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RESEARCH ARTICLE

Gas chromatography–mass spectrometry analysis on effects of thermal shock on the fatty acid composition of the gills of the Antarctic teleost, Trematomus bernacchii

Cristina Truzzi https://orcid.org/0000-0002-7429-9880 A B , Anna Annibaldi A , Matteo Antonucci A , Giuseppe Scarponi A and Silvia Illuminati A
+ Author Affiliations
- Author Affiliations

A Department of Life and Environmental Sciences, Università Politecnica delle Marche, via Brecce Bianche 60131 Ancona, Italy.

B Corresponding author. Email: c.truzzi@univpm.it

Environmental Chemistry 15(7) 424-435 https://doi.org/10.1071/EN18130
Submitted: 11 June 2018  Accepted: 9 August 2018   Published: 24 September 2018

Environmental context. Global warming is an important problem for life on Earth, and there is an increasing need to understand how organisms respond to rising temperatures. We show that an Antarctic fish, the emerald rockcod, can acclimate to thermal shock by modifying the fatty acid composition and total lipid content in its gills. This study contributes to our understanding of how the physiology of Antarctic life could be influenced by climate change.

Abstract. As a result of rising temperatures in the Antarctic seawater, there is an increasing interest to investigate the capacities for inducing a temperature acclimation response in Antarctic organisms. We analysed the effect of a thermal shock on the fatty acid (FA) composition of gills of the Antarctic notothenioid Trematomus bernacchii. To perform the quantification of fatty acids in gills, we applied an analytical method based on a fast microwave-assisted extraction (MAE) of lipids from a lyophilised sample, a base-catalysed trans-esterification of lipid extract to obtain fatty acid methyl esters (FAMEs), and their separation and identification by gas chromatography–mass spectrometry. The percentage of lipids extracted with MAE preceded by sample lyophilisation, 0.6 ± 0.3 % ww (wet weight), was consistent with the lipids obtained by the official Bligh and Dyer method, 0.8 ± 0.3 % ww. These data are among the first ever published for T. bernacchii. Specimens, caught in Terra Nova Bay (Ross Sea), were held in different tanks at 0, +1 and +2 °C, for 1, 5 and 10 days. In general, thermal shock produced an alteration in total lipid content, an increase in the percentage of saturated FAs, a decrease in mono-unsaturated FAs, and a variable response of poly-unsaturated FAs (an increase in specimens exposed to 0 and +1 °C, a decrease in those exposed to +2 °C). A chemometric approach based on principal component analysis indicated that temperature and exposure time influenced the composition of FAs in the gills, probably through an alteration of the metabolic pathways of FAs. This is the first study ever published on the FA composition of total lipids in gills of T. bernacchii exposed to high temperatures. This study demonstrates that T. bernacchii is capable of rapidly acclimating to a thermal shock, and contributes to increasing the knowledge on the effect of temperature on Antarctic notothenioids.

Additional keywords : microwave-assisted extraction, principal component analysis.


References

Abele D, Puntarulo S (2004). Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 138, 405–415.
Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fishCrossref | GoogleScholarGoogle Scholar |

Ackman RG (1989). ‘Marine biogenic lipids, Vol. 1.’ (CRC Press: Boca Raton, FL)

Barbaro E, Zangrando R, Kirchgeorg T, Bazzano A, Illuminati S, Annibaldi A, Rella S, Truzzi C, Grotti M, Ceccarini A, Malitesta C, Scarponi G, Gambaro A (2016). An integrated study of the chemical composition of Antarctic aerosol to investigate natural and anthropogenic sources. Environmental Chemistry 125, 212–221.

Bargagli R, Corsolini S, Fossi MC, Sanchez-Hernandez JC, Focardi S (1998). Antarctic fish Trematomus bernacchii as biomonitor of environmental contaminants at Terra Nova Bay Station (Ross Sea). Memoirs of National Institute of Polar Research 52, 220–229.

Barnes DKA, Peck LS, Morley SA (2010). Ecological relevance of laboratory determined temperature limits: colonization potential, biogeography and resilience of Antarctic invertebrates to environmental change. Global Change Biology 16, 3164–3169.

