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High concentrations of isovaleric acid in the fats of odontocetes: variation and patterns of accumulation in blubber vs. stability in the melon

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Abstract

Isovaleric acid (iso5:0) is an unusual fatty acid that is important for echolocation and hearing in acoustic tissues of some odontocetes, but its functional significance in blubber is unknown. We examined patterns of accumulation of this compound in blubber in 30 species of odontocetes (n=299). Iso5:0 concentrations in blubber varied with phylogeny, ontogeny and body topography. Iso5:0 accumulated in greater quantities in superficial/outer blubber than in deep/inner blubber. In the outer blubber of northern right whale and Hector's dolphins, iso5:0 accounted for one-third to one-half of all fatty acids. Total blubber burden of iso5:0 in harbour porpoises represented up to 15 times the amount deposited in the melon. The composition of the melon does not change during starvation in harbour porpoises, supporting the hypothesis that lipids in melon are conserved for a specific function. Some odontocetes continually deposit iso5:0 in blubber after levels in melon have reached asymptotic levels, suggesting independent control of iso5:0 synthesis and storage in these compartments. Dolphins and porpoises inhabiting cold waters possess higher concentrations of iso5:0 in their outer blubber layers than species from warmer regions. We propose that this relationship represents an adaptive secondary role for iso5:0 in maintaining blubber flexibility in cold environments.

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Abbreviations

iso5:0:

isovaleric acid

GC:

gas chromatograph

GLC:

gas-liquid chromatography

IUPAC:

International Union of Pure and Applied Chemistry

IVA:

isovaleric academia

IVD:

isovaleryl-CoA dehydrogenase

mol%:

molar percentage of total fatty acids

PUFA:

polyunsaturated fatty acid

SE:

standard error

wt%:

weight percentage of total fatty acids

References

  • Ackman RG, Sipos JC, Eaton CA, Hilaman BL, Litchfield C (1973) Molecular species of wax esters in jaw fat of Atlantic bottlenose dolphin, Tursiops truncatus. Lipids 8:661–667

    CAS  PubMed  Google Scholar 

  • Ackman RG, Eaton CA, Kinneman J, Litchfield C (1975) Lipids of the freshwater dolphin Sotalia fluviatilis: comparison of odontocete bioacoustic lipids and habitat. Lipids 10:44–49

    CAS  PubMed  Google Scholar 

  • Ando T, Nyhan WL, Bachmann C, Rasmussen K, Scott R, Smith E (1973) Isovaleric acidemia: identification of isovalerate, isovalerylglycine, and 3-hydroxyisovalerate in urine of a patient previously reported as having butyric and hexanoic acidemia. J Pediatrics 82:243–248

    CAS  Google Scholar 

  • Bjørge A, Hohn AA, Lockyer C, Schweder T (1995) Summary report from the harbour porpoise age determination workshop, Oslo, 21–23 May 1990. Rep Int Whal Commn Special Issue16:477–545

    Google Scholar 

  • Borobia M, Gearing PJ, Simard Y, Gearing JN, Béland P (1995) Blubber fatty acids of finback and humpback whales from the Gulf of St. Lawrence. Mar Biol 122:341–353

    CAS  Google Scholar 

  • Budd MA, Tanaka K, Holmes LB, Efron ML, Crawford JD, Isselbacher KJ (1967) Isovaleric acidemia: clinical features of a new genetic defect of leucine metabolism. New Eng J Med 277:321–327

    CAS  PubMed  Google Scholar 

  • Cranford TW (2000) In search of impulse sound sources in odontocetes. In: Au WW, Popper AN, Fay RR (eds) Hearing in whales and dolphins. Springer, Berlin Heidelberg New York, pp 109–155

  • Cranford TW, Amundin M, Norris KS (1996) Functional morphology and homology in the odontocete nasal complex: implications for sound generation. J Morph 228:223–285

    CAS  PubMed  Google Scholar 

  • Doidge DW (1990) Integumentary heat loss and blubber distribution in the beluga, Delphinapterus leucas, with comparisons to the narwhal, Monodon monoceros. In: Smith TG, St. Aubin DJ, Geraci JR (eds) Advances in research on the beluga whale, Delphinapterus leucas. Can Bull Fish Aquat Sci 224:129–140

    Google Scholar 

  • Efron ML (1967) Isovaleric acidemia. Am J Dis Children 113:74–75

    CAS  Google Scholar 

  • Elsner R (1999) Living in water: solutions to physiological problems. In: Reynolds JE, Rommel SA (eds) Biology of marine mammals. Smithsonian Institution, Washington, pp 73–116

  • Evans K, Kemper C, Hill M (2001) First records of the spectacled porpoise Phocoena dioptrica in continental Australian waters. Mar Mamm Sci 17:161–169

