Marine Biology

, Volume 157, Issue 6, pp 1367–1384 | Cite as

Lipid composition and partitioning of deepwater chondrichthyans: inferences of feeding ecology and distribution

  • Heidi Pethybridge
  • Ross Daley
  • Patti Virtue
  • Peter Nichols
Original Paper


The composition of lipids and fatty acids was determined for the livers, muscle, pancreas, kidney and stomach fluids of deepwater chondrichthyan species (including 11 squaliformes, 3 chimaeriformes, 1 hexanchiforme and 3 carcharhiniformes) caught as bycatch from continental waters off south-eastern Australia. The lipid class, fatty acid and fatty alcohol composition differed markedly in each tissue and in each species. The lipid and fatty acid composition of large, lipid-rich (38–70% wet weight, ww) livers demonstrated the multifunctional role of this organ in: lipid distribution, storage and biosynthesis, and buoyancy regulation. In the liver, the importance of certain lipids (including squalene, diacylglyceryl ethers, triacylglycerols and to a lesser extent wax esters) as mediators of buoyancy varied according to lifestyle and habitat. Less variability was observed in the muscle profiles, characterized by low lipid content (<1.0% ww) and high relative levels of polar lipids (>70%). The lipid and fatty acid profiles of the kidney and pancreas showed the highest intraspecific variability, suggesting these organs also have complex roles in lipid storage and metabolism. Overall intra- and interspecific differences in the tissue fatty acid profiles could be related to differences in a number of factors including phylogeny, habitat (depth), buoyancy regulation and diet and presumably also reflect different ecological roles. The lipid and fatty acid profiles are the first published for Rhinochimaera pacifica, Chimaera lignaria and Figaro boardmani and the first to demonstrate interspecific variation in lipid profiles of various tissues of deepwater chondrichthyans. The application of multivariate analysis to lipid class and fatty acid tissue profiles in chondrichthyans inferred dietary differences and metabolic preferences between species and habitats. These results have important implications for the future use of fatty acids as dietary tracers in chondrichthyan research.


  1. Bakes MJ, Nichols PD (1995) Lipid, fatty acid and squalene composition of liver oil from 6 species of deep-sea sharks collected in southern Australian waters. Comp Biochem Physiol B 110(1):267–275CrossRefGoogle Scholar
  2. Ballantyne J (1997) Jaws: the inside story. The metabolism of Elasmobranch fishes. Comp Biochem Physiol B 118(4):703–742CrossRefGoogle Scholar
  3. Bligh EG, Dyer WG (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol B 37:911–917Google Scholar
  4. Body DR, Johnson CB, Shaw GJ (1985) The monounsaturated acyl-and alkyl-moieties of wax esters and their distribution in commercial orange roughy (Hoplostethus atlanticus) oil. Lipids 20:680–684CrossRefPubMedGoogle Scholar
  5. Böer M, Gannefors C, Kattner G, Graeve M, Hop H, Falk-Petersen S (2005) The Arctic pteropod Clione limacina: seasonal lipid dynamics and life strategy. Mar Biol 147:707–717CrossRefGoogle Scholar
  6. Dahlqvist A, Ståhl U, Lenman M, Banas A, Lee M, Sandager L, Ronne H, Stymne S (2000) Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc Natl Acad Sci USA 97(12):6487–6492CrossRefPubMedGoogle Scholar
  7. Daley RK, Stevens JD, Last PR, Yearsley GK (2002a) Field guide to Australian sharks and rays. CSIRO, VictoriaGoogle Scholar
  8. Daley R, Stevens J, Graham A (2002b) Catch analysis and productivity of the deepwater dogfish resources in southern Australia. FRDC Project 1998/108. CSIRO Marine Research, AustraliaGoogle Scholar
  9. Dalsgaard J, St. John M, Kattner G, Mueller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340CrossRefPubMedGoogle Scholar
  10. Deprez PP, Volkman JK, Davenport SR (1990) Squalene content and neutral lipid composition of livers from deep-sea sharks in Tasmanian waters. Aust J Mar Freshw Res 41:375–387CrossRefGoogle Scholar
  11. Didier DA (2002) Chimaeras. In: Carpenter KE (ed) The living marine resources of the Western Central Atlantic. FAO, Rome, pp 1–600Google Scholar
  12. Didier DA, Last PR, White WT (2008) Three new species of the genus Chimaera Linnaeus (Chimaeriformes: Chimaeridae) from Australia. In: Last PR, White WT, Pogonoski JJ (eds) Descriptions of new Australian chondrichthyans. CSIRO Marine and Atmospheric Research Paper no. 22Google Scholar
  13. Drazen JC (2002) A seasonal analysis of the nutritional condition of deep-sea macrourid fishes in the north-east Pacific. Fish Biol 60:1280–1295CrossRefGoogle Scholar
  14. Drazen JC (2007) Depth related trends in proximate composition of demersal fishes in the eastern North Pacific. Deep Sea Res I 54:203–219CrossRefGoogle Scholar
  15. Drazen JC, Seibel BA (2007) Depth-related trends in metabolism of benthic and benthopelagic deep-sea fishes. Limnol Oceanogr 52(5):2306–2316Google Scholar
  16. Drazen JC, Phleger CF, Guest MA, Nichols PD (2009) Lipid composition and diet inferences in abyssal macrourids of the eastern North Pacific. Mar Ecol Prog Ser 387:1–14CrossRefGoogle Scholar
  17. Ebert DA (1991) Observations on the predatory behaviour of the sevengill shark Notorynchus cepedianus. S Afr J Mar Sci 11:455–465Google Scholar
  18. Farquhar JW (1962) Identification and gas-liquid chromatographic behaviour of plasmalogen aldehydes and their acetal, alcohol, and acetylated alcohol derivatives. J Lipid Res 3:21–30Google Scholar
  19. Friedrich C, Hagen W (1994) Lipid contents of five species of notothenioid fish from high-Antarctic waters and ecological implications. Polar Biol 14:359–369CrossRefGoogle Scholar
  20. Gage JD, Tyler PA (1991) Deep-sea biology: a natural history of organisms at the deep-sea floor. Cambridge University Press, CambridgeGoogle Scholar
  21. Hayashi K, Kishimura H (2002) Amount and composition of diacyl glyceryl ethers in various tissue lipids of the deep-sea squid Berryteuthis magister. J Oleo Sci 51:523–530Google Scholar
  22. Hayashi K, Takagi T (1980) Composition of diacyl glyceryl ethers in the liver lipids of ratfish, Hydrolagus novaezealandiae. Bull Jpn Soc Sci Fish 46:855–861Google Scholar
  23. Hayashi K, Takagi T (1981) Distribution of squalene and diacyl glyceryl ethers in the different tissues of deep-sea shark, Dalatias licha. Bull Jpn Soc Sci Fish 47:281–288Google Scholar
  24. Henderson RJ, Toucher DR (1987) The lipid composition and biochemistry of freshwater fish. Prog Lipid Res 26:281–347CrossRefPubMedGoogle Scholar
  25. Iverson SJ, Frost KJ, Lowry LF (1997) Fatty acid signatures reveal fine scale structure of foraging distribution of harbour seals and their prey in Prince William Sound, Alaska. Mar Ecol Prog Ser 151:255–271CrossRefGoogle Scholar
  26. Iverson SJ, Field C, Bowen WD, Blanchard W (2004) Quantitative fatty acid signature analysis: a new method of estimating predator diets. Ecol Monogr 74(2):221–235CrossRefGoogle Scholar
  27. Jayasinghe C, Gotoha N, Wadaa S (2003) Variation in lipid classes and fatty acid composition of salmon shark (Lamna ditropis) liver with season and gender. Comp Biochem Physiol B 134:287–295CrossRefGoogle Scholar
  28. Jeckel WH, Aizpun de Moreno JE, Moreno VG (1989) Biochemical composition, lipid classes and fatty acids in the ovary of the shrimp Pleoticus muelleri Bate. Comp Biochem Physiol B 92(2):271–276CrossRefGoogle Scholar
  29. Last PR, Stevens JD (2009) Sharks and rays of Australia, 2nd edn. CSIRO, Melbourne, pp 1–656Google Scholar
  30. Malins DC, Barone A (1970) Glyceryl ether metabolism: regulation of buoyancy in dogfish Squalus acanthias. Science 167:79–80CrossRefPubMedGoogle Scholar
  31. Moyes LT, Buck LT, Hochachka PW (1990) Mitochondrial and peroxisomal fatty acid oxidation in elasmobranchs. Am J Physiol 258:756–762Google Scholar
  32. Nevenzel JC (1989) Biogenic hydrocarbons of marine organisms. In: Ackman RG (ed) Marine biogenic lipids, fats, and oils, vol 1. CRC Press, Florida, pp 3–71Google Scholar
  33. Nichols PD, Nichols DS, Bakes MJ (1994) Recent developments in marine oil products in Australia. INFORM 5:254–261Google Scholar
  34. Nichols PD, Bakes MJ, Elliott NG (1998a) Oils rich in docosahexaenoic acid in livers of sharks from temperate Australian waters. Aust J Mar Freshw Res 49(7):763–767CrossRefGoogle Scholar
  35. Nichols PD, Virtue P, Mooney BD, Elliott NG, Yearsley GK (1998b) Seafood the good food. FRDC Project 95/122. CSIRO, HobartGoogle Scholar
  36. Økland IS, Stoknes IS, Remme JF, Kjerstad M, Synnes M (2005) Proximate composition, fatty acid and lipid class composition of the muscle from deep-sea teleost and elasmobranchs. Comp Biochem Physiol B 140:437–443CrossRefPubMedGoogle Scholar
  37. Phillips KL, Nichols PD, Jackson GD (2003) Dietary variation of the squid Moroteuthis ingens at four sites in the Southern Ocean: stomach contents, lipid and fatty acid profiles. J Mar Biol Assoc UK 83:523–534CrossRefGoogle Scholar
  38. Phleger CF (1991) Biochemical aspects of buoyancy in fishes. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes. Elsevier, New York, pp 209–247Google Scholar
  39. Phleger CF (1998) Buoyancy in marine fishes: direct and indirect role of lipids. Am Zool 38:321–330Google Scholar
  40. Phleger CF, Nichols PD, Virtue P (1997) The lipid, fatty acid and fatty alcohol composition of the myctophid fish Electrona antarctica: high level of wax ester and food-chain implications. Antarct Sci 9:258–265CrossRefGoogle Scholar
  41. Phleger CF, Nichols PD, Erb E, Williams R (1999) Lipids of the notothenioid fishes Trematomus spp. and Pagothenia borchgrevinki from east Antarctica. Polar Biol 22:241–247CrossRefGoogle Scholar
  42. Rao CV, Newmark HL, Reddy BS (1998) Chemopreventive effect of squalene on colon cancer. Carcinogenesis 19:287–290CrossRefPubMedGoogle Scholar
  43. Remme JF, Larssen WE, Bruheim I, Saebo PC, Saebo A, Stoknes IS (2006) Lipid content and fatty acid distribution in tissues from Portugal dogfish, leafscale gulper shark and black dogfish. Comp Biochem Physiol B 143(4):459–464CrossRefPubMedGoogle Scholar
  44. Sargent JR (1989) Ether-linked glycerides in marine animals. In: Ackman RG (ed) Marine biogenic lipids, fats, and oils, vol 1. CRC Press, Florida, pp 175–197Google Scholar
  45. Sargent JR, Tocher DR, Bell JG (2002) The lipids. In: Halver HE, Hardy RW (eds) Fish nutrition, 3rd edn. Elsevier, New York, pp 181–257Google Scholar
  46. Schaufler L, Heintz R, Sigler M, Hulbert L (2005) Fatty acid composition of sleeper shark (Somniosus pacificus) liver and muscle reveals nutritional dependence on planktivores. ICES CM 5Google Scholar
  47. Sheridan MA (1994) Regulation of lipid metabolism in poikilothermic vertebrates. Comp Biochem Physiol B 107(4):495–508CrossRefGoogle Scholar
  48. Speers-Roesch B, Robinson JW, Ballantyne JS (2006) Metabolic organization of the spotted ratfish, Hydrolagus colliei (Holocephali: Chimaeriformes): insight into the evolution of energy metabolism in the chondrichthyan Fishes. J Exp Zool 305:631–644CrossRefGoogle Scholar
  49. Stowasser G, McAllen R, Pierce JG, Collins MA, Moffat CF, Priede IG, Pond DW (2009) Trophic position of deep-sea fish—assessment through fatty acid and stable isotope analyses. Deep Sea Res I: Oceanogr Res 56(5):812–826CrossRefGoogle Scholar
  50. Volkman JK, Nichols PD (1991) Application of thin layer chromatography-flame ionization detection to the analysis of lipids and pollutants in marine environmental samples. J Planar Chromatogr 4:19–26Google Scholar
  51. Wetherbee BM, Nichols PD (2000) Lipid composition of the liver oil of deep-sea sharks from the Chatham Rise, New Zealand. Comp Biochem Physiol B 125:511–521CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Heidi Pethybridge
    • 1
    • 2
  • Ross Daley
    • 2
  • Patti Virtue
    • 1
  • Peter Nichols
    • 1
    • 2
  1. 1.IMASUniversity of TasmaniaHobartAustralia
  2. 2.CSIRO Marine and Atmospheric ResearchHobartAustralia

Personalised recommendations