in

Interannual variability in the lipid and fatty acid profiles of east Australia-migrating humpback whales (Megaptera novaeangliae) across a 10-year timeline

  • 1.

    Waugh, C. A., Nichols, P. D., Noad, M. C. & Bengtson Nash, S. M. Lipid and fatty acid profiles of migrating Southern Hemisphere humpback whales Megaptera novaeangliae. Mar. Ecol. Prog. Ser. 471, 271–281 (2012).

    ADS  CAS  Article  Google Scholar 

  • 2.

    Chittleborough, R. G. Dynamics of two populations of the humpback whale, Megaptera novaeangliae (Borowski). Mar. Freshw. Res. 16, 33–128 (1965).

    Article  Google Scholar 

  • 3.

    Kawamura, A. A Review of food of balaenopterid whales. Sci. Rep. Whales Res. Inst. 32, 155–197 (1980).

    Google Scholar 

  • 4.

    Danilewicz, D., Tavares, M., Moreno, I. B., Ott, P. H. & Trigo, C. C. Evidence of feeding by the humpback whale (Megaptera novaeangliae) in mid-latitude waters of the western South Atlantic. Mar. Biodivers. Rec. 2, 1–3 (2009).

    Article  Google Scholar 

  • 5.

    Pinto de sa Alves, L. C. et al. Record of feeding by humpback whales (Megaptera novaeangliae) in tropical waters off Brazil. Mar. Mammal Sci. 25, 416–419 (2009).

    Article  Google Scholar 

  • 6.

    Stamation, K. A., Croft, D. B., Shaughnessy, P. D. & Waples, K. A. Observations of humpback whales (Megaptera novaeangliae) feeding during their southward migration along the coast of Southeastern New South Wales, Australia: Identification of a possible supplemental feeding ground. Aquat. Mamm. 33, 165–174 (2007).

    Article  Google Scholar 

  • 7.

    Owen, K. et al. Potential energy gain by whales outside of the Antarctic: Prey preferences and consumption rates of migrating humpback whales (Megaptera novaeangliae). Polar Biol. 40, 277–289 (2017).

    Article  Google Scholar 

  • 8.

    Eisenmann, P. et al. Isotopic evidence of a wide spectrum of feeding strategies in southern hemisphere humpback whale baleen records. PLoS One 11, e0156698 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 9.

    Bengtson Nash, S. M. et al. Signals from the south; humpback whales carry messages of Antarctic sea-ice ecosystem variability. Glob. Chang. Biol. 24, 1500–1510 (2018).

    ADS  PubMed  Article  PubMed Central  Google Scholar 

  • 10.

    IWC. Report of the workshop on the comprehensive assessment of southern hemisphere humpback whales. J. Cetacean Res. Manag. (Spec Issue) 3, 1–50 (2011).

    Google Scholar 

  • 11.

    Owen, K. et al. Effect of prey type on the fine-scale feeding behaviour of migrating east Australian humpback whales. Mar. Ecol. Prog. Ser. 541, 231–244 (2015).

    ADS  Article  Google Scholar 

  • 12.

    Gales, N. et al. Satellite tracking of southbound East Australian humpback whales (Megaptera novaeangliae): Challenging the feast or famine model for migrating whales. J. Cetacean Res. Manag. 61 (2009).

  • 13.

    Falk-Petersen, S., Hagen, W., Kattner, G., Clarke, A. & Sargent, J. Lipids, trophic relationships, and biodiversity in Arctic and Antarctic krill. Can. J. Fish. Aquat. Sci. 57, 178–191 (2000).

    CAS  Article  Google Scholar 

  • 14.

    Clarke, A. Lipid Content and Composition of Antarctic Krill, Euphausia Superba Dana. J. Crustac. Biol. 4, 285–294 (1984).

    CAS  Article  Google Scholar 

  • 15.

    Budge, S. M., Iverson, S. J. & Koopman, H. N. Studying trophic ecology in marine ecosystems using fatty acids: A primer on analysis and interpretation. Mar. Mammal Sci. 22, 759–801 (2006).

    Article  Google Scholar 

  • 16.

    Cook, H. W. Fatty acid desaturation and chain elongation in eucaryotes. In Biochemistry of Lipids, Lipoproteins and Membranes (eds Vance, D. E. & Vance, J.) 141–169 (Elsevier, New York, 1991).

    Google Scholar 

  • 17.

    Guang, Y., Li, C. & Yanqing, W. Fatty acid composition of Euphausia superba, Thysanoessa macrura and Euphausia crystallorophias collected from Prydz Bay, Antarctica. J. Ocean Univ. China 15, 297–302 (2016).

    Article  CAS  Google Scholar 

  • 18.

    Hagen, W. & Kattner, G. Lipid metabolism of the Antarctic euphausiid Thysanoessa macrura and its ecological implications. Limnol. Oceanogr. 43, 1894–1901 (1998).

    ADS  CAS  Article  Google Scholar 

  • 19.

    Mayzaud, P., Boutoute, M. & Alonzo, F. Lipid composition of the euphausiids Euphausia vallentini and Thysanoessa macrura during summer in the Southern Indian Ocean. Antarct. Sci. 15, 463–475 (2003).

    ADS  Article  Google Scholar 

  • 20.

    O’Brien, C., Virtue, P., Kawaguchi, S. & Nichols, P. D. Aspects of krill growth and condition during late winter-early spring off East Antarctica (110–130°E). Deep. Res. Part II 58, 1211–1221 (2011).

    Article  CAS  Google Scholar 

  • 21.

    Phleger, C. F., Nichols, P. D. & Virtue, P. Lipids and trophodynamics of Antarctic zooplankton. Comp. Biochem. Physiol. Part B 120, 311–323 (1998).

    Article  Google Scholar 

  • 22.

    Stübing, D. & Hagen, W. Fatty acid biomarker ratios-suitable trophic indicators in Antarctic euphausiids?. Polar Biol. 26, 774–782 (2003).

    Article  Google Scholar 

  • 23.

    Phleger, C. F., Nelson, M. M., Mooney, B. D. & Nichols, P. D. Interannual and between species comparison of the lipids, fatty acids and sterols of Antarctic krill from the US AMLR Elephant Island survey area. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 131, 733–747 (2002).

    PubMed  Article  Google Scholar 

  • 24.

    Varisco, M., Crovetto, C., Colombo, J., Vinuesa, J. & Risso, S. Proximate composition and nutritional quality of the meat of the squat lobster Munida gregaria (Fabricius 1973). J. Aquat. Food Prod. Technol. 29, 229–237 (2020).

    CAS  Article  Google Scholar 

  • 25.

    Phillips, K. L., Nichols, P. D. & Jackson, G. D. Size-related dietary changes observed in the squid Moroteuthis ingens at the Falkland Islands: Stomach contents and fatty-acid analyses. Polar Biol. 26, 474–485 (2003).

    Article  Google Scholar 

  • 26.

    Virtue, P. Lipids in Euphausia superba. PhD thesis. (University of Tasmania, 1995).

  • 27.

    Baylis, A. M. M., Hamer, D. J. & Nichols, P. D. Assessing the use of milk fatty acids to infer the diet of the Australian sea lion (Neophoca cinerea). Wildl. Res. 36, 169–176 (2009).

    CAS  Article  Google Scholar 

  • 28.

    Nichols, P. D., Virtue, P., Mooney, B. D., Elliott, N. G. & Yearsley, G. K. Seafood the good food: The oil (fat) content and composition of Australian commercial fishes, shellfishes and crustaceans (CSIRO Div. of Marine Research//Fisheries Research & Development Corporation, 1998).

  • 29.

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

    CAS  Article  Google Scholar 

  • 30.

    Bengtson Nash, S. M., Waugh, C. A. & Schlabach, M. Metabolic concentration of lipid soluble organochlorine burdens in the blubber of southern hemisphere humpback whales through migration and fasting. Environ. Sci. Technol. 47, 9404–9413 (2013).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 31.

    Lockyer, C. Body weights of some species of large whales. ICES J. Mar. Sci. 36, 259–273 (1976).

    Article  Google Scholar 

  • 32.

    Castrillon, J. & Bengtson Nash, S. Evaluating cetacean body condition: A review of traditional approaches and new developments. Ecol. Evol. 1–19 (2020).

  • 33.

    Kershaw, J. L., Hall, A. J., Brownlow, A., Ramp, C. A. & Miller, P. J. O. Assessing cetacean body condition: Is total lipid content in blubber biopsies a useful monitoring tool?. Aquat. Conserv. Mar. Freshw. Ecosyst. 29, 271–282 (2019).

    Article  Google Scholar 

  • 34.

    Christiansen, F. et al. Variation in outer blubber lipid concentrations does not reflect morphological body condition in humpback whales. J. Exp. Biol. 223, jeb213769 (2020).

    PubMed  Article  PubMed Central  Google Scholar 

  • 35.

    Christiansen, F. et al. Response to: Lipid content of whale blubber cannot be measured using biopsies. J. Exp. Biol. 223, 1–2 (2020).

    Google Scholar 

  • 36.

    Arts, M. T., Brett, M. T. & Kainz, M. J. Lipids in Aquatic Ecosystems (Springer, New York, 2009). https://doi.org/10.1007/978-0-387-89366-2.

    Google Scholar 

  • 37.

    Ackman, R. G., Hingley, J. H., Eaton, C. A., Sipos, J. C. & Mitchell, E. D. Blubber fat deposition in mysticeti whales. Can. J. Zool. 53, 1332–1339 (1975).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 38.

    Olsen, E. & Grahl-Nielsen, O. Blubber fatty acids of minke whales: Stratification, population identification and relation to diet. Mar. Biol. 142, 13–24 (2003).

    CAS  Article  Google Scholar 

  • 39.

    Iverson, S. J. Blubber. In Encyclopedia of Marine Mammals 115–120 (Elsevier Ltd, 2009). https://doi.org/10.1016/B978-0-12-373553-9.00032-8.

  • 40.

    Noren, D. P. & Mangel, M. Energy reserve allocation in fasting Northern Elephant Seal Pups: Inter-relationships between body condition and fasting duration. Funct. Ecol. 18, 233–242 (2004).

    Article  Google Scholar 

  • 41.

    Grahl-Nielsen, O., Krakstad, J. O., Nøttestad, L. & Axelsen, B. E. Dusky dolphins Lagenorhynchus obscurus and Cape fur seals Arctocephalus pusillus pusillus: Fatty acid composition of their blubber and prey species. Afr. J. Mar. Sci. https://doi.org/10.2989/1814232x.2010.501556 (2010).

    Article  Google Scholar 

  • 42.

    Guerrero, A. I. et al. Vertical fatty acid composition in the blubber of leopard seals and the implications for dietary analysis. J. Exp. Mar. Bio. Ecol. 478, 54–61 (2016).

    CAS  Article  Google Scholar 

  • 43.

    Ruchonnet, D., Boutoute, M., Guinet, C. & Mayzaud, P. Fatty acid composition of Mediterranean fin whale Balaenoptera physalus blubber with respect to body heterogeneity and trophic interaction. Mar. Ecol. Prog. Ser. 311, 165–174 (2006).

    ADS  CAS  Article  Google Scholar 

  • 44.

    Strandberg, U. et al. Stratification, composition, and function of marine mammal blubber: The ecology of fatty acids in marine mammals. Physiol. Biochem. Zool. 81, 473–485 (2008).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 45.

    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 Biochem. Syst. Environ. Physiol. 173, 247–261 (2003).

    CAS  Article  Google Scholar 

  • 46.

    Herman, D. P. et al. Feeding ecology of eastern North Pacific killer whales Orcinus orca from fatty acid, stable isotope, and organochlorind analyses of blubber biopsies. Mar. Ecol. Prog. Ser. 302, 275–291 (2005).

    ADS  Article  Google Scholar 

  • 47.

    Virtue, P., Nichols, P. D., Nicol, S., McMinn, A. & Sikes, E. L. The lipid composition of Euphausia superba Dana in relation to the nutritional value of Phaeocystis pouchetii (Hariot) Lagerheim. Antarct. Sci. 5, 169–177 (1993).

    ADS  Article  Google Scholar 

  • 48.

    Stübing, D., Hagen, W. & Schmidt, K. On the use of lipid biomarkers in marine food web analyses: An experimental case study on the Antarctic krill. Euphausia superba. Limnol. Oceanogr. 48, 1685–1700 (2003).

    ADS  Article  Google Scholar 

  • 49.

    Falk-Petersen, S., Hopkins, C. E. & Sargent, J. R. Trophic relationships in the pelagic, Arctic food web. in Trophic relationships in marine environments (eds Barnes, M. & Gibson, R. N.) 315-333 (Aberdeen University Press, 1990).

  • 50.

    Auel, H., Harjes, M., da Rocha, R., Stübing, D. & Hagen, W. Lipid biomarkers indicate different ecological niches and trophic relationships of the Arctic hyperiid amphipods Themisto abyssorum and T. libellula. Polar Biol. 25, 374–383 (2002).

    Article  Google Scholar 

  • 51.

    Scott, C., Kwasniewski, S., Falk-Petersen, S. & Sargent, J. Species differences, origins and functions of fatty alcohols and fatty acids in the wax esters and phospholipids of Calanus hyperboreus, C. glacialis and C. finmarchicus from Arctic waters. Mar. Ecol. Prog. Ser. 235, 127–134 (2002).

    ADS  CAS  Article  Google Scholar 

  • 52.

    Dalsgaard, J., John, M. S., Kattner, G., Müller-Navarra, D. & Hagen, W. Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol. 46, 225–340 (2003).

    PubMed  Article  Google Scholar 

  • 53.

    Graeve, M., Kattner, G. & Hagen, W. Diet-induced changes in the fatty acid composition of Arctic herbivorous copepods: Experimental evidence of trophic markers. J. Exp. Mar. Biol. Ecol. 182, 97–110 (1994).

    CAS  Article  Google Scholar 

  • 54.

    Iverson, S. J., Field, C., Don Bowen, W. & Blanchard, W. Quantitative fatty acid signature analysis: A new method of estimating predator diets. Ecol. Monogr. 74, 211–235 (2004).

    Article  Google Scholar 

  • 55.

    Fleming, A. H., Clark, C. T., Calambokidis, J. & Barlow, J. Humpback whale diets respond to variance in ocean climate and ecosystem conditions in the California Current. Glob. Chang. Biol. 22, 1214–1224 (2016).

    ADS  PubMed  Article  Google Scholar 

  • 56.

    Ericson, J. A. et al. Seasonal and interannual variations in the fatty acid composition of adult Euphausia superba Dana, 1850 (Euphausiacea) samples derived from the Scotia Sea krill fishery. J. Crustac. Biol. 38, 673–681 (2018).

    Google Scholar 

  • 57.

    Reiss, C. S., Walsh, J. & Goebel, M. E. Winter preconditioning determines feeding ecology of Euphausia superba in the Antarctic Peninsula. Mar. Ecol. Prog. Ser. 519, 89–101 (2015).

    ADS  CAS  Article  Google Scholar 

  • 58.

    Cleary, A., Durbin, E. & Casas, M. Feeding by Antarctic krill Euphausia superba in the West Antarctic Peninsula: Differences between fjords and open waters. Mar. Ecol. Prog. Ser. 595, 39–54 (2018).

    ADS  CAS  Article  Google Scholar 

  • 59.

    Schmidt, K. & Atkinson, A. Feeding and food processing in Antarctic krill (Euphausia superba Dana). In Biology and Ecology of Antarctic Krill 175–224 (Springer, 2016).

  • 60.

    Hagen, W., Kattner, G., Terbrüggen, A. & Van Vleet, E. S. Lipid metabolism of the antarctic krill Euphausia superba and its ecological implications. Mar. Biol. 139, 95–104 (2001).

    CAS  Article  Google Scholar 

  • 61.

    Cripps, G. C., Watkins, J. L., Hill, H. J. & Atkinson, A. Fatty acid content of Antarctic krill Euphausia superba at South Georgia related to regional populations and variations in diet. Mar. Ecol. Prog. Ser. 181, 177–188 (1999).

    ADS  CAS  Article  Google Scholar 

  • 62.

    Lambertsen, R., Baker, C., Weinrich, M. & Modi, W. An improved whale biopsy system designed for multidisciplinary research. In Nondestructive biomarkers in vertebrates 219–244 (Lewis Publishers, 1994).