Basconcillo LS, McCarry BE (2008). Comparison of three GC/MS methodologies for the analysis of fatty acids in Sinorhizobium meliloti: Development of a micro-scale, one-vial method. Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Sciences 871, 22–31.
Comparison of three GC/MS methodologies for the analysis of fatty acids in Sinorhizobium meliloti: Development of a micro-scale, one-vial methodCrossref | GoogleScholarGoogle Scholar |

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?. The Journal of Experimental Biology 218, 1834–1845.
Antarctic notothenioid fish: what are the future consequences of ‘losses’ and ‘gains’ acquired during long-term evolution at cold and stable temperatures?Crossref | GoogleScholarGoogle Scholar |

Bilyk KT, DeVries AL (2011). Heat tolerance and its plasticity in Antarctic fishes. Comparative Biochemistry and Physiology Part A,:Molecular & Integrative Physiology 158, 382–390.
Heat tolerance and its plasticity in Antarctic fishesCrossref | GoogleScholarGoogle Scholar |

Bligh EG, Dyer WJ (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917.
A rapid method of total lipid extraction and purificationCrossref | GoogleScholarGoogle Scholar |

Borghesi N, Corsolini S, Focardi S (2008). Levels of polybrominated diphenyl ethers (PBDEs) and organochlorine pollutants in two species of Antarctic fish (Chionodraco hamatus and Trematomus bernacchii). Chemosphere 73, 155–160.
Levels of polybrominated diphenyl ethers (PBDEs) and organochlorine pollutants in two species of Antarctic fish (Chionodraco hamatus and Trematomus bernacchii)Crossref | GoogleScholarGoogle Scholar |

Brauer PR, Sanmann JN, Petzel DH (2005). Effects of warm acclimation on Na+/K+-ATPase α-subunit expression in chloride cells of Antarctic fish. The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology 285A, 600–609.
Effects of warm acclimation on Na+/K+-ATPase α-subunit expression in chloride cells of Antarctic fishCrossref | GoogleScholarGoogle Scholar |

Brodte E, Graeve M, Jacob U, Knust R, Pörtner HO (2008). Temperature-dependent lipid levels and components in polar and temperate eelpout (Zoarcidae). Fish Physiology and Biochemistry 34, 261–274.
Temperature-dependent lipid levels and components in polar and temperate eelpout (Zoarcidae)Crossref | GoogleScholarGoogle Scholar |

Buckley BA, Somero GN (2009). cDNA microarray analysis reveals the capacity of the cold-adapted Antarctic fish Trematomus bernacchii to alter gene expression in response to heat stress. Polar Biology 32, 403–415.
cDNA microarray analysis reveals the capacity of the cold-adapted Antarctic fish Trematomus bernacchii to alter gene expression in response to heat stressCrossref | GoogleScholarGoogle Scholar |

Buckley BA, Place SP, Hofmann GE (2004). Regulation of heat shock genes in isolated hepatocytes from an Antarctic fish, Trematomus bernacchii. The Journal of Experimental Biology 207, 3649–3656.
Regulation of heat shock genes in isolated hepatocytes from an Antarctic fish, Trematomus bernacchiiCrossref | GoogleScholarGoogle Scholar |

Canonico L, Ashoor S, Taccari M, Comitini F, Antonucci M, Truzzi C, Scarponi G, Ciani M (2016). Conversion of raw glycerol to microbial lipids by new Metschnikowia and Yarrowia lipolytica strains. Annals of Microbiology 66, 1409–1418.
Conversion of raw glycerol to microbial lipids by new Metschnikowia and Yarrowia lipolytica strainsCrossref | GoogleScholarGoogle Scholar |

Carney Almroth B, Asker N, Wassmur B, Rosengren M, Jutfelt F, Gräns A, Sundell K, Axelsson M, Sturve J (2015). Warmer water temperature results in oxidative damage in an Antarctic fish, the bald notothen. Journal of Experimental Marine Biology and Ecology 468, 130–137.
Warmer water temperature results in oxidative damage in an Antarctic fish, the bald notothenCrossref | GoogleScholarGoogle Scholar |

Clarke A (1991). What is cold adaptation and how should we measure it?. American Zoologist 31, 81–92.
What is cold adaptation and how should we measure it?Crossref | GoogleScholarGoogle Scholar |

Colella A, Patamia M, Galtieri A, Giardina B (2000). Cold adaptation and oxidative metabolism of Antarctic fish. The Italian Journal of Zoology 67, 33–36.
Cold adaptation and oxidative metabolism of Antarctic fishCrossref | GoogleScholarGoogle Scholar |

