Skip to main content

Advertisement

SpringerLink
Log in

Lipid signature of neural tissues of marine and terrestrial mammals: consistency across species and habitats

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Marine mammals are exposed to O2-limitation and increased N2 gas concentrations as they dive to exploit habitat and food resources. The lipid-rich tissues (blubber, acoustic, neural) are of particular concern as N2 is five times more soluble in lipid than in blood or muscle, creating body compartments that can become N2 saturated, possibly leading to gas emboli upon surfacing. We characterized lipids in the neural tissues of marine mammals to determine whether they have similar lipid profiles compared to terrestrial mammals. Lipid profiles (lipid content, lipid class composition, and fatty acid signatures) were determined in the neural tissues of 12 cetacean species with varying diving regimes, and compared to two species of terrestrial mammals. Neural tissue lipid profile was not significantly different in marine versus terrestrial mammals across tissue types. Within the marine species, average dive depth was not significantly associated with the lipid profile of cervical spinal cord. Across species, tissue type (brain, spinal cord, and spinal nerve) was a significant factor in lipid profile, largely due to the presence of storage lipids (triacylglycerol and wax ester/sterol ester) in spinal nerve tissue only. The stability of lipid signatures within the neural tissue types of terrestrial and marine species, which display markedly different dive behaviors, points to the consistent role of lipids in these tissues. These findings indicate that despite large differences in the level of N2 gas exposure by dive type in the species examined, the lipids of neural tissues likely do not have a neuroprotective role in marine mammals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aggarwal S, Yurlova L, Simons M (2011) Central nervous system myelin: structure, synthesis and assembly. Trends Cell Biol 21(10):585–593

    Article  CAS  PubMed  Google Scholar 

  • Baird RW, Webster DL, Schorr GS, McSweeney DJ, Barlow J (2008) Diel variation in beaked whale diving behavior. Mar Mamm Sci 24(3):630–642

    Article  Google Scholar 

  • Bernaldo de Quirós Y, Fernandez A, Baird R, Brownell R Jr, Aguilar de Soto N, Allen D, Arbelo M, Arregui M, Costidis A, Fahlman A (2019) Advances in research on the impacts of anti-submarine sonar on beaked whales. Proc R Soc B 286(1895):20182533

    Article  PubMed  PubMed Central  Google Scholar 

  • Berta A, Sumich JL, Kovacs KM (2015) Marine mammals: evolutionary biology. Academic Press, New York

    Google Scholar 

  • Björkhem I (2006) Crossing the barrier: oxysterols as cholesterol transporters and metabolic modulators in the brain. J Intern Med 260(6):493–508

    Article  PubMed  CAS  Google Scholar 

  • Bolton B (1939) The blood supply of the human spinal cord. J Neurol Psychol 2:137–148

    Article  CAS  Google Scholar 

  • Bourre J (2004) Roles of unsaturated fatty acids (especially omega-3 fatty acids) in the brain at various ages and during ageing. J Nutr 8:163–174

    CAS  Google Scholar 

  • Brenna JT, Diau G-Y (2007) The influence of dietary docosahexaenoic acid and arachidonic acid on central nervous system polyunsaturated fatty acid composition. Prostaglandins Leukot Essent Fatty Acids 77(5):247–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brockstein B, Johns L, Gewertz B (1994) Blood supply to the spinal cord: anatomic and physiologic correlations. Ann Vasc Surg 8:394–399

    Article  CAS  PubMed  Google Scholar 

  • Bürgisser P, Matthieu J-M, Jeserich G, Waehneldt TV (1986) Myelin lipids: a phylogenetic study. Neurochem Res 11(9):1261–1272

    Article  PubMed  Google Scholar 

  • Cermenati G, Mitro N, Audano M, Melcangi RC, Crestani M, De Fabiani E, Caruso D (2015) Lipids in the nervous system: from biochemistry and molecular biology to patho-physiology. Biochimica et Biophysica Acta (BBA) Mol Cell Biol Lipids 1851(1):51–60

    Article  CAS  Google Scholar 

  • Christie WW (1973) Lipid analysis, vol 167. Pergamon Press, Oxford

    Google Scholar 

  • Clandinin M (1999) Brain development and assessing the supply of polyunsaturated fatty acid. Lipids 34(2):131–137