    Google Scholar 

  • Fasman GD (1975) Handbook of biochemistry and molecular biology, 3rd edn. CRC, Cleveland

  • Folch J, Lees M, Sloan-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    Google Scholar 

  • Grompone MA, Sienra B, Quilez JL (1990) Fatty acid composition of fats from the Uruguayan fur seal (Arctocephalus australis Zimmerman). Mar Mamm Sci 6:48–53

    Google Scholar 

  • Iverson SJ (1993) Milk secretion in marine mammals in relation to foraging: can milk fatty acids predict diet? Symp Zool Soc Lond 66:263–291

    Google Scholar 

  • Iverson, SJ (2002) Blubber. In: Perrin WF, Wursig B, Thewissen HGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, pp 107–112

  • Iverson SJ, Frost KJ, Lowry LF (1997) Fatty acid signatures reveal fine scale structure of foraging distribution of harbor seals and their prey in Prince William Sound, Alaska. Mar Ecol Prog Ser 151:255–271

    CAS  Google Scholar 

  • Iverson SJ, McDonald JE, Smith LH (2001) Changes in diet of free-ranging black bears in years of contrasting food availability revealed through milk fatty acids. Can J Zool 79:2268–2279

    Article  Google Scholar 

  • Kastelein RA, van Battum R (1990) The relationship between body weight and morphological measurements in harbour porpoises (Phocoena phocoena) from the North Sea. Aquat Mamm 16:48–52

    Google Scholar 

  • Koopman HN (1998) Topographical distribution of the blubber of harbor porpoises (Phocoena phocoena). J Mamm 79:260–270

    Google Scholar 

  • Koopman HN (2001) The structure and function of the blubber of odontocetes. PhD, Duke University, Durham

  • Koopman HN, Iverson SJ, Gaskin DE (1996) Stratification and age-related differences in blubber fatty acids of the male harbour porpoise (Phocoena phocoena). J Comp Phys B 165:628–639

    CAS  Google Scholar 

  • Leatherwood S, Reeves RR (1983) The Sierra Club handbook of whales and dolphins. Sierra Club, San Francisco

  • LeDuc RG, Perrin WF, Dizon AE (1999) Phylogenetic relationships among the delphinid cetaceans based on full cytochrome b sequences. Mar Mamm Sci 15:619–648

    Google Scholar 

  • Litchfield C, Greenberg AJ (1974) Comparative lipid patterns in the melon fats of dolphins, porpoises and toothed whales. Comp Biochem Physiol B 47:401–407

    Article  CAS  Google Scholar 

  • Litchfield C, Ackman RG, Sipos JC, Eaton CA (1971) Isovaleroyl triglycerides from the blubber and melon oils of the beluga (Delphinapterus leucas). Lipids 6:674–681

    CAS  PubMed  Google Scholar 

  • Litchfield C, Karol R, Greenberg AJ (1973) Compositional topography of melon lipids in the Atlantic bottlenosed dolphin Tursiops truncatus: implications for echolocation. Mar Biol 23:165–169

    CAS  Google Scholar 

  • Litchfield C, Greenberg AJ, Caldwell DK, Caldwell MC, Sipos JC, Ackman RG (1975) Comparative lipid patterns in acoustical and nonacoustical fatty tissues of dolphins, porpoises and toothed whales. Comp Biochem Physiol B 50:591–597

    Article  CAS  PubMed  Google Scholar 

  • Litchfield C, Karol R, Mullen ME, Dilger JP, Lüthi B (1979) Physical factors influencing refraction of the echolocative sound beam in delphinid cetaceans. Mar Biol 52:285–290

    Google Scholar 

  • Lockyer CH, McConnell LC, Waters TD (1984) The biochemical composition of fin whale blubber. Can J Zool 62:2553–2562

    CAS  Google Scholar 

  • Lovern JA (1934) Liv. fat metabolism in fishes, III: selective formation of fat deposits. Biochem J 28:394–402

    CAS  Google Scholar 

  • Malins DC, Varanasi U (1975) Cetacean biosonar, part II: the biochemistry of lipids in acoustic tissues. In: Malins DC, Sargent JR (eds) Biochemical and biophysical perspectives in marine biology, vol. 2. Academic Press, London, pp 237–290

  • Malins DC, Robisch PA, Varanasi U (1972a) Biosynthesis of triacylglycerols containing isovaleric acid. Biochem BioPhys Res Commun 48:314–319

    CAS  PubMed  Google Scholar 

  • Malins DC, Varanasi U, Wekell JC (1972b) Lipid biosynthesis and increase in isovaleric acid of plasma. Science 176:1357