Constable AJ, Melbourne-Thomas J, Corney SP, Arrigo KR, Barbraud C, Barnes DKA, Bindoff NL, Boyd PW, Brandt A, Costa DP, Davidson AT, Ducklow HW, Emmerson L, Fukuchi M, Gutt J, Hindell MA, Hofmann EE, Hosie GW, Iida T, Jacob S, Johnston NM, Kawaguchi S, Kokubun N, Koubbi P, Lea M-A, Makhado A, Massom RA, Meiners K, Meredith MP, Murphy EJ, Nicol S, Reid K, Richerson K, Riddle MJ, Rintoul SR, Smith WO, Southwell C, Stark JS, Sumner M, Swadling KM, Takahashi KT, Trathan PN, Welsford DC, Weimerskirch H, Westwood KJ, Wienecke BC, Wolf-Gladrow D, Wright SW, Xavier JC, Ziegler P (2014). Climate change and Southern Ocean ecosystems I: how changes in physical habitats directly affect marine biota. Global Change Biology 20, 3004–3025.
Climate change and Southern Ocean ecosystems I: how changes in physical habitats directly affect marine biotaCrossref | GoogleScholarGoogle Scholar |

Corsolini S, Covaci A, Ademollo N, Focardi S, Schepens P (2006). Occurrence of organochlorine pesticides (OCPs) and their enantiomeric signatures, and concentrations of polybrominated diphenyl ethers (PBDEs) in the Adélie penguin food web, Antarctica. Environmental Pollution 140, 371–382.
Occurrence of organochlorine pesticides (OCPs) and their enantiomeric signatures, and concentrations of polybrominated diphenyl ethers (PBDEs) in the Adélie penguin food web, AntarcticaCrossref | GoogleScholarGoogle Scholar |

Daniel WW, Cross CL (2013). ‘Biostatistics: a foundation for analysis in the health sciences, 10th edn.’ Student solution manual (Wiley and Sons: New York, NY)

Davis BE, Flynn EE, Miller NA, Nelson FA, Fangue NA, Todgham AE (2018). Antarctic emerald rockcod have the capacity to compensate for warming when uncoupled from CO2 -acidification. Global Change Biology 24, e655–e670.
Antarctic emerald rockcod have the capacity to compensate for warming when uncoupled from CO2 -acidificationCrossref | GoogleScholarGoogle Scholar |

de 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.
Heat stress in the heart and muscle of the Antarctic fishes Notothenia rossii and Notothenia coriiceps: Carbohydrate metabolism and antioxidant defenceCrossref | GoogleScholarGoogle Scholar |

Eastman JT, Gon O, Heemstra PC (1990). The biology and physiological ecology of notothenioid fishes. In ‘Fishes of the Southern Ocean’. (Eds O Gon, PC Heemstra) pp. 34–51 (JLB Smith Institute of Ichthyology: Grahamstown, South Africa)

Eastman JT (1993). ‘Antarctic fish biology: evolution in a unique environment.’ (Academic Press: New York, NY)

Enzor LA, Place SP (2014). Is warmer better? Decreased oxidative damage in notothenioid fish after long-term acclimation to multiple stressors. The Journal of Experimental Biology 217, 3301–3310.

Enzor LA, Hunter EM, Place SP (2017). The effects of elevated temperature and ocean acidification on the metabolic pathways of notothenioid fish. Conservation Physiology 5, cox019
The effects of elevated temperature and ocean acidification on the metabolic pathways of notothenioid fishCrossref | GoogleScholarGoogle Scholar |

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. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 187, 1137–1154.
Effects of heat stress on the renal and branchial carbohydrate metabolism and antioxidant system of Antarctic fishCrossref | GoogleScholarGoogle Scholar |

Franklin CE, Axelsson M, Davison W (2001). Constancy and control of heart rate during an increase in temperature in the Antarctic fish Pagothenia borchgrevinki. Experimental Biology Online 6, 1–8.
Constancy and control of heart rate during an increase in temperature in the Antarctic fish Pagothenia borchgrevinkiCrossref | GoogleScholarGoogle Scholar |

Franklin CE, Davison W, Seebacher F (2007). Antarctic fish can compensate for rising temperatures: thermal acclimation of cardiac performance in Pagothenia borchgrevinki. The Journal of Experimental Biology 210, 3068–3074.
Antarctic fish can compensate for rising temperatures: thermal acclimation of cardiac performance in Pagothenia borchgrevinkiCrossref | GoogleScholarGoogle Scholar |

Ghosh R, Lokman PM, Lamare MD, Metcalf VJ, Burritt DJ, Davison W, Hageman KJ (2013). Changes in physiological responses of an Antarctic fish, the emerald rock cod (Trematomus bernacchii), following exposure to polybrominated diphenyl ethers (PBDEs). Aquatic Toxicology (Amsterdam, Netherlands) 128–129, 91–100.
Changes in physiological responses of an Antarctic fish, the emerald rock cod (Trematomus bernacchii), following exposure to polybrominated diphenyl ethers (PBDEs)Crossref | GoogleScholarGoogle Scholar |

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. The Journal of Experimental Biology 198, 2279–2291.

Grim JM, Miles DRB, Crockett EL (2010). Temperature acclimation alters oxidative capacities and composition of membrane lipids without influencing activities of enzymatic antioxidants or susceptibility to lipid peroxidation in fish muscle. The Journal of Experimental Biology 213, 445–452.
Temperature acclimation alters oxidative capacities and composition of membrane lipids without influencing activities of enzymatic antioxidants or susceptibility to lipid peroxidation in fish muscleCrossref | GoogleScholarGoogle Scholar |

Guynn S, Dowd F, Petzel D (2002). Characterization of gill Na/K-ATPase activity and ouabain binding in Antarctic and New Zealand nototheniid fishes. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 131, 363–374.
Characterization of gill Na/K-ATPase activity and ouabain binding in Antarctic and New Zealand nototheniid fishesCrossref | GoogleScholarGoogle Scholar |

Hashimoto M, Hossain S, Shido O (2006). Docosahexaenoic acid but not eicosapentaenoic acid withstands dietary cholesterol-induced decreases in platelet membrane fluidity. Molecular and Cellular Biochemistry 293, 1–8.
Docosahexaenoic acid but not eicosapentaenoic acid withstands dietary cholesterol-induced decreases in platelet membrane fluidityCrossref | GoogleScholarGoogle Scholar |

Hazel JR (1983). The incorporation of unsaturated fatty acids of the n-9, n-6, and n-3 families into individual phospholipids by isolated hepatocytes of thermally-acclimated rainbow trout, Salmo gairdneri. The Journal of Experimental Zoology 227, 167–176.
The incorporation of unsaturated fatty acids of the n-9, n-6, and n-3 families into individual phospholipids by isolated hepatocytes of thermally-acclimated rainbow trout, Salmo gairdneriCrossref | GoogleScholarGoogle Scholar |

Hixson SM, Arts MT (2016). Climate warming is predicted to reduce omega-3, long-chain, polyunsaturated fatty acid production in phytoplankton. Global Change Biology 22, 2744–2755.
Climate warming is predicted to reduce omega-3, long-chain, polyunsaturated fatty acid production in phytoplanktonCrossref | GoogleScholarGoogle Scholar |

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 Biology 31, 991–997.
Effects of warm acclimation on serum osmolality, cortisol and hematocrit levels in the Antarctic fish, Trematomus bernacchiiCrossref | GoogleScholarGoogle Scholar |

Huth TJ, Place SP (2013). De novo assembly and characterization of tissue specific transcriptomes in the emerald notothen, Trematomus bernacchii. BMC Genomics 14, 805

Huth TJ, Place SP (2016). Transcriptome wide analyses reveal a sustained cellular stress response in the gill tissue of Trematomus bernacchii after acclimation to multiple stressors. BMC Genomics 17, 127
Transcriptome wide analyses reveal a sustained cellular stress response in the gill tissue of Trematomus bernacchii after acclimation to multiple stressorsCrossref | GoogleScholarGoogle Scholar |

Illuminati S, Truzzi C, Annibaldi A, Migliarini B, Carnevali O, Scarponi G (2010). Cadmium bioaccumulation and metallothionein induction in the liver of the Antarctic teleost Trematomus bernacchii during an on-site short-term exposure to the metal via seawater. Toxicological and Environmental Chemistry 92, 617–640.
Cadmium bioaccumulation and metallothionein induction in the liver of the Antarctic teleost Trematomus bernacchii during an on-site short-term exposure to the metal via seawaterCrossref | GoogleScholarGoogle Scholar |

Illuminati S, Annibaldi A, Romagnoli T, Libani G, Antonucci M, Scarponi G, Totti C, Truzzi C (2017). Distribution of Cd, Pb and Cu between dissolved fraction, inorganic particulate and phytoplankton in seawater of Terra Nova Bay (Ross Sea, Antarctica) during austral summer 2011–12. Chemosphere 185, 1122–1135.
Distribution of Cd, Pb and Cu between dissolved fraction, inorganic particulate and phytoplankton in seawater of Terra Nova Bay (Ross Sea, Antarctica) during austral summer 2011–12Crossref | GoogleScholarGoogle Scholar |

IPCC (2014). . . Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. (IPCC: Geneva, Switzerland)