    Article  CAS  PubMed  Google Scholar 

  • Costidis AM, Rommel SA (2016) The extracranial arterial system in the heads of beaked whales, with implications on diving physiology and pathogenesis. J Morphol 277(1):5–33

    Article  CAS  PubMed  Google Scholar 

  • Cox TM, Ragen T, Read A, Vos E, Baird RW, Balcomb K, Barlow J, Caldwell J, Cranford T, Crum L (2006) Understanding the impacts of anthropogenic sound on beaked whales. Space and Naval Warfare Systems Center, San Diego

    Google Scholar 

  • Dalal KB, Einstein ER (1969) Biochemical maturation of the central nervous system: I. Lipid changes. Brain Res 16(2):441–451

    Article  CAS  PubMed  Google Scholar 

  • Davis RW (2014) A review of the multi-level adaptations for maximizing aerobic dive duration in marine mammals: from biochemistry to behavior. J Comp Physiol B 184(1):23–53

    Article  PubMed  Google Scholar 

  • Davis RW, Kanatous SB (1999) Convective oxygen transport and tissue oxygen consumption in Weddell seals during aerobic dives. J Exp Biol 202(9):1091–1113

    Article  CAS  PubMed  Google Scholar 

  • Dawson G (2015) Measuring brain lipids. Biochimica et Biophysica Acta (BBA) Mol Cell Biol Lipids 1851(8):1026–1039

    Article  CAS  Google Scholar 

  • Dienel GA, Hertz L (2001) Glucose and lactate metabolism during brain activation. J Neurosci Res 66(5):824–838

    Article  CAS  PubMed  Google Scholar 

  • Divecha N, Irvine RF (1995) Phospholipid signaling. Cell 80(2):269–278

    Article  CAS  PubMed  Google Scholar 

  • Downes CP (1983) Inositol phospholipids and neurotransmitter-receptor signalling mechanisms. Trends Neurosci 6:313–316

    Article  CAS  Google Scholar 

  • Else P, Hulbert A (1985) Mammals: an allometric study of metabolism at tissue and mitochondrial level. Am J Physiol Regul Integr Comp Physiol 248(4):R415–R421

    Article  CAS  Google Scholar 

  • Fahlman A, Schmidt A, Jones D, Bostrom B, Handrich Y (2007) To what extent might N2 limit dive performance in king penguins? J Exp Biol 210(19):3344–3355

    Article  CAS  PubMed  Google Scholar 

  • Feldman ML, Peters A (1998) Ballooning of myelin sheaths in normally aged macaques. J Neurocytol 27(8):605–614

    Article  CAS  PubMed  Google Scholar 

  • Fernández A, Edwards J, Rodriguez F, De Los Monteros AE, Herraez P, Castro P, Jaber J, Martin V, Arbelo M (2005) “Gas and fat embolic syndrome” involving a mass stranding of beaked whales (family Ziphiidae) exposed to anthropogenic sonar signals. Vet Pathol 42(4):446–457

    Article  PubMed  Google Scholar 

  • Fish FE (2000) Biomechanics and energetics in aquatic and semiaquatic mammals: platypus to whale. Physiol Biochem Zool 73(6):683–698

    Article  CAS  PubMed  Google Scholar 

  • Folch J, Lees M, Stanley G (1957) A simple method for total lipid extraction and purification. J Biol Chem 226:497–509

    Article  CAS  PubMed  Google Scholar 

  • Fox J, Weisberg S (2010) car: Companion to applied regression. R package version 2.0–2.

  • Fredheim B, Holen S, Ugland KI, Grahl-Nielsen O (1995) Fatty acid composition in blubber, heart and brain from phocid seals. Developments in marine biology, vol 4. Elsevier, pp 153–168

    Google Scholar 

  • Galli C, Fumagalli R (1968) Lipid composition of the central nervous system of marine vertebrates. J Neurochem 15:35–40

    Article  CAS  PubMed  Google Scholar 

  • Hooker SK, Baird RW, Fahlman A (2009) Could beaked whales get the bends?: Effect of diving behaviour and physiology on modelled gas exchange for three species: Ziphius cavirostris, Mesoplodon densirostris and Hyperoodon ampullatus. Respir Physiol Neurobiol 167(3):235–246

    Article  PubMed  Google Scholar 

  • Hooker SK, Fahlman A, Moore MJ, De Soto NA, De Quiros YB, Brubakk AO, Costa DP, Costidis AM, Dennison S, Falke K (2012) Deadly diving? Physiological and behavioural management of decompression stress in diving mammals. Proc R Soc B 171:1041–1050

    Article  Google Scholar 

  • Houser D, Howard R, Ridgway S (2001) Can diving-induced tissue nitrogen supersaturation increase the chance of acoustically driven bubble growth in marine mammals? J Theor Biol 213(2):183–195

    Article  CAS  PubMed  Google Scholar 

  • Irvine AB, Scott MD, Wells RS, Kaufmann JH (1981) Movements and activities of the Atlantic bottlenose dolphin, Tursiops truncatus, near Sarasota, Florida. Fish Bull 79(4):671–688

    Google Scholar 

  • Jepson P, Arbelo M, Deaville R, Patterson I, Castro P, Baker J, Degollada E, Ross H, Herráez P, Pocknell A (2003) Gas-bubble lesions in stranded cetaceans. Nature 425(6958):575–576

    Article  CAS  PubMed  Google Scholar 

  • Kenny RD (1990) Bottlenose dolphins off the northeastern United States. In: Leatherwood S, Reeves R (eds) The bottlenose dolphin. Academic Press, San Diego, pp 369–386

    Chapter  Google Scholar 

  • Ketten DR (1992) The marine mammal ear: specializations for aquatic audition and echolocation. The evolutionary biology of hearing. Springer, pp 717–750

    Chapter  Google Scholar 

  • Koopman HN (2007) Phylogenetic, ecological, and ontogenetic factors influencing the biochemical structure of the blubber of odontocetes. Mar Biol 151(1):277–291

    Article  Google Scholar 

  • Koopman HN, Westgate AJ (2012) Solubility of nitrogen in marine mammal blubber depends on its lipid composition. J Exp Biol 215(21):3856–3863

    CAS  PubMed  Google Scholar 

  • Koopman HN, Budge SM, Ketten DR, Iverson SJ (2006) Topographical distribution of lipids inside the mandibular fat bodies of odontocetes: remarkable complexity and consistency. IEEE J Ocean Eng 31(1):95–106

    Article  Google Scholar 

  • Kooyman GL (1985) Physiology without restraint in diving mammals. Mar Mamm Sci 1(2):166–178

    Article  Google Scholar 

  • Lassmann H, Bartsch U, Montag D, Schachner M (1997) Dying-back oligodendrogliopathy: a late sequel of myelin-associated glycoprotein deficiency. Glia 19(2):104–110

    Article  CAS  PubMed  Google Scholar 

  • Lonati GL, Westgate AJ, Pabst DA, Koopman HN (2015) Nitrogen solubility in odontocete blubber and mandibular fats in relation to lipid composition. J Exp Biol 218(16):2620–2630

    Article  PubMed  Google Scholar 

  • Maggio B, Cumar F, Maccioni H (1972) Lipid content in brain and spinal cord during experimental allergic encephalo-myelitis in rats. J Neurochem 19(4):1031–1037

    Article  CAS  PubMed  Google Scholar 

  • Mauch DH, Nägler K, Schumacher S, Göritz C, Müller E-C, Otto A, Pfrieger FW (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294(5545):1354–1357

    Article  CAS  PubMed  Google Scholar 

  • McFarland WL, Jacobs MS, Morgane PJ (1979) Blood supply to the brain of the dolphin, Tursiops truncatus, with comparative observation on special aspects of the cerebrovascular supply of other vertebrates. Neurosci Behav Res 3:1–93

    Google Scholar 

  • Mehta J, Braund K, Toivio-Kinnucan M (1990) Elemental composition, water, and total lipid content in peripheral nerves, spinal cord and brain of healthy adult dogs. Res Vet Sci 49(2):250–252

