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Non-parametric analysis of the spatio-temporal variability in the fatty-acid profiles among Greenland sharks

Published online by Cambridge University Press:  28 October 2016

Holly N. Steeves ,
Bailey Mcmeans ,
Chris Field ,
Connie Stewart ,
Michael T. Arts ,
Aaron T. Fisk ,
Christian Lydersen ,
Kit M. Kovacs  and
M. Aaron Macneil
Holly N. Steeves*
Affiliation:
Department of Mathematics and Statistics, Dalhousie University, Halifax, NS B3H 3J5, Canada
Bailey Mcmeans
Affiliation:
Department of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada
Chris Field
Affiliation:
Department of Mathematics and Statistics, Dalhousie University, Halifax, NS B3H 3J5, Canada
Connie Stewart
Affiliation:
Department of Computer Science and Applied Statistics, University of New Brunswick Saint John, Saint John, NB E2L 4L5, Canada
Michael T. Arts
Affiliation:
Department of Chemistry and Biology, Ryerson University, Toronto, ON M5B 2K3, Canada
Aaron T. Fisk
Affiliation:
Great Lakes Institute for Environmental Research, University of Windsor, Windsor, ON N9B 3P4, Canada
Christian Lydersen
Affiliation:
Norwegian Polar Institute, N-9296 Tromsø, Norway
Kit M. Kovacs
Affiliation:
Norwegian Polar Institute, N-9296 Tromsø, Norway
M. Aaron Macneil
Affiliation:
Department of Mathematics and Statistics, Dalhousie University, Halifax, NS B3H 3J5, Canada Australian Institute of Marine Science, PMB 3 Townsville MC, Townsville QLD, 4810, Australia
*
Correspondence should be addressed to: H.N. Steeves Department of Mathematics and Statistics, Dalhousie University, Halifax, NS B3H 3J5, Canada email: [email protected]
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Abstract

Shifting prey distributions due to global warming are expected to generate dramatic ecosystem-wide changes in trophic structure within Arctic marine ecosystems. Yet a relatively poor understanding of contemporary Arctic food webs makes it difficult to predict the consequences of such changes for Arctic predators. Doing so requires quantitative approaches that can track contemporary changes in predator diets through time, using accurate, well-defined methods. Here we use fatty acids (FA) to quantify differences in consumer diet using permutational multivariate analysis of variance tests that characterize spatial and temporal changes in consumer FA signatures. Specifically we explore differences in Greenland shark (Somniosus microcephalus) FA to differentiate their potential trophic role between Svalbard, Norway and Cumberland Sound, Canada. Greenland shark FA signatures revealed significant inter-annual differences, probably driven by varying seal and Greenland halibut responses to environmental conditions such as the NAO, bottom temperature, and annual sea-ice extent. Uncommon FA were also found to play an important role in driving spatial and temporal differences in Greenland shark FA profiles. Our statistical approach should facilitate quantification of changing consumer diets across a range of marine ecosystems.