  • 63.

    Waugh, C. A., Nichols, P. D., Schlabach, M., Noad, M. & Bengtson Nash, S. M. Vertical distribution of lipids, fatty acids and organochlorine contaminants in the blubber of southern hemisphere humpback whales (Megaptera novaeangliae). Mar. Environ. Res. 94, 24–31 (2014).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 64.

    Druskat, A., Ghosh, R., Castrillon, J. & Bengtson Nash, S. M. Sex ratios of migrating southern hemisphere humpback whales: A new sentinel parameter of ecosystem health. Mar. Environ. Res. 151, 1–7 (2019).

    Article  CAS  Google Scholar 

  • 65.

    Bligh, E. G. & Dyer, W. J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911–917 (1959).

    CAS  PubMed  Article  Google Scholar 

  • 66.

    Couturier, L. I. E. et al. State of art and best practices for fatty acid analysis in aquatic sciences. ICES J. Mar. Sci. fsaa121, 1–21 (2020).

    Google Scholar 

  • 67.

    Volkman, J. K. & Nichols, P. D. Applications of thin-layer chromatography-flame ionization detection to the analysis for lipids and pollutants in marine and environmental samples. J. Planar Chromatogr. Mod. TLC 4, 19–26 (1991).

    CAS  Google Scholar 

  • 68.

    Alhazzaa, R., Bridle, A. R., Nichols, P. D. & Carter, C. G. Up-regulated desaturase and elongase gene expression promoted accumulation of polyunsaturated fatty acid (PUFA) but not long-chain PUFA in Lates calcarifer, a tropical euryhaline fish, fed a stearidonic acid- and γ-linoleic acid-enriched diet. J. Agric. Food Chem. 59, 8423–8434 (2011).

    CAS  PubMed  Article  Google Scholar 

  • 69.

    Bode, M. et al. Feeding strategies of tropical and subtropical calanoid copepods throughout the eastern Atlantic Ocean – Latitudinal and bathymetric aspects. Prog. Oceanogr. 138, 268–282 (2015).

    ADS  Article  Google Scholar 

  • 70.

    Nicol, S. Krill, currents, and sea ice: Euphausia superba and its changing environment. Bioscience 56, 111 (2006).

    Article  Google Scholar 

  • 71.

    Flores, H. et al. Impact of climate change on Antarctic krill. Mar. Ecol. Prog. Ser. 458, 1–19 (2012).

    ADS  Article  Google Scholar 

  • 72.

    Turner, J., Hosking, J. S., Bracegirdle, T. J., Marshall, G. J. & Phillips, T. Recent changes in Antarctic Sea Ice. Philos. Trans. R. Soc. A Math. Phys. Eng. Sci. 73 (2015).

  • 73.

    Holland, M. M., Landrum, L., Kostov, Y. & Marshall, J. Sensitivity of Antarctic sea ice to the Southern Annular Mode in coupled climate models. Clim. Dyn. 49, 1813–1831 (2017).

    Article  Google Scholar 

  • 74.

    Bellenger, H., Guilyardi, E., Leloup, J., Lengaigne, M. & Vialard, J. ENSO representation in climate models: From CMIP3 to CMIP5. Clim. Dyn. 42, 1999–2018 (2014).

    Article  Google Scholar 

  • 75.

    O’Carroll, A. G. et al. Observational needs of sea surface temperature. Front. Mar. Sci. 6 (2019).

  • 76.

    Atkinson, A. et al. Oceanic circumpolar habitats of Antarctic krill. Mar. Ecol. Prog. Ser. 362, 1–23 (2008).

    ADS  CAS  Article  Google Scholar 

  • 77.

    Kattner, G., Hagen, W., Falk-Petersen, S., Sargent, J. R. & Henderson, R. J. Antarctic krill Thysanoessa macrura fills a major gap in marine lipogenic pathways. Mar. Ecol. Prog. Ser. 134, 295–298 (1996).

    ADS  Article  Google Scholar 


  • Source: Ecology - nature.com

    Universities should lead the way on climate action, MIT panelists say

    Stressor-induced ecdysis and thecate cyst formation in the armoured dinoflagellates Prorocentrum cordatum