    Article  CAS  PubMed  Google Scholar 

  • Nieuwenhuys R, Voogd J, Van Huijzen C (2007) The human central nervous system: a synopsis and atlas. Springer

    Google Scholar 

  • O’Brien JS, Sampson EL, Stern MB (1967) Lipid composition of myelin from the peripheral nervous system: intradural spinal roots. J Neurochem 14(3):357–365

    Article  CAS  PubMed  Google Scholar 

  • Oksanen JF, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) vegan: Community Ecology Package., R package version 2.5–6

  • Panov A, Orynbayeva Z, Vavilin V, Lyakhovich V (2014) Fatty acids in energy metabolism of the central nervous system. BioMed Res Int 2014:472459

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2015) nlme: Linear and nonlinear mixed effects models.

  • Piscitelli MA, McLellan WA, Rommel SA, Blum JE, Barco SG, Pabst DA (2010) Lung size and thoracic morphology in shallow-and deep-diving cetaceans. J Morphol 271(6):654–673

    PubMed  Google Scholar 

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

    Book  Google Scholar 

  • Ponganis PJ (2011) Diving mammals. Compr Physiol 1(1):447–465

    Article  PubMed  Google Scholar 

  • Ponganis PJ (2015) Diving physiology of marine mammals and seabirds. Cambridge University Press

    Book  Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ridgway SH, Howard R (1979) Dolphin lung collapse and intramuscular circulation during free diving: evidence from nitrogen washout. Science 206(4423):1182–1183

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez M (2007) Effectors of demyelination and remyelination in the CNS: implications for multiple sclerosis. Brain Pathol 17(2):219–229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouser G, Kritchevsky G, Galli C, Yamamoto A, Knudson A (1967) Variation in lipid composition of human brain during development and in sphingolipidoses: use of two-dimensional thin layer chromatography. Inborn disorders of sphingolipid metabolism. Elsevier, pp 303–316

    Chapter  Google Scholar 

  • Rowlands CE (2020) Comparative morphology of the spinal cord and associated vasculature in shallow versus deep diving cetaceans. University of North Carolina Wilmington, Wilmington

    Google Scholar 

  • Saher G, Brügger B, Lappe-Siefke C, Möbius W, Tozawa R-i, Wehr MC, Wieland F, Ishibashi S, Nave K-A (2005) High cholesterol level is essential for myelin membrane growth. Nat Neurosci 8(4):468

    Article  CAS  PubMed  Google Scholar 

  • Salem N, Lin Y, Moriguchi T, Lim S, Salem N Jr, Hibbeln J (2015) Distribution of omega-6 and omega-3 polyunsaturated fatty acids in the whole rat body and 25 compartments. Prostaglandins Leukot Essent Fatty Acids 100:13–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saltiel AR, Kahn CR (2001) Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414(6865):799

    Article  CAS  PubMed  Google Scholar 

  • Santos MB, Pierce GJ, Herman J, López A, Guerra A, Mente E, Clarke M (2001) Feeding ecology of Cuvier’s beaked whale (Ziphius cavirostris): a review with new information on the diet of this species. J Mar Biol Assoc UK 81(4):687–694

    Article  Google Scholar 

  • Schaller O, Constantinescu GM (2007) Illustrated veterinary anatomical nomenclature. Georg Thieme Verlag

    Google Scholar 

  • Schmitt S, Castelvetri LC, Simons M (2015) Metabolism and functions of lipids in myelin. Biochimica et Biophysica Acta (BBA) Mol Cell Biol Lipids 181(8):999–1005

    Article  CAS  Google Scholar 

  • Schorr GS, Falcone EA, Moretti DJ, Andrews RD (2014) First long-term behavioral records from Cuvier’s beaked whales (Ziphius cavirostris) reveal record-breaking dives. PLoS ONE 9(3):e92633

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sierra E, Díaz-Delgado J, Sacchini S, Sánchez-Paz Y, Suárez-Santana C, Fernández Rodríguez AJ, Arregui M, Arbelo Hernández MA, de Quirós B, Miranda Y (2017) Deadly acute decompression sickness in Risso’s dolphins. Sci Rep 7:13621

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Singh M (2005) Essential fatty acids, DHA and human brain. Indian J Pediatr 72(3):239–242

