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Molecular analyses of gut contents: elucidating the feeding of co-occurring salps in the Lazarev Sea from a different perspective

Published online by Cambridge University Press:  12 May 2014

Katja Metfies*
Affiliation:
Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany Jacobs University Bremen, Campus Ring 1, 28759 Bremen, Germany
Anja Nicolaus
Affiliation:
Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany
Lena Von Harbou
Affiliation:
Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany
Ulrich Bathmann
Affiliation:
Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany Leibniz-Institute for Baltic Sea Research, Seestrasse 15, 18119 Rostock, Germany
Ilka Peeken
Affiliation:
Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany MARUM – Center for Marine Environmental Sciences, University of Bremen, 28334 Bremen, Germany

Abstract

The diet of Antarctic salps was elucidated by investigating their gut content using automated ribosomal intergenic spacer analysis (ARISA) and 454-pyrosequencing. Salp samples were collected during the Lazarev Sea Krill Study in the western Weddell Sea (summer 2005–06 and 2007–08, autumn 2004 and winter 2006). Two salp species, Salpa thompsoni and Ihlea racovitzai, both occur in the Southern Ocean and can overlap geographically and seasonally. We provide evidence that, despite the non-selective feeding mechanism, the two co-occurring salp species might have different niches within a habitat. ARISA-patterns of 93 gut content samples revealed strong differences between the two salp species, even at the same sampling site. These differences were confirmed by 454-pyrosequencing of the V4-18S rDNA of ten salps. The pyrosequencing data indicate that flagellates, in particular dinophyceae, constitute a high proportion of the sequence reads identified in the gut content of both salp species. However, within the dinophyceae, differences in the read composition were detected between the two salp species. This supports the findings of a previous study where fatty acid signatures indