Advertisement

Fish Physiology and Biochemistry

, Volume 34, Issue 3, pp 261–274 | Cite as

Temperature-dependent lipid levels and components in polar and temperate eelpout (Zoarcidae)

  • Eva Brodte
  • M. Graeve
  • U. Jacob
  • R. Knust
  • H.-O. Pörtner
Article

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.

Keywords

Antarctic Boreal Eurythermy Fatty acids Fishes Lipid classes Stenothermy 

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

Notes

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.

References

  1. Ackman RG (1989) Marine biogenic lipids, vol 1. CRC Press, Boca RatonGoogle Scholar
  2. 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 24:869–874CrossRefGoogle Scholar
  3. Brett JR, Groves TD (1979) Physiological energetics. Fish Physiol 8:279–352CrossRefGoogle Scholar
  4. Brodte E (2001) Wachstum und Fruchtbarkeit der Aalmutterarten Zoarces viviparus (Linne) und Pachycara brachycephalum (Pappenheim) aus unterschiedlichen klimatischen Regionen. PhD thesis, Universität Bremen, Bremen, GermanyGoogle Scholar
  5. Brodte E, Knust R, Pörtner HO, Arntz WE (2006a) The biology of the Antarctic eelpout Pachycara brachycephalum. Deep-Sea Res II 53:1131–1140Google Scholar
  6. Brodte E, Knust R, Pörtner H-O (2006b) Temperature dependent energy allocation to growth in Antarctic and boreal eelpout (Zoarcidae), Polar Biol 30:95–107Google Scholar
  7. 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 19:272–282CrossRefGoogle Scholar
  8. Crockett EL, Sidell BD (1990) Some pathways of energy metabolism are cold adapted in Antarctic fishes. Physiol Zool 63:472–488Google Scholar
  9. Desaulniers N, Moerland TS, Sidell BD (1996) High lipid content enhances rate of oxygen diffusion through fish skeletal muscle. Am J Physiol 271:R42–R47PubMedGoogle Scholar
  10. Eastman JT, DeVries AL (1982) Buoyancy studies of notothenioid fishes in McMurdo Sound, Antarctica. Copeia 2:385–393CrossRefGoogle Scholar
  11. Egginton S, Sidell BD (1989) Thermal acclimation induces adaptive changes in subcellular structure of fish skeletal muscle. Am J Physiol 256:R1–R9PubMedGoogle Scholar
  12. 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 20:29–40CrossRefGoogle Scholar
  13. 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 50:147–155PubMedCrossRefGoogle Scholar
  14. Farkas T, Fodor E, Kitajka K, Halver JE (2001) Response of fish membranes to environmental temperature. Aquac Res 32:645–655CrossRefGoogle Scholar
  15. Folch J, Lees M, Stanley GHS (1957) A simple method for isolation and purification of total lipid from animal tissue. J Biol Chem 266:467–509Google Scholar
  16. 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:31Google Scholar
  17. 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 2:129–143Google Scholar
  18. Gnaiger E, Bitterlich G (1984) Proximate biochemical composition and caloric content calculated from elemental CHN analysis: a stoichiometric concept. Oecologia 62:289–298CrossRefGoogle Scholar
  19. Grove TJ, Sidell BD (2004) Fatty acyl CoA synthetase from Antarctic notothenioid fishes may influence substrate specificity of fat oxidation. Comp Biochem Physiol B 139:53–63PubMedCrossRefGoogle Scholar
  20. 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 16:531–541CrossRefGoogle Scholar
  21. Hazel JR (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annu Rev Physiol 57:19–42PubMedGoogle Scholar
  22. Houlihan DF, Hall SJ, Gray C, Noble BS (1988) Growth rates and protein turnover in Atlantic cod, Gadus morhua. Can J Fish Aquatic Sci 45:951–964CrossRefGoogle Scholar
  23. Hubold G (1985) Krill and fishes in the Antarctic ecosystems. J IOUSP 3:2–4Google Scholar
  24. 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 287:251–253CrossRefGoogle Scholar
  25. 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 24:613–627Google Scholar
  26. 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 34:1423–1441CrossRefGoogle Scholar
  27. 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 361:263–268CrossRefGoogle Scholar
  28. 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 63:1–10CrossRefGoogle Scholar
  29. 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, CAGoogle Scholar
  30. Mark FC, Hirse T, Pörtner H-O (2005) Thermal sensitivity of cellular energy budgets in Antarctic fish hepatocytes. Polar Biol 28:805–814CrossRefGoogle Scholar
  31. Marsh JB, Weinstein DB (1966) Simple charring method for determination of lipids. J Lipid Res 7:574–576PubMedGoogle Scholar
  32. North AW (1998) Growth of young fish during winter and summer at South Georgia. Polar Biol 19:198–205CrossRefGoogle Scholar
  33. 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 58:1010–1024CrossRefGoogle Scholar
  34. 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 25:280–287Google Scholar
  35. 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 300:135–145CrossRefGoogle Scholar
  36. 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):189–197CrossRefGoogle Scholar
  37. 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 17:249–254Google Scholar
  38. Pörtner HO (2002) Physiological basis of temperature-dependent biogeography: trade-offs in muscle design and performance in polar ectotherms. J Exp Biol 205:2217–2230PubMedGoogle Scholar
  39. Pörtner HO (2004) Climate variability and the energetic pathways of evolution: the origin of endothermy in mammals and birds. Physiol Biochem Zool 77:959–981PubMedCrossRefGoogle Scholar
  40. 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 Google Scholar
  41. 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 220–231Google Scholar
  42. Sidell BD, Hazel JR (2002) Triacylglycerol lipase activities in tissue of Antarctic fishes. Polar Biol 25:517–522CrossRefGoogle Scholar
  43. 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, GermanyGoogle Scholar
  44. Urich K (1990) Vergleichende Biochemie der Tiere. Gustav Fischer Verlag, StuttgartGoogle Scholar
  45. 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 119–128Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Eva Brodte
    • 1
  • M. Graeve
    • 2
  • U. Jacob
    • 3
  • R. Knust
    • 1
  • H.-O. Pörtner
    • 1
  1. 1.Physiology of Marine AnimalsAlfred–Wegener-Institute for Polar and Marine ResearchBremerhavenGermany
  2. 2.Chemical EcologyAlfred–Wegener-Institute for Polar- and Marine ResearchBremerhavenGermany
  3. 3.Animal EcologyAlfred–Wegener-Institute for Polar- and Marine ResearchBremerhavenGermany

Personalised recommendations