Keywords

Ecological tracersquantifying changepredator dietspolar ecologyfatty acid signatures
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 3 , May 2018 , pp. 627 - 633
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Aitchison, J. (1986) The statistical analysis of compositional data. London: Chapman & Hall.Google Scholar
Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Google Scholar
Budge, S.M., Iverson, S.J. and Koopman, H.N. (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Marine Mammal Science 22, 759–801.CrossRefGoogle Scholar
Cheung, W.W.L., Lam, V.W.Y., Sarmiento, J.L., Kearney, K., Watson, R.E.G., Zeller, D. and Pauly, D. (2010) Large-scale redistribution of maximum fisheries catch potential in the global ocean under climate change. Global Change Biology 16, 24–35.Google Scholar
Dennard, S.T., MacNeil, M.A., Treble, M.A., Campana, S. and Fisk, A.T. (2010) Hierarchical analysis of a remote, Arctic, artisanal longline fishery. ICES Journal of Marine Science 67, 41–51.Google Scholar
Devine, J.A., Zuur, A.F., Ieno, E.N. and Smith, G.M. (2007) Common trends in demersal communities on the Newfoundland–Labrador Shelf. In Zuur, A.F., Ieno, E.N. and Smith, G.M. (eds) Analysing ecological data. New York, NY: Springer, pp. 589–599.Google Scholar
Friedlaender, A.S., Johnston, D.W. and Halpin, P.N. (2010) Effects of the North Atlantic Oscillation on sea ice breeding habitats of harp seals (Pagophilus groenlandicus) across the North Atlantic. Progress in Oceanography 86, 261–266.CrossRefGoogle Scholar
Gannes, L.Z., O'Brien, D.M. and del Rio, C.M. (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78, 1271–1276.Google Scholar
Hobson, K.A. (1993) Trophic relationships among high Arctic seabirds: insights from tissue-dependent stable-isotope models. Marine Ecology Progress Series 95, 7–18.Google Scholar
Hyslop, E.J. (1980) Stomach contents analysis – a review of methods and their application. Journal of Fish Biology 17, 411–429.Google Scholar
Iverson, S.J., Field, C., Bowen, W.D. and Blanchard, W. (2004) Quantitative fatty acid signature analysis: a new method of estimating predator diets. Ecological Monographs 74, 211–235.Google Scholar
Iverson, S.J., Springer, A.M. and Kitaysky, A.S. (2007) Seabirds as indicators of food web structure and ecosystem variability: qualitative and quantitative diet analyses using fatty acids. Marine Ecology Progress Series 352, 235–244.Google Scholar
Kattner, G., Hirche, H.J. and Krause, M. (1989) Spatial variability in lipid composition of calanoid copepods from Fram Strait, the Arctic. Marine Biology 102, 473–480.Google Scholar
Kihara, K. and Shimada, A.M. (1988) Prey–predator interactions of walleye pollock Theragra chalcogramma and water temperature. Japanese Society of Fisheries Science 54, 1131–1135.Google Scholar
Kovacs, K.M., Moore, S.E., Overland, J.E. and Lydersen, C. (2011) Impacts of changing sea ice conditions on Arctic marine mammals. Marine Biodiversity 41, 181–194.Google Scholar
Lea, M.A., Cherel, Y., Guinet, C. and Nichols, P.D. (2002) Antarctic fur seals foraging in the polar frontal zone: inter-annual shifts in diet as shown from fecal and fatty acid analyses. Marine Ecology Progress Series 245, 281–297.Google Scholar
Leclerc, L.M.E., Lydersen, C., Haug, T. and Bachmann, L. (2012) A missing piece in the Arctic food web puzzle? Stomach contents of Greenland sharks sampled in Svalbard, Norway. Polar Biology 35, 1197–1208.Google Scholar
MacNeil, M.A., Graham, N.A.J., Cinner, J.E., Dulvy, N.K., Loring, P.A., Jennings, S., Polunin, N.V.C., Fisk, A.T. and McClanahan, T.R. (2010) Transitional states in marine fisheries: adapting to predicted global change. Philosophical Transactions of the Royal Society B 365, 3753–3763.Google Scholar
MacNeil, M.A., McMeans, B.C., Hussey, N.E., Vecsei, P., Svavarsson, J., Kovacs, K.M., Lydersen, C., Treble, M.A., Skomal, G.B., Ramsey, M. and Fisk, A.T. (2012) Biology of the Greenland shark Somniosus microcephalus. Journal of Fish Biology 80, 991–1018.Google Scholar
McArdle, B.H. and Anderson, M.J. (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82, 290–297.Google Scholar
McMeans, B.C., Arts, M.T. and Fisk, A.T. (2012) Similarity between predator and prey fatty acid profiles is tissue dependent in Greenland sharks (Somniosus microcephalus): implications for diet reconstruction. Journal of Experimental Marine Biology and Ecology 429, 55–63.Google Scholar
McMeans, B.C., Arts, M.T. and Fisk, A.T. (2015) Impacts of food web structure and feeding behavior on mercury exposure in Greenland sharks (Somniosus microcephalus). Science of the Total Environment 509–510, 216–225.Google Scholar
McMeans, B.C., Arts, M.T., Lydersen, C., Kovacs, K.M., Hop, H., Falk-Petersen, S. and Fisk, A.T. (2013) The role of Greenland sharks (Somniosus microcephalus) in an Arctic ecosystem: assessed via stable isotopes and fatty acids. Marine Biology 160, 1223–1238.Google Scholar
McMeans, B.C., Svavarsson, J., Dennard, S. and Fisk, A.T. (2010) Diet and resource use among Greenland sharks (Somniosus microcephalus) and teleosts sampled in Icelandic waters, using δ13C, δ15N, and mercury. Canadian Journal of Fisheries and Aquatic Sciences 67, 1428–1438.Google Scholar
Overpeck, J.T., Strum, M., Francis, J.A., Perovich, D.K., Serreze, M.C., Benner, R., Carmack, E.C., Chapin, F.S. III, Gerlach, S.C., Hamilton, L.C., Hinzman, L.D., Holland, M., Huntington, H.P., Key, J.R., Lloyd, A.H., MacDonald, G.M., McFadden, J., Noone, D., Prowse, T.D., Schlosser, P., and Vörösmarty, C. (2005) Arctic system on trajectory to new, seasonally ice-free state. Eos, Transactions of the American Geophysical Union 86, 309–313.Google Scholar
Pethybridge, H., Daley, R.K. and Nichols, P.D. (2011) Diet of demersal sharks and chimaeras inferred by fatty acid profiles and stomach content analysis. Journal of Experimental Marine Biology and Ecology 409, 290–299.Google Scholar
Pethybridge, H., Daley, R.K., Virtue, P. and Nichols, P.D. (2010) Lipid composition and partitioning of deepwater chondrichthyans: inferences of feeding ecology and distribution. Marine Biology 157, 1367–1384.Google Scholar
R Core Team (2015) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, available at http://www.R-project.org/Google Scholar
Søreide, J.E., Leu, E., Berge, J., Graeve, M. and Falk-Petersen, S. (2010) Timing of blooms, algal food quality and Calanus glacialis reproduction and growth in a changing Arctic. Global Change Biology 16, 3154–3163.Google Scholar
Stewart, C., Iverson, S. and Field, C. (2014) Testing for a change in diet using fatty acid signatures. Environmental and Ecological Statistics 21, 775–792.Google Scholar
Thiemann, G.W., Iverson, S.J., Stirling, I. and Obbard, M.E. (2011) Individual patterns of prey selection and dietary specialization in an Arctic marine carnivore. Oikos 120, 1469–1478.CrossRefGoogle Scholar
Wyllie-Echeverria, T. and Wooster, W.S. (1998) Year-to-year variations in Bering Sea ice cover and some consequences for fish distributions. Fisheries Oceanography 7, 159–170.Google Scholar
Supplementary material: File

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