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Distribution and development of the highly specialized lipids in the sound reception systems of dolphins

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Abstract

Fat bodies in the heads of toothed whales, which serve to transmit and receive sound, represent extraordinary examples of physiological specialization in adipose tissues among mammals, yet we know surprisingly little about their biochemical composition. We describe the spatial distributions and development of unusual endogenous lipids (branched-chain [“iso”] molecules and wax esters) in the mandibular fat bodies of bottlenose dolphins (Tursiops truncatus) using an ontogenetic series (fetus to adult; n = 10). Although concentrations of iso-acids, iso-alcohols and waxes were lower in younger dolphins than in adults, the same relative spatial arrangement was present in all age classes, implying a set “pattern” of acoustic lipid distribution that is established very early in life. In all age classes, a small region of blubber overlying the lateral region contained unusually high concentrations of iso-acids, exhibiting a tenfold increase over “normal” adjacent blubber. Being chemically more similar to the acoustic fat bodies, this region may serve as an entry point for sound into the head. Developmental accumulations of some iso-acids and iso-alcohols occurred more rapidly than others, implying that not only are the spatial distributions of branched-chain molecules under extremely fine-scale control, but the regulatory mechanisms controlling acoustic lipid synthesis are also highly complex.

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References

  • Ackman RG (1991) Application of gas-liquid chromatography to lipid separation and analysis: qualitative and quantitative analysis. In: Perkins EG (ed) Analysis of fats. oils and lipoproteins. American Oil Chemists Society, Chicago, pp 271–300

    Google Scholar 

  • Ackman RG, Eaton CA (1971) The bottle-nosed dolphin Tursiops truncatus: fatty acid composition of milk triglycerides. Can J Biochem 49:1172–1174

    Article  PubMed  CAS  Google Scholar 

  • Ackman RG, Eaton CA, Litchfield C (1971) Composition of wax esters, triglycerides and diacyl glyceryl ethers in the jaw and blubber fats of the Amazon river dolphin (Inia geoffrensis). Lipids 6:69–77

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Brill RL (1988) The acoustical function of the lower jaw of the bottlenose dolphin, Tursiops truncatus (Montagu), during echolocation. Ph.D. Dissertation, Loyola University of Chicago, Chicago, 123 pp

  • Brill RL, Harder PJ (1991) The effects of attenuating returning echolocation signals at the lower jaw of a dolphin (Tursiops truncatus). J Acoust Soc Am 89:2851–2857

    Article  Google Scholar 

  • Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mamm Sci 22:759–801

    Article  Google Scholar 

  • Bullock TH, Grinnell AD, Ikezono E, Kameda K, Katsuki Y, Nomoto M, Sato O, Suga N, Yanagisawa K (1968) Electrophysiology studies of central auditory mechanisms in cetaceans. Z Vgl Physiol 59:117–156

    Google Scholar 

  • Christie WW (1989) Gas chromatography and lipids: a practical guide. The Oily Press, Ayr

    Google Scholar 

  • Cranford TW (1999) The sperm whale’s nose: sexual selection on a grand scale? Mar Mamm Sci 15:1133–1157

    Article  Google Scholar 

  • Cranford TW, Krysl P, Hilderbrand JA (2008) Acoustic pathways revealed: simulated sound transmission and reception in Cuvier’s beaked whale (Ziphius cavirostris). Bioinspir Biomim 3:016001

    Article  PubMed  Google Scholar 

  • Dearolf JL, McLellan WA, Dillaman RM, Frierson D Jr, Pabst DA (2000) Precocial development of axial locomotor muscle in bottlenose dolphins (Tursiops truncatus). J Morphol 244:203–215

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Gardner SC, Varanasi U (2003) Isovaleric acid accumulation in odontocete melon during development. Naturwissenschaften 90:528–531

    Article  PubMed  CAS  Google Scholar 

  • Geraci JR, Lounsbury VJ (1993) Marine mammals ashore: a field guide for strandings. Texas A&M University Sea Grant Program, Galveston

    Google Scholar 

  • Gouw TH, Vlugter JG (1967) Physical properties of triglycerides III: ultrasonic sound velocity. Fette Seifen Anstrichm 69:159–164

    Article  CAS  Google Scholar 

  • Hendry JL, Kuczaj SA, Dudzinski K, Houser DS (2005) The ontogeny of echolocation in Atlantic bottlenose dolphins (Tursiops truncatus). Conference on the Biology of Marine Mammals, San Diego

    Google Scholar 

  • Hustad GO, Richardson T, Winder WC, Dean MP (1971) Acoustic properties of some lipids. Chem Phys Lipids 7:61–74

    Article  CAS  Google Scholar 

  • Koopman HN (2007) Phylogenetic, ecological and ontogenetic factors influencing the biochemical structure if the blubber of odontocetes. Mar Biol 151:277–291

    Article  Google Scholar 

  • Koopman HN, Zahorodny ZP (2008) Life history constrains biochemical development in the highly specialized odontocete echolocation system. Proc Roy Soc B 275:2327–2334

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Koopman HN, Pabst DA, McLellan WA, Dillaman RM, Read AJ (2002) Changes in blubber distribution and morphology associated with starvation in the harbor porpoise (Phocoena phocoena): evidence for regional differences in blubber structure and function. Physiol Biochem Zool 75:498–512

    Article  PubMed  CAS  Google Scholar 

  • Koopman HN, Iverson SJ, Read AJ (2003) High concentrations of isovaleric acid in the fats of odontocetes: variation and patterns of accumulation in blubber vs. stability in the melon. J Comp Phys B 173:247–261

    CAS  Google Scholar 

  • Koopman HN, Budge SM, Ketten DR, Iverson SJ (2006) The topographical distribution of lipids in the mandibular fat bodies of ondontocetes: remarkable complexity and consistency. J Oceanogr Eng 31:95–106 (Special Issue on the Effects of Sound in the Marine Environment)

    Google Scholar 

  • Kruskal WH, Wallis WA (1952) Use of ranks in one-criterion variance analysis. J Am Stat Assoc 47:583–621

    Article  Google Scholar 

  • Lindhard M (1988) Apparent sonar clicks from a captive bottlenose dolphin. In: Nachtigall PE, Moore PWD (eds) Animal sonar: processes and performance. Plenum Press, New York, pp 109–113

    Google Scholar 

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

    Article  CAS  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

    Article  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  PubMed  CAS  Google Scholar 

  • Litchfield C, Greenberg AJ, Ackman RG, Eaton CA (1978) Distinctive medium chain wax esters, triglycerides, and diacyl glyceryl ethers in the head fats of the Pacific beaked whale, Berardius bairdi. Lipids 13:860–866

    Article  PubMed  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. Academic, London, pp 237–290

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • McCormick JG, Wever EG, Dalin J (1970) Sound conduction in the dolphin ear. J Acoust Soc Am 6:1418–1428

    Article  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

    Article  Google Scholar 

  • Møhl B, Au WWL, Pawloski J, Nachtigall PE (1999) Dolphin hearing: relative sensitivity as a function of point of application of a contact sound source in the jaw and head region. J Acoust Soc Am 105:3421–3424

    Article  PubMed  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 Phys B 71:357–365

    Article  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 

  • Morris RJ (1986) The acoustic faculty of dolphins. In: Bryden MM, Harrison R (eds) Research on dolphins. Clarendon Press, Oxford, pp 369–399

    Google Scholar 

  • Norris KS (1968) The evolution of acoustic mechanisms in Odontocete cetaceans. In: Drake ET (ed) Evolution and environment. Yale University Press, New Haven, pp 297–324

    Google Scholar 

  • Pond CM (1998) The fats of life. Cambridge University Press, Cambridge, p 314

    Google Scholar 

  • Read AJ, Wells RS, Hohn AA, Scott MD (1993) Patterns of growth in wild dolphins, Tursiops truncatus. J Zool 231:107–123

    Article  Google Scholar 

  • Reiss D (1988) Observations on the development of echolocation in young bottlenose dolphins. In: Nachtigall PE, Moore PWD (eds) Animal sonar: processes and performance. Plenum Press, New York, pp 121–127

    Google Scholar 

  • Robisch PA, Malins DC, Best R, Varanasi U (1972) Differences in triacylglycerols from acoustic tissues and posterior cranial blubber of the Narwhal (Monodon monoceros). Biochem J 130:33–34

    Google Scholar 

  • Samuel AM, Worthy GAJ (2004) Variability in fatty acid composition of bottlenose dolphin (Tursiops truncatus) blubber as a function of body site, season and reproductive state. Can J Zool 82:1933–1942

    Article  CAS  Google Scholar 

  • Sargent JR (1976) The structure, metabolism and function of lipids in marine organisms. In: Malins DC, Sargent JR (eds) Biochemical and biophysical perspectives in marine biology. Academic, London, pp 149–212

    Google Scholar 

  • Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York, p 399

    Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tranel K, Kuczaj SA (2005) Ontogeny of echolocation in bottlenose dolphins (Tursiops truncatus) during the first six months of life. Conference on the Biology of Marine Mammals, San Diego

    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

    PubMed  CAS  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 FR, Malins DC (1975) Molecular basis for formation of lipid sound lens in echolocating cetaceans. Nature 255:340–343

    Article  CAS  Google Scholar 

  • 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 Biophys Acta 326:439–447

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank the UNCW Marine Mammal Stranding Network, the Virginia Aquarium Stranding Program and the NOAA Beaufort Laboratory (United States National Marine Fisheries Service; SEFSC) for access to dolphin samples. Work carried out during this study complied with the current United States and Canadian laws. Support for this work was provided by Natural Sciences and Engineering Research Council (NSERC—Canada), UNCW, Sigma Xi, and the United States Office of Naval Research. The authors would also like to thank Ann Pabst, Ted Cranford, Bill McLellan and Butch Rommel for their help, insight and comments. This manuscript was also improved by the comments of two anonymous reviewers.

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Authors and Affiliations

  1. Department of Biology, Dalhousie University, 1355 Oxford Street, Halifax, NS, B3H 4J1, Canada

    Zoey P. Zahorodny Duggan

  2. Biology and Marine Biology, University of North Carolina Wilmington, 601 South College Road, Wilmington, NC, 28403, USA

    Zoey P. Zahorodny Duggan & Heather N. Koopman

  3. Department of Process Engineering and Applied Science, Dalhousie University, 1360 Barrington Street, Halifax, NS, B3J 2X4, Canada

    Suzanne M. Budge

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  1. Zoey P. Zahorodny Duggan
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  2. Heather N. Koopman
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  3. Suzanne M. Budge
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Correspondence to Heather N. Koopman.

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Communicated by I. D. Hume.

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Zahorodny Duggan, Z.P., Koopman, H.N. & Budge, S.M. Distribution and development of the highly specialized lipids in the sound reception systems of dolphins. J Comp Physiol B 179, 783–798 (2009). https://doi.org/10.1007/s00360-009-0360-6

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