Jayasundara N, Healy TM, Somero GN (2013). Effects of temperature acclimation on cardiorespiratory performance of the Antarctic notothenioid Trematomus bernacchii. Polar Biology 36, 1047–1057.
Effects of temperature acclimation on cardiorespiratory performance of the Antarctic notothenioid Trematomus bernacchiiCrossref | GoogleScholarGoogle Scholar |

Juárez M, Polvillo O, Contò M, Ficco A, Ballico S, Failla S (2008). Comparison of four extraction/methylation analytical methods to measure fatty acid composition by gas chromatography in meat. Journal of Chromatography. A 1190, 327–332.
Comparison of four extraction/methylation analytical methods to measure fatty acid composition by gas chromatography in meatCrossref | GoogleScholarGoogle Scholar |

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. Journal of Thermal Biology 68, 110–118.
Effects of increasing temperature on antioxidant defense system and oxidative stress parameters in the Antarctic fish Notothenia coriiceps and Notothenia rossiiCrossref | GoogleScholarGoogle Scholar |

Lana NB, Berton P, Covaci A, Ciocco NF, Barrera-Oro E, Atencio A, Altamirano JC (2014). Fingerprint of persistent organic pollutants in tissues of Antarctic notothenioid fish. Science of the Total Environment 499, 89–98.
Fingerprint of persistent organic pollutants in tissues of Antarctic notothenioid fishCrossref | GoogleScholarGoogle Scholar |

Lowe CJ, Seebacher F, Davison W (2005). Thermal sensitivity of heart rate and insensitivity of blood pressure in the Antarctic nototheniid fish Pagothenia borchgrevinki. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 175, 97–105.
Thermal sensitivity of heart rate and insensitivity of blood pressure in the Antarctic nototheniid fish Pagothenia borchgrevinkiCrossref | GoogleScholarGoogle Scholar |

Machado C, Zaleski T, Rodrigues E, Carvalho C. dos S., Cadena SMSC, Gozzi GJ, Krebsbach P, Rios FS, Donatti L (2014). Effect of temperature acclimation on the liver antioxidant defence system of the Antarctic nototheniids Notothenia coriiceps and Notothenia rossii. Comparative Biochemistry and Physiology Part B: Biochemistry & Molecular Biology 172–173, 21–28.
Effect of temperature acclimation on the liver antioxidant defence system of the Antarctic nototheniids Notothenia coriiceps and Notothenia rossiiCrossref | GoogleScholarGoogle Scholar |

Mahesar SA, Sherazi STH, Abro K, Kandhro A, Bhanger MI, van de Voort FR, Sedman J (2008). Application of microwave heating for the fast extraction of fat content from the poultry feeds. Talanta 75, 1240–1244.
Application of microwave heating for the fast extraction of fat content from the poultry feedsCrossref | GoogleScholarGoogle Scholar |

Malekar VC, Morton JD, Hider RN, Cruickshank RH, Hodge S, Metcalf VJ (2018). Effect of elevated temperature on membrane lipid saturation in Antarctic notothenioid fish. PeerJ 6,
Effect of elevated temperature on membrane lipid saturation in Antarctic notothenioid fishCrossref | GoogleScholarGoogle Scholar |

Mayzaud P, Chevallier J, Tavernier E, Moteki M, Koubbi P (2011). Lipid composition of the Antarctic fish Pleuragramma antarcticum. Influence of age class. Polar Science 5, 264–271.
Lipid composition of the Antarctic fish Pleuragramma antarcticum. Influence of age classCrossref | GoogleScholarGoogle Scholar |

Morrison JF, Guynn SR, Scofield MA, Dowd FJ, Petzel DH (2006). Warm acclimation changes the expression of the Na+/K+-ATPase α subunit isoforms in Antarctic fish gills. Journal of Experimental Marine Biology and Ecology 333, 129–139.
Warm acclimation changes the expression of the Na+/K+-ATPase α subunit isoforms in Antarctic fish gillsCrossref | GoogleScholarGoogle Scholar |

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 Biology 37, 311–320.
Moderate elevations in temperature do not increase oxidative stress in oxidative muscles of Antarctic notothenioid fishesCrossref | GoogleScholarGoogle Scholar |

Murzina S, Nefedova Z, Falk-Petersen S, Ripatti P, Ruokolainen T, Pekkoeva S, Nemova N (2013). Lipid Status of the Two High Latitude Fish Species, Leptoclinus maculatus and Lumpenus fabricii. International Journal of Molecular Sciences 14, 7048–7060.
Lipid Status of the Two High Latitude Fish Species, Leptoclinus maculatus and Lumpenus fabriciiCrossref | GoogleScholarGoogle Scholar |

Near TJ, Cheng C-HC (2008). Phylogenetics of notothenioid fishes (Teleostei: Acanthomorpha): Inferences from mitochondrial and nuclear gene sequences. Molecular Phylogenetics and Evolution 47, 832–840.
Phylogenetics of notothenioid fishes (Teleostei: Acanthomorpha): Inferences from mitochondrial and nuclear gene sequencesCrossref | GoogleScholarGoogle Scholar |

Palacios-Pelaez R, Lukiw WJ, Bazan NG (2010). Omega-3 Essential Fatty Acids Modulate Initiation and Progression of Neurodegenerative Disease. Molecular Neurobiology 41, 367–374.
Omega-3 Essential Fatty Acids Modulate Initiation and Progression of Neurodegenerative DiseaseCrossref | GoogleScholarGoogle Scholar |

Parihar MS, Javeri T, Hemnani T, Dubey AK, Prakash P (1997). Responses of superoxide dismutase, glutathione peroxidase and reduced glutathione antioxidant defenses in gills of the freshwater catfish (Heteropneustes fossillis) to short-term elevated temperature. Journal of Thermal Biology 22, 151–156.
Responses of superoxide dismutase, glutathione peroxidase and reduced glutathione antioxidant defenses in gills of the freshwater catfish (Heteropneustes fossillis) to short-term elevated temperatureCrossref | GoogleScholarGoogle Scholar |

Perry SF, Gilmour KM (2002). Sensing and transfer of respiratory gases at the fish gill. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 293, 249–263.
Sensing and transfer of respiratory gases at the fish gillCrossref | GoogleScholarGoogle Scholar |

Place SP, Hofmann GE (2005). Constitutive expression of a stress-inducible heat shock protein gene, hsp70, in phylogenetically distant Antarctic fish. Polar Biology 28, 261–267.
Constitutive expression of a stress-inducible heat shock protein gene, hsp70, in phylogenetically distant Antarctic fishCrossref | GoogleScholarGoogle Scholar |

Podrabsky JE, Somero GN (2006). Inducible heat tolerance in Antarctic notothenioid fishes. Polar Biology 30, 39–43.
Inducible heat tolerance in Antarctic notothenioid fishesCrossref | GoogleScholarGoogle Scholar |

Porta A, Fortino V, Armenante A, Maresca B (2013). Cloning and characterization of a Δ9-desaturase gene of the Antarctic fish Chionodraco hamatus and Trematomus bernacchii. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 183, 379–392.
Cloning and characterization of a Δ9-desaturase gene of the Antarctic fish Chionodraco hamatus and Trematomus bernacchiiCrossref | GoogleScholarGoogle Scholar |

Pörtner H (2001). Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88, 137–146.
Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animalsCrossref | GoogleScholarGoogle Scholar |

Pörtner HO, Knust R (2007). Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95–97.
Climate change affects marine fishes through the oxygen limitation of thermal toleranceCrossref | GoogleScholarGoogle Scholar |

Pörtner HO, Playle RC (2007). ‘Cold ocean physiology.’ Seminar series (Cambridge University Press: Cambridge).

Pörtner HO, Lucassen M, Storch D (2005). Metabolic biochemistry: its role in thermal tolerance and in the capacities of physiological and ecological function. Fish Physiology 22, 79–154.
Metabolic biochemistry: its role in thermal tolerance and in the capacities of physiological and ecological functionCrossref | GoogleScholarGoogle Scholar |

Ramalhosa MJ, Paíga P, Morais S, Rui Alves M, Delerue-Matos C, Oliveira MBPP (2012). Lipid content of frozen fish: Comparison of different extraction methods and variability during freezing storage. Food Chemistry 131, 328–336.
Lipid content of frozen fish: Comparison of different extraction methods and variability during freezing storageCrossref | GoogleScholarGoogle Scholar |

Regoli F, Nigro M, Benedetti M, Gorbi S, Pretti C, Gervasi PG, Fattorini D (2005). Interactions between metabolism of trace metals and xenobiotic agonists of the aryl hydrocarbon receptor in the antarctic fish Trematomus bernacchii: Environmental perspectives. Environmental Toxicology and Chemistry 24, 1475–1482.
Interactions between metabolism of trace metals and xenobiotic agonists of the aryl hydrocarbon receptor in the antarctic fish Trematomus bernacchii: Environmental perspectivesCrossref | GoogleScholarGoogle Scholar |

Ríos JM, Lana NB, Ciocco NF, Covaci A, Barrera-Oro E, Moreira E, Altamirano JC (2017). Implications of biological factors on accumulation of persistent organic pollutants in Antarctic notothenioid fish. Ecotoxicology and Environmental Safety 145, 630–639.
Implications of biological factors on accumulation of persistent organic pollutants in Antarctic notothenioid fishCrossref | GoogleScholarGoogle Scholar |

Roche H, Pérès G (1984). Influence of acclimatization to different temperatures and of the seasonal factor on the lipid composition of liver, muscle and intestinal tissues of the sea dace (Dicentrarchus labrax, Pisces). Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 78, 755–759.
Influence of acclimatization to different temperatures and of the seasonal factor on the lipid composition of liver, muscle and intestinal tissues of the sea dace (Dicentrarchus labrax, Pisces)Crossref | GoogleScholarGoogle Scholar |

Ryan SN (1995). The effect of chronic heat stress on cortisol levels in the antarctic fish Pagothenia borchgrevinki. Experientia 51, 768–774.
The effect of chronic heat stress on cortisol levels in the antarctic fish Pagothenia borchgrevinkiCrossref | GoogleScholarGoogle Scholar |

Sandersfeld T, Davison W, Lamare MD, Knust R, Richter C (2015). Elevated temperature causes metabolic trade-offs at the whole-organism level in the Antarctic fish Trematomus bernacchii. The Journal of Experimental Biology 218, 2373–2381.
Elevated temperature causes metabolic trade-offs at the whole-organism level in the Antarctic fish Trematomus bernacchiiCrossref | GoogleScholarGoogle Scholar |

Schulte PM (2007). Responses to environmental stressors in an estuarine fish: Interacting stressors and the impacts of local adaptation. Journal of Thermal Biology 32, 152–161.
Responses to environmental stressors in an estuarine fish: Interacting stressors and the impacts of local adaptationCrossref | GoogleScholarGoogle Scholar |

Seebacher F, Davison W, Lowe CJ, Franklin CE (2005). A falsification of the thermal specialization paradigm: compensation for elevated temperatures in Antarctic fishes. Biology Letters 1, 151–154.
A falsification of the thermal specialization paradigm: compensation for elevated temperatures in Antarctic fishesCrossref | GoogleScholarGoogle Scholar |

Serhan CN, Chiang N, Van Dyke TE (2008). Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nature Reviews. Immunology 8, 349–361.
Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediatorsCrossref | GoogleScholarGoogle Scholar |

Sidell BD (1998). Intracellular oxygen diffusion: the roles of myoglobin and lipid at cold body temperature. The Journal of Experimental Biology 201, 1119–1128.

Sidell BD, Hazel JR (2002). Triacylglycerol lipase activities in tissues of Antarctic fishes. Polar Biology 25, 517–522.
Triacylglycerol lipase activities in tissues of Antarctic fishesCrossref | GoogleScholarGoogle Scholar |

Sinensky M (1974). Homeoviscous adaptation – a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 71, 522–525.
Homeoviscous adaptation – a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coliCrossref | GoogleScholarGoogle Scholar |

Sleadd IM (2014). Sub-lethal heat stress causes apoptosis in an Antarctic fish that lacks an inducible heat shock response. Journal of Thermal Biology 44, 119–125.
Sub-lethal heat stress causes apoptosis in an Antarctic fish that lacks an inducible heat shock responseCrossref | GoogleScholarGoogle Scholar |

Smetacek V, Nicol S (2005). Polar ocean ecosystems in a changing world. Nature 437, 362–368.
Polar ocean ecosystems in a changing worldCrossref | GoogleScholarGoogle Scholar |

Somero GN, DeVries AL (1967). Temperature tolerance of some Antarctic fishes. Science 156, 257–258.
Temperature tolerance of some Antarctic fishesCrossref | GoogleScholarGoogle Scholar |

Strobel A, Graeve M, Poertner HO, Mark FC (2013). Mitochondrial acclimation capacities to ocean warming and acidification are limited in the Antarctic Nototheniid fish, Notothenia rossii and Lepidonotothen squamifrons. PLoS One 8, e68865
Mitochondrial acclimation capacities to ocean warming and acidification are limited in the Antarctic Nototheniid fish, Notothenia rossii and Lepidonotothen squamifronsCrossref | GoogleScholarGoogle Scholar |

Teoh M-L, Chu W-L, Phang S-M (2010). Effect of temperature change on physiology and biochemistry of algae: a review. Malaysian Journal of Science 29, 82–97.
Effect of temperature change on physiology and biochemistry of algae: a reviewCrossref | GoogleScholarGoogle Scholar |

Tiku PE, Gracey AY, Macartney AI, Beynon RJ, Cossins AR (1996). Cold-induced expression of Δ9-desaturase in carp by transcriptional and posttranslational mechanisms. Science 271, 815–818.
Cold-induced expression of Δ9-desaturase in carp by transcriptional and posttranslational mechanismsCrossref | GoogleScholarGoogle Scholar |

Timmermann R, Hellmer HH (2013). Southern Ocean warming and increased ice shelf basal melting in the twenty-first and twenty-second centuries based on coupled ice-ocean finite-element modelling. Ocean Dynamics 63, 1011–1026.
Southern Ocean warming and increased ice shelf basal melting in the twenty-first and twenty-second centuries based on coupled ice-ocean finite-element modellingCrossref | GoogleScholarGoogle Scholar |

Tolomeo AM, Carraro A, Bakiu R, Toppo S, Place SP, Ferro D, Santovito G (2016). Peroxiredoxin 6 from the Antarctic emerald rockcod: molecular characterization of its response to warming. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 186, 59–71.
Peroxiredoxin 6 from the Antarctic emerald rockcod: molecular characterization of its response to warmingCrossref | GoogleScholarGoogle Scholar |

Tomanek L (2008). The importance of physiological limits in determining biogeographical range shifts due to global climate change: the heat-shock response. Physiological and Biochemical Zoology 81, 709–717.
The importance of physiological limits in determining biogeographical range shifts due to global climate change: the heat-shock responseCrossref | GoogleScholarGoogle Scholar |

Truzzi C, Illuminati S, Annibaldi A, Finale C, Rossetti M, Scarponi G (2014). Physicochemical properties of honey from Marche, Central Italy: classification of unifloral and multifloral honeys by multivariate analysis. Natural Product Communications 9, 1595–1602.

Truzzi C, Illuminati S, Annibaldi A, Antonucci M, Scarponi G (2017). Quantification of fatty acids in the muscle of Antarctic fish Trematomus bernacchii by gas chromatography-mass spectrometry: Optimization of the analytical methodology. Chemosphere 173, 116–123.
Quantification of fatty acids in the muscle of Antarctic fish Trematomus bernacchii by gas chromatography-mass spectrometry: Optimization of the analytical methodologyCrossref | GoogleScholarGoogle Scholar |

Truzzi C, Illuminati S, Antonucci M, Scarponi G, Annibaldi A (2018). Heat shock influences the fatty acid composition of the muscle of the Antarctic fish Trematomus bernacchii. Marine Environmental Research 139, 122–128.
Heat shock influences the fatty acid composition of the muscle of the Antarctic fish Trematomus bernacchiiCrossref | GoogleScholarGoogle Scholar |

Virot M, Tomao V, Colnagui G, Visinoni F, Chemat F (2007). New microwave-integrated Soxhlet extraction: An advantageous tool for the extraction of lipids from food products. Journal of Chromatography A 1174, 138–144.
New microwave-integrated Soxhlet extraction: An advantageous tool for the extraction of lipids from food productsCrossref | GoogleScholarGoogle Scholar |

Weinstein RB, Somero GN (1998). Effects of temperature on mitochondrial function in the Antarctic fish Trematomus bernacchii. Journal of Comparative Physiology B: Biochemical, Systems and Environmental Physiology 168, 190–196.
Effects of temperature on mitochondrial function in the Antarctic fish Trematomus bernacchiiCrossref | GoogleScholarGoogle Scholar |

Wilhelm-Filho D, González-Flecha B, Boveris A (1994). Gill diffusion as a physiological mechanism for hydrogen peroxide elimination by fish. Brazilian Journal of Medical and Biological Research 27, 2879–2882.

Windisch HS, Frickenhaus S, John U, Knust R, Pörtner H-O, Lucassen M (2014). Stress response or beneficial temperature acclimation: transcriptomic signatures in Antarctic fish (Pachycara brachycephalum). Molecular Ecology 23, 3469–3482.
Stress response or beneficial temperature acclimation: transcriptomic signatures in Antarctic fish (Pachycara brachycephalum)Crossref | GoogleScholarGoogle Scholar |

Wold S (1978). Cross-Validatory Estimation of the Number of Components in Factor and Principal Components Models. Technometrics 20, 397–405.
Cross-Validatory Estimation of the Number of Components in Factor and Principal Components ModelsCrossref | GoogleScholarGoogle Scholar |