    Article  PubMed  Google Scholar 

  • Spector AA (1999) Essentiality of fatty acids. Lipids 34(1):S1–S3

    Article  CAS  PubMed  Google Scholar 

  • Tsuyuki H, Itoh S (1970) Fatty acid components of black right whale oil by gas chromatography. Liver 2(189.5):131–134

    Google Scholar 

  • Varanasi U, Malins DC (1975) Brain lipids from the porpoise (Delphinus delphis): phosphoglycerides rich in isovaleric acid and long-chain iso-acids. Biochimica et Biophysica Acta (BBA) Lipids Lipid Metab 409(3):304–310

    Article  CAS  Google Scholar 

  • Verheijen MH, Chrast R, Burrola P, Lemke G (2003) Local regulation of fat metabolism in peripheral nerves. Genes Dev 17(19):2450–2464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vitello F, Zanetta J-P (1978) Thin-layer chromatography of phospholipids. J Chromatogr A 166(2):637–640

    Article  Google Scholar 

  • Vogl A, Fisher H (1981) Arterial circulation of the spinal cord and brain in the Monodontidae (Order Cetacea). J Morphol 170(2):171–180

    Article  CAS  PubMed  Google Scholar 

  • Weathersby P, Homer L (1980) Solubility of inert gases in biological fluids and tissues: a review. Undersea Biomed Res 7(4):277–296

    CAS  PubMed  Google Scholar 

  • Williams TM, Zavanelli M, Miller MA, Goldbeck RA, Morledge M, Casper D, Pabst DA, McLellan W, Cantin LP, Kliger DS (2008) Running, swimming and diving modifies neuroprotecting globins in the mammalian brain. Proc R Soc B Biol Sci 275(1636):751–758

    Article  CAS  Google Scholar 

  • Zimmer WM, Tyack PL (2007) Repetitive shallow dives pose decompression risk in deep-diving beaked whales. Mar Mamm Sci 23(4):888–925

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Drs. S. Rommel and P. Soudant for guidance with sample processing and lipid chemistry, and K. Guarino, T. Keenan, C. Rowlands, and L. Murley for help with dissections. Samples for this project were provided by the Marine Mammal Stranding Program at UNCW, the International Fund for Animal Welfare Stranding Program (M. Niemeyer), the Florida Fish and Wildlife Commission (N. Gordon), the National Park Service (Cape Hatteras National Seashore and Cape Lookout National Seashore), the North Carolina Aquarium Jennette’s Pier, the North Carolina Wildlife Resources Commission’s Outer Banks Center for Wildlife Education, North Carolina Marine Fisheries, the Virginia Aquarium and Marine Science Center, and the National Oceanic and Atmospheric Association. Samples were held under a Letter of Authorization from the National Marine Fisheries Service, Southeast Region to H.N.K. This project was funded by an Office of Naval Research Grant (N00014-17-1-2997) to H.N.K. The authors report no conflicts of interest or competing interests.

Funding

This project was funded by an Office of Naval Research Grant (N00014-17-1-2997) to H.N.K.

Author information

Author notes

  1. Hillary L. Glandon

    Present address: Prairie Research Institute, University of Illinois Urbana-Champaign, Champaign, IL, USA

Authors and Affiliations

  1. Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, NC, USA

    Hillary L. Glandon, William A. McLellan, D. Ann Pabst, Andrew J. Westgate & Heather N. Koopman

  2. Department of Earth and Ocean Sciences, University of North Carolina Wilmington, Wilmington, NC, USA

    Ai Ning Loh

Authors
  1. Hillary L. Glandon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ai Ning Loh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. William A. McLellan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. D. Ann Pabst
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrew J. Westgate
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Heather N. Koopman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hillary L. Glandon.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Communicated by H.V. Carey.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (TIF 2176 kb)

Supplementary file2 (XLSX 44 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Glandon, H.L., Loh, A.N., McLellan, W.A. et al. Lipid signature of neural tissues of marine and terrestrial mammals: consistency across species and habitats. J Comp Physiol B 191, 815–829 (2021). https://doi.org/10.1007/s00360-021-01373-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-021-01373-x

Keywords

Search

Navigation