    PubMed  Google Scholar 

  • McLellan WA, Koopman HN, Rommel SA, Read AJ, Potter CW, Nicolas JR, Westgate AJ, Pabst DA (2002) Ontogenetic allometry and body composition of harbour porpoises (Phocoena phocoena L.) from the western north Atlantic. J Zool (Lond) 257:457–472

    Google Scholar 

  • Morii H, Kaneda T (1982) Biosynthesis of branched-chain fatty acids from branched-chain amino acids in subcutaneous tissue of the marine little toothed whale, Stenella caeruleo-alba. Comp Biochem Physiol B 71:357–365

    Article  CAS  PubMed  Google Scholar 

  • Morris RJ (1973) The lipid structure of the spermaceti organ of the sperm whale (Physeter catodon). Deep-Sea Res 20:911–916

    CAS  Google Scholar 

  • Morris RJ (1975) Further studies into the lipid structure of the spermaceti organ of the sperm whale (Physeter catodon). Deep-Sea Res 22:483–489

    CAS  Google Scholar 

  • Nyhan WL (1984) Abnormalities in amino acid metabolism in clinical medicine. Appleton-Century-Crofts, Norwalk

  • Pabst DA (1996) Springs in swimming animals. Am Zool 36:723–735

    Google Scholar 

  • Pabst DA, Rommel SA, McLellan WA (1999) The functional morphology of marine mammals. In: Reynolds JE, Rommel SA (eds) Biology of marine mammals. Smithsonian Institution, Washington,pp 15–72

  • Patton JS (1981) Gastrointestinal lipid digestion. In: Johnson LR (ed) Physiology of the gastrointestinal tract. Raven, New York, pp 1123–1146

  • Pond CM, Mattacks CA, Colby RH, Ramsay MA (1992) The anatomy, chemical composition, and metabolism of adipose tissue in wild polar bears (Ursus maritimus). Can J Zool 70:326–341

    CAS  Google Scholar 

  • Read AJ (1999) Harbour porpoise Phocoena phocoena (Linnaeus, 1758). In: Ridgway SH, Harrison R (eds) Handbook of marine mammals, vol. 6. Academic Press, San Diego, pp 323–355

  • Read AJ, Hohn AA (1995) Life in the fast lane: the life history of harbor porpoises from the Gulf of Maine. Mar Mamm Sci 11:423–440

    Google Scholar 

  • Read AJ, Tolley KA (1996) Postnatal growth and allometry of harbour porpoises from the Bay of Fundy, Canada. Can J Zool 75:122–130

    Google Scholar 

  • Rhead WJ, Dubiel B, Tanaka K (1981) The tissue distribution of isovaleryl CoA dehydrogenase in the rat. In: Walser M, Williamson JR (eds) Metabolism and clinical implications of branched chain amino acids and ketoacids. Elsevier-North Holland, New York, pp 47–52

  • Rice DW (1998) Marine mammals of the world: systematics and distribution. Special Publication Number 4, Society for Marine Mammalogy, Lawrence, KS

    Google Scholar 

  • Rosel PE, Haygood MG, Perrin WF (1995) Phylogenetic relationships among the true porpoises (Cetacea: Phocoenidae). Mol Phyl Evol 4:463–474

    Article  CAS  Google Scholar 

  • Ryg M, Smith TG, Øritsland NA (1988) Thermal significance of the topographical distribution of blubber in ringed seals (Phoca hispida). Can J Fish Aquat Sci 45:985–992

    Google Scholar 

  • Steel RGD, Torrie JH (1980) Principles and procedures of statistics: a biometrical approach, 2nd edn. McGraw-Hill, New York

    Google Scholar 

  • Stegall VK, McLellan WA, Dillaman RJ, Read AJ, Pabst DA (1999) Epaxial muscle morphology of robust vs. emaciated harbor porpoises. Am Zool 39:84A

    Google Scholar 

  • Stryer L (1988) Biochemistry, 3rd edn. WH Freeman, New York

  • Tabachnick BG, Fidell LS (1996) Using multivariate statistics, 3rd edn. Harper Collins, New York

  • Tanaka K (1973) Isovaleric acidemia and its induction in experimental animals by hypoglycin A. In: Hommes F, van den Berg CJ (eds) Inborn errors of metabolism. Academic Press, London, pp 269–289

  • Tanaka K, Isselbacher KJ (1967) The isolation and identification of N-isovalerylglycine from urine of patients with isovaleric acidemia. J Biol Chem 242:2966–2972

    CAS  PubMed  Google Scholar 

  • Tanaka K, Budd MA, Efron ML, Isselbacher KJ (1966) Isovaleric acidemia: a new genetic defect of leucine metabolism. Proc Nat Acad Sci 56:236–242

    CAS  PubMed  Google Scholar 

  • Tanaka K, Ikeda Y, Matsubara Y, Hyman D (1988) Molecular basis of isovaleric acidemia and the study of the acyl-CoA dehydrogenase family. Adv Neurol 48:107–131

