Abstract
Total lipid content, lipid classes and fatty acid composition were analysed in tissues from two eelpout species fed on the same diet, the Antarctic Pachycara brachycephalum and the temperate Zoarces viviparus, with the aim of determining the role of lipids in fishes from different thermal habitats. The lipid content increased with decreasing temperature in the liver of both species, suggesting enhanced lipid storage under cold conditions. In P. brachycephalum, lipid composition in the liver and muscle was strongly dominated by triacylglycerols between 0 and 6°C. In contrast, in the temperate species, lipid class composition changed with changes in the temperature. When acclimatized to 4 and 6°C Z. viviparus not only displayed a shift to lipid anabolism and pronounced lipid storage, as indicated by high triacylglycerol levels, but also a shift to patterns of cold adaptation, as reflected by an increased content of polyunsaturated fatty acids in the lipid extract. Unsaturated fatty acids were also abundant in the Antarctic eelpout, but when compared to Z. viviparus at the same temperatures, the latter had significantly higher ratios of polyunsaturated to saturated fatty acid levels, whereas the Antarctic eelpout showed significantly higher ratios of monounsaturated to saturated fatty acid levels. High δ-15N values of the Antarctic eelpout reflect the high trophic level of this scavenger in the Weddell Sea food web. Stable carbon values suggest that lipid-enriched prey forms a major part of its diet. The strategy to accumulate storage lipids in the cold is interpreted to be adaptive behaviour at colder temperatures and during periods of irregular, pulsed food supply.
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Abbreviations
- CHOL:
-
Cholesterol
- DAGE:
-
Diacylglycerol ethers
- FFA:
-
Free fatty acids
- MUFA:
-
Monounsaturated fatty acids
- PL:
-
Polar lipids
- PUFA:
-
Polyunsaturated fatty acids
- SFA:
-
Saturated fatty acids
- TAG:
-
Triacylglycerols
- UFA:
-
Unsaturated fatty acids
- WE:
-
Wax esters
References
Ackman RG (1989) Marine biogenic lipids, vol 1. CRC Press, Boca Raton
Bock C, Sartoris F, Wittig R-M, Pörtner H-O (2001) Temperature-dependent pH regulation in stenothermal Antarctic and eurythermal temperate eelpout (Zoarcidae): an in-vivo NMR study. Polar Biol 24:869–874
Brett JR, Groves TD (1979) Physiological energetics. Fish Physiol 8:279–352
Brodte E (2001) Wachstum und Fruchtbarkeit der Aalmutterarten Zoarces viviparus (Linne) und Pachycara brachycephalum (Pappenheim) aus unterschiedlichen klimatischen Regionen. PhD thesis, Universität Bremen, Bremen, Germany
Brodte E, Knust R, Pörtner HO, Arntz WE (2006a) The biology of the Antarctic eelpout Pachycara brachycephalum. Deep-Sea Res II 53:1131–1140
Brodte E, Knust R, Pörtner H-O (2006b) Temperature dependent energy allocation to growth in Antarctic and boreal eelpout (Zoarcidae), Polar Biol 30:95–107
Burns JM, Trumble SJ, Castellini MA, Testa JW (1998) The diet of Weddell seals in McMurdo Sound, Antarctica as determined from scat collections and stable isotope analysis. Polar Biol 19:272–282
Crockett EL, Sidell BD (1990) Some pathways of energy metabolism are cold adapted in Antarctic fishes. Physiol Zool 63:472–488
Desaulniers N, Moerland TS, Sidell BD (1996) High lipid content enhances rate of oxygen diffusion through fish skeletal muscle. Am J Physiol 271:R42–R47
Eastman JT, DeVries AL (1982) Buoyancy studies of notothenioid fishes in McMurdo Sound, Antarctica. Copeia 2:385–393
Egginton S, Sidell BD (1989) Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am J Physiol 256:R1–R9
Farkas T, Csengeri I, Majoros F, Olah J (1980) Metabolism of fatty acids in fish 3. combined effect of environmental temperature and diet on formation and deposition of fatty acids in the carp, Cyprinus carpio Linnaeus 1758. Aquaculture 20:29–40
Farkas T, Dey I, Buda C, Halver JE (1994) Role of phospholipid molecular species in maintaining lipid membrane structure in response to temperature. Biophys Chem 50:147–155
Farkas T, Fodor E, Kitajka K, Halver JE (2001) Response of fish membranes to environmental temperature. Aquac Res 32:645–655
Folch J, Lees M, Stanley GHS (1957) A simple method for isolation and purification of total lipid from animal tissue. J Biol Chem 266:467–509
Fonds M, Jaworski A, Iedema A, Puyl PVD (1989) Metabolism, food consumption, growth and food conversion of shorthorn sculpin (Myoxocephalus scorpius) and eelpout (Zoarces viviparus). ICES Council Meeting Papers:G:31
Fraser AJ, Sargent JR, Gamble JC, MacLachlan P (1987) Lipid class and fatty acid composition as indicators of the nutritional condition of larval Atlantic herring. Am Fish Soc Symp Ser 2:129–143
Gnaiger E, Bitterlich G (1984) Proximate biochemical composition and caloric content calculated from elemental CHN analysis: a stoichiometric concept. Oecologia 62:289–298
