressure adaptations of Na+/K+-ATPase in gills of marine teleosts. J Exp Biol 143:475–492PubMedGoogle Scholar
  38. Goddard PB, Dufour CO, Yin J, Griffies SM, Winton M (2017) CO2-induced ocean warming of the Antarctic continental shelf in an eddying global climate model. J Geophys Res Ocean 122:8079–8101. CrossRefGoogle Scholar
  39. Gonzalez-Cabrera PJ, Dowd F, Pedibhotla VK et al (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 198:2279–2291PubMedGoogle Scholar
  40. 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. CrossRefPubMedGoogle Scholar
  41. Hagen W, Kattner G, Friedrich C (2000) The lipid compositions of high-Antarctic notothenioid fish species with different life strategies. Polar Biol 23:785–791. CrossRefGoogle Scholar
  42. Harrower JR, Brown CH (1972) Blood lactic acid. A micromethod adaptes to field collection of microliter samples. J Appl Physiol 32:224–228CrossRefGoogle Scholar
  43. Heise K, Abele D (2008) Response of blood parameters of the Antarctic fish Notothenia coriiceps (Richardson, 1844) to warming and hypoxia. In: Wiencke C, Ferreyra G, Abele D, Marenssi S (eds) The Potter Cove coastal ecosystem, Antarctica. Synopsis of research performed 1999–2006 at the Dallmann LAboratory and Jubany Station. Berichte zur Polarforschu, King George Island (Isla 25 de Mayo)Google Scholar
  44. Hoseini SM, Hedayati A, Ghelichpour M (2014) Plasma metabolites, ions and thyroid hormones levels, and hepatic enzymes [U + 05F3] activity in Caspian roach (Rutilus rutilus caspicus) exposed to waterborne manganese. Ecotoxicol Environ Saf 107:84–89. CrossRefPubMedGoogle Scholar
  45. 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. CrossRefGoogle Scholar
  46. Hwang PP, Lee TH (2007) New insights into fish ion regulation and mitochondrion-rich cells. Comp Biochem Physiol A Mol Integr Physiol 148:479–497. CrossRefPubMedGoogle Scholar
  47. Islam Z, Hayashi N, Yamamoto Y, DOI H, Romero MF, Hirose S, Kato A (2013) Identification and proximal tubular localization of the Mg2+ transporter, Slc41a1, in a seawater fish. Am J Physiol Regul Integr Comp Physiol 305:R385–R396CrossRefGoogle Scholar
  48. 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. CrossRefGoogle Scholar
  49. Johnston IA, Calvo J, Guderley H, Fernandez D, Palmer L (1998) Latitudinal variation in the abundance and oxidative capacities of muscle mitochondria in perciform fishes. J Exp Biol 201:1–12PubMedGoogle Scholar
  50. Klein RD, Borges VD, Rosa CE et al (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. CrossRefPubMedGoogle Scholar
  51. Kulesz J (1999) Ichthyofauna of lagoons of the Admiralty Bay (King George Island, Antarctica) in 1997. Pol Arch Hydrobiol 46:173–184Google Scholar
  52. Kültz D, Somero G (1995) Osmotic and thermal effects on in situ ATPase activity in permeabilized gill epithelial cells of the fish Gillichthys mirabilis. J Exp Biol 198:1883–1894Google Scholar
  53. 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. CrossRefGoogle Scholar
  54. 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 33:249–254CrossRefGoogle Scholar
  55. Lu Y, Wu Z, Song Z et al (2016) Insight into the heat resistance of fish via blood: effects of heat stress on metabolism, oxidative stress and antioxidant response of olive flounder Paralichthys olivaceus and turbot Scophthalmus maximus. Fish Shellfish Immunol 58:125–135. CrossRefPubMedGoogle Scholar
  56. Machado C, Zaleski T, Rodrigues E et al (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. CrossRefPubMedGoogle Scholar
  57. Mark FC, Lucassen M, Strobel A et al (2012) Mitochondrial function in antarctic nototheniids with ND6 translocation. PLoS ONE 7:e31860. CrossRefPubMedPubMedCentralGoogle Scholar
  58. Meredith MP, King JC (2005) Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Lett 32:1–5. CrossRefGoogle Scholar
  59. 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. In: Jacob U, Woodward G (eds) Advances in ecological research, vol 46. Academic Press, Burlington, pp 351–426Google Scholar
  60. Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts:dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268. CrossRefGoogle Scholar
  61. Mueller IA, Grim JM, Beers JM et al (2011) Inter-relationship between mitochondrial function and susceptibility to oxidative stress in red- and white-blooded Antarctic notothenioid fishes. J Exp Biol 214:3732–3741. CrossRefPubMedGoogle Scholar
  62. Mueller IA, Devor DP, Grim JM et al (2012) Exposure to critical thermal maxima increases oxidative stress in hearts of white- but not red-blooded Antarctic notothenioid fishes. J Exp Biol 215:3655–3664. CrossRefPubMedGoogle Scholar
  63. Mueller I, Hoffman M, Dullen K, O’Brien K (2013) Moderate elevations in temperature do not increase oxidative stress in oxidative muscles of antarctic notothenioid fishes. Polar Biol 37:311–320. CrossRefGoogle Scholar
  64. 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 32:881–891CrossRefGoogle Scholar
  65. Pankhurst NW (2011) The endocrinology of stress in fish: an environmental perspective. Gen Comp Endocrinol 170:265–275. CrossRefPubMedGoogle Scholar
  66. Peck LS, Webb K, Bailey D (2004) Extreme sensitivity of biological function to temperature in Antarctic marine species. Funct Ecol 18:625–630CrossRefGoogle Scholar
  67. Peres H, Costas B, Perez-Jimenez A et al (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. CrossRefGoogle Scholar
  68. Petzel D (2005) Drinking in Antarctic fishes. Polar Biol 28:763–768. CrossRefGoogle Scholar
  69. Podrabsky JE, Somero GN (2006) Inducible heat tolerance in Antarctic notothenioid fishes. Polar Biol 30:39–43. CrossRefGoogle Scholar
  70. Poledník L, Rehulka J, Kranz A, Pledníková K, Hlavác V, Kazihnitková H (2008) Physiological responses of over-wintering common carp (Cyprinus carpio) to disturbance by Eurasian otter (Lutra lutra). Fish Physiol Biochem 34:223–234CrossRefGoogle Scholar
  71. Portner H-O (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. CrossRefPubMedGoogle Scholar
  72. Pörtner HO (2002) Climate variation and physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A 132:739–761CrossRefGoogle Scholar
  73. Pörtner HO (2004) Climate variability and the energetic pathways of evolution: the origin of endothermy in mammals and birds. Physiol Biochem Zool 77:959–998CrossRefGoogle Scholar
  74. Pörtner HO (2006) Climate-dependent evolution of Antarctic ectotherms: an integrative analysis. Deep Res Part II Top Stud Oceanogr 53:1071–1104. CrossRefGoogle Scholar
  75. Pörtner HO, Langenbuch M (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. CrossRefGoogle Scholar
  76. Raga G, Pichler HA, Zaleski T et al (2015) Ecological and physiological aspects of the antarctic fishes Notothenia rossii and Notothenia coriiceps in Admiralty Bay, Antarctic Peninsula. Environ Biol Fishes 98:775–788. CrossRefGoogle Scholar
  77. Rodrigues E, Feijó-Oliveira M, Vani GS et al (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. CrossRefPubMedGoogle Scholar
  78. Rodrigues E, Feijó-Oliveira M, Suda CNK et al (2015) Metabolic responses of the Antarctic fishes Notothenia rossii and Notothenia coriiceps to sewage pollution. Fish Physiol Biochem 41:1205–1220. CrossRefPubMedGoogle Scholar
  79. Roessig JM, Woodley CM, Cech JJ, Hansen LJ (2004) Effects of global climate change on marine and estuarine fishes and fisheries. Rev Fish Biol Fish 14:251–275CrossRefGoogle Scholar
  80. Rossi A, Bacchetta C, Cazenave J (2017) Effect of thermal stress on metabolic and oxidative stress biomarkers of Hoplosternum littorale (Teleostei, Callichthyidae). Ecol Indic 79:361–370. CrossRefGoogle Scholar
  81. Ruane NM, Huisman EA, Komen J (2001) Plasma cortisol and metabolite level profiles in two isogenic strains of common carp during confinement. J Fish Biol 59:1–12CrossRefGoogle Scholar
  82. Ryan SN (1995) The effect of chronic heat stress on cortisol levels in the Antarctic fish Pagothenia borchgrevinki. Experientia 51:768–774. CrossRefGoogle Scholar
  83. Sandersfeld T, Mark FC, Knust R (2017) Temperature-dependent metabolism in Antarctic fish: do habitat temperature conditions affect thermal tolerance ranges? Polar Biol 40:141–149. CrossRefGoogle Scholar
  84. Schielzeth H (2010) Simple means to improve the interpretability of regression coefficient. Methods Ecol Evol 1:103–113CrossRefGoogle Scholar
  85. Somero GN, Devries AL (1967) Temperature tolerance of some antarctic fishes. Science 156:257CrossRefGoogle Scholar
  86. Souza MRDP, Herrerias T, Zaleski T, Forgati M, Kandalski PK, Machado C, Silva DT, Piechnik CA, Moura MO, Donatti 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. CrossRefPubMedGoogle Scholar
  87. Spence P, Holmes RM, Hogg AM et al (2017) Localized rapid warming of West Antarctic subsurface waters by remote winds. Nat Clim Chang 7:595–603. CrossRefGoogle Scholar
  88. Strobel A, Bennecke S, Leo E et al (2012) Metabolic shifts in the Antarctic fish Notothenia rossii in response to rising temperature and PCO2. Front Zool 9:28. CrossRefPubMedPubMedCentralGoogle Scholar
  89. 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 Biochem Mol Biol 166:48–57CrossRefGoogle Scholar
  90. Takei Y, Hwang PP (2016) Homeostatic responses to osmotic stress. In: Schreck CB, Tort L, Farrell AP, Brauner CJ (eds) Fish physiology—biology of stress in fish, 35. Academic Press, San Diego, pp 207–249CrossRefGoogle Scholar
  91. 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 85:603–611CrossRefGoogle Scholar
  92. Tipsmark CK, Madsen SS (2001) Rapid modulation of Na+/K+-ATPase activity in osmoregulatory tissues of a salmonid fish. Journal Exp Biol 204:701–709Google Scholar
  93. Turner J, Barrand NE, Bracegirdle TJ et al (2014) Antarctic climate change and the environment: an update. Polar Rec (Gr Brit) 50:237–259. CrossRefGoogle Scholar
  94. Vaughan DG, Vaughan DG, MarshalL GJ, Connolley WM, Parkinson C, Mulvaney R, Hodgson DA, King JC, Pudsey CJ, Turner J (2003) Recent rapid regional climate warming on the Antarctic Peninsula. Clim Chang 60:243–274CrossRefGoogle Scholar
  95. Verde C, Parisi E, di Prisco G (2006) The evolution of thermal adaptation in polar fish. Gene 385:137–145. CrossRefPubMedGoogle Scholar
  96. Whiteley NM, Egginton S (1999) Antarctic fishes have a limited capacity for catecholamine synthesis. J Exp Biol 202:3623–3629PubMedGoogle Scholar
  97. Whittamore JM, Cooper CA, Wilson RW (2010) HCO3 secretion and CaCO3 precipitation play major roles in intestinal water absorption in marine teleost fish in vivo. Am J Physiol Regul Integr Comp Physiol 298:R877–R886. CrossRefPubMedPubMedCentralGoogle Scholar
  98. Zafalon-Silva B, Zebral YD, Bianchini A et al (2017) Erythrocyte nuclear abnormalities and leukocyte profile in the Antarctic fish Notothenia coriiceps after exposure to short- and long-term heat stress. Polar Biol 40:1755–1760. CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Priscila Krebsbach Kandalski
    • 1
  • Maria Rosa Dmengeon Pedreiro de Souza
    • 1
  • Tatiana Herrerias
    • 2
  • Cintia Machado
    • 1
  • Tania Zaleski
    • 1
  • Mariana Forgati
    • 1
  • Angela Carolina Guillen
    • 1
  • Douglas Viana
    • 1
  • Maurício Osvaldo Moura
    • 3
  • Lucélia Donatti
    • 1
    Email author
  1. 1.Adaptive Biology Laboratory, Department of Cell BiologyFederal University of ParanaCuritibaBrazil
  2. 2.Faculty GuairacáGuarapuavaBrazil
  3. 3.Department of ZoologyFederal University of ParanaCuritibaBrazil

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