    CAS  PubMed  Google Scholar 

  • Varanasi U, Malins DC (1971) Unique lipids of the porpoise (Tursiops gilli): differences in triacyl glycerols and wax esters of acoustic (mandibular canal and melon) and blubber tissues. Biochim Biophys Acta 231:415–418

    Article  CAS  PubMed  Google Scholar 

  • Varanasi U, Malins DC (1972) Triacylglycerols characteristic of porpoise acoustic tissues: molecular structure of diisovaleroylglycerides. Science 176:926–928

    CAS  PubMed  Google Scholar 

  • Varanasi U, Everitt M, Malins DC (1973) The isomeric composition of diisovaleroyl-glycerides: a specificity for the biosynthesis of the 1,3-diisovaleroyl structures. Int J Biochem 4:373–378

    Article  CAS  Google Scholar 

  • Varanasi U, Feldman HR, Malins DC (1975) Molecular basis for formation of lipid sound lens in echolocating cetaceans. Nature 255:340–343

    CAS  PubMed  Google Scholar 

  • Varanasi U, Markey D, Malins DC (1982) Role of isovaleroyl lipids in channelling of sound in the porpoise melon. Chem Phys Lipids 31:237–244

    Article  CAS  PubMed  Google Scholar 

  • Wartzok D, Ketten DR (1999) Marine mammal sensory systems. In: Reynolds JE, Rommel SA (eds) Biology of marine mammals. Smithsonian Institution, Washington, pp 117–175

  • Wedmid Y, Litchfield C, Ackman RG, Sipos JC, Eaton CA, Mitchell ED (1973) Heterogeneity of lipid composition within the cephalic melon tissue of the pilot whale (Globicephala melaena). Biochim Biophy Acta 326:439–447

    Article  CAS  Google Scholar 

  • West GC, Burns JJ, Modafferi M (1979a) Fatty acid composition of blubber from the four species of Bering Sea phocid seals. Can J Zool 57:189–195

    CAS  Google Scholar 

  • West GC, Burns JJ, Modafferi M (1979b) Fatty acid composition of Pacific walrus skin and blubber fats. Can J Zool 57:1249–1255

    CAS  Google Scholar 

  • Wretlind A (1957) The toxicity of low-molecular triglycerides. Acta Physiol Scand 40:338–343

    CAS  Google Scholar 

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Acknowledgements

We wish to thank many individuals and organisations for their generosity in contributing samples and assisting with sample collection: Bill McLellan and Ann Pabst (University of North Carolina at Wilmington; John Nicolas (National Marine Fisheries Service, Northeast Fisheries Science Center); Charley Potter (National Museum of Natural History, Smithsonian Institution); Thomas Jefferson and Susan Chivers (NMFS, Southwest Fisheries Science Center); Ellie Dickson and Elizabeth Slooten (University of Otago); Koen van Waerebeek and Julio Reyes; and many people from: state stranding networks from Massachusetts to Florida; Virginia Marine Science Museum; Hubbs-Sea World, Orlando, Florida; Mote Marine Laboratory, Sarasota, Florida; the Beaufort, North Carolina and Woods Hole, Massachusetts NMFS offices; the Marine Mammal Stranding Program at UNCW; the Duke University Marine Laboratory, Beaufort, North Carolina; the Canadian Department of Fisheries and Oceans; the Grand Manan Whale and Seabird Research Station, New Brunswick, Canada; and the fishermen of the Bay of Fundy and Gulf of Maine. This manuscript was improved by the comments of Ann Pabst and Kay Tanaka, and we also thank Dr. Tanaka for useful insights into, and suggestions regarding, iso5:0 metabolism. Samples were imported into Canada and the United States of America under appropriate CITES and US Department of Fish and Wildlife permits, and all analytical methods complied with current US and Duke University regulations. This study was supported by postgraduate fellowships from the Canadian Natural Sciences and Engineering Research Council (NSERC) and the Duke University Marine Laboratory to H.N.K., a postdoctoral scholarship at Woods Hole Oceanographic Institution to H.N.K., a Duke University Marine/Freshwater Biomedical Center Feasibility Study grant to H.N.K. and A.J.R., and NSERC Research and Equipment Grants to S.J.I. This represents Woods Hole Oceanographic Institution contribution number 10683.

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Correspondence to H. N. Koopman.

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Communicated by L.C.-H. Wang

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Koopman, H.N., Iverson, S.J. & Read, A.J. High concentrations of isovaleric acid in the fats of odontocetes: variation and patterns of accumulation in blubber vs. stability in the melon. J Comp Physiol B 173, 247–261 (2003). https://doi.org/10.1007/s00360-003-0329-9

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