Grove TJ, Sidell BD (2004) Fatty acyl CoA synthetase from Antarctic notothenioid fishes may influence substrate specificity of fat oxidation. Comp Biochem Physiol B 139:53–63
Guderley H, St. Pierre J, Couture P, Hulbert AJ (1997) Plasticity of properties of mitochondria from rainbow trout red muscle with seasonal acclimatization. Fish Physiol Biochem 16:531–541
Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42
Houlihan DF, Hall SJ, Gray C, Noble BS (1988) Growth rates and protein turnover in Atlantic cod, Gadus morhua. Can J Fish Aquatic Sci 45:951–964
Hubold G (1985) Krill and fishes in the Antarctic ecosystems. J IOUSP 3:2–4
Jacob U, Mintenbeck K, Brey T, Knust R, Beyer K (2005) Stable isotope food web studies: a case for standardized sample treatment. Mar Ecol Prog Ser 287:251–253
Jangaard PM, Ackman RG, Sipos JC (1967) Seasonal changes in fatty acid composition of cod liver, flesh, roe, and milt lipids. J Fish Res Board Can 24:613–627
Jobling M, Bendiksen AA (2003) Dietary lipids and temperature interact to influence tissue fatty acid compositions of Atlantic salmon, Salmo salar L., parr. Aquac Res 34:1423–1441
Kattner G, Fricke HSG (1986) Simple gas-liquid chromatographic method for simultaneous determination of fatty acids and alcohols in wax esters of marine organisms. J Chromatogr 361:263–268
Larsen DA, Beckman BR, Dickhoff WW (2001) The effect of low temperature and fasting during the winter on growth and smoltification of Coho Salmon. North Am J Aquac 63:1–10
Lipski J (2001) AMLR 2000/2001 Field season report – objectives, accomplishment and tentative conclusions. NOAA–TM–NMFS–SWFSC-314, Southwest Fisheries Science Center, Antarctic Ecosystems Research Division, La Jolla, CA
Mark FC, Hirse T, Pörtner H-O (2005) Thermal sensitivity of cellular energy budgets in Antarctic fish hepatocytes. Polar Biol 28:805–814
Marsh JB, Weinstein DB (1966) Simple charring method for determination of lipids. J Lipid Res 7:574–576
North AW (1998) Growth of young fish during winter and summer at South Georgia. Polar Biol 19:198–205
Norton EC, Macfarlane RB, Mohr MS (2001) Lipid class dynamics during development in early life stages of shortbelly rockfish and their application to condition assessment. J Fish Biol 58:1010–1024
Nyssen F, Brey T, Lepoint G, Bouquegneau JM, DeBroyer C, Dauby P (2002) A stable isotope approach to the eastern Weddell Sea trophic web: focus on benthic amphipods. Polar Biol 25:280–287
Nyssen F, Brey T, Dauby P, Graeve M (2005) Trophic position of Antarctic amphipods – enhanced analysis by a 2-dimensional biomarker assay. Mar Ecol Prog Ser 300:135–145
Olsen RE, Henderson RJ (1989) The rapid analysis of neutral and polar marine lipids using double-development HPTLC and scanning densitometry. J Exp Mar Biol Ecol 129(2):189–197
Pekkarinen M (1980) Seasonal variations in lipid content and fatty acids in the liver, muscle and gonads of the eel-pout, Zoarces viviparus (Teleostei) in brackish water. Ann Zool Fenn 17:249–254
Pörtner HO (2002) Physiological basis of temperature-dependent biogeography: trade-offs in muscle design and performance in polar ectotherms. J Exp Biol 205:2217–2230
Pörtner HO (2004) Climate variability and the energetic pathways of evolution: the origin of endothermy in mammals and birds. Physiol Biochem Zool 77:959–981
Pörtner HO, Lucassen M, Storch D (2005) Metabolic biochemistry: its role in thermal tolerance and in the capacities of physiological and ecological function. In: Steffensen JF, Farrell AP (guest eds), Randall DR, Farrell AP (series eds) The physiology of polar fishes. Fish Physiol 22:79–154
Sidell BD (1991) Physiological roles of high lipid content in tissues of Antarctic fish species. In: Di Prisco G, Maresca B, Tota B (eds) Biology of Antarctic fish. Springer, Berlin, pp 220–231
Sidell BD, Hazel JR (2002) Triacylglycerol lipase activities in tissue of Antarctic fishes. Polar Biol 25:517–522
Ulleweit J (1995) Zur Ökologie zweier Standfischarten, der Aalmutter (Zoarces viviparus, L.) und des Butterfisches ( Pholis gunnellus, L.) aus dem Niedersächsischen Wattenmeer. PhD thesis, Universität Bremen, Bremen, Germany
Urich K (1990) Vergleichende Biochemie der Tiere. Gustav Fischer Verlag, Stuttgart
Wöhrmann APA (1998) Aspects of eco-physiological adaptations in Antarctic fish. In: Di Prisco G, Pisano E, Clarke A (eds) Fishes of Antarctica – a biological overview. Sprinter, Milan, pp 119–128
Acknowledgements
The authors would like to thank Marco Böer for his support in the lipid class and fatty acid analyses and Dr. Ulrich Struck (GeoBioCenter, München) for analysing the stable isotope samples.
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Brodte, E., Graeve, M., Jacob, U. et al. Temperature-dependent lipid levels and components in polar and temperate eelpout (Zoarcidae). Fish Physiol Biochem 34, 261–274 (2008). https://doi.org/10.1007/s10695-007-9185-y
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DOI: https://doi.org/10.1007/s10695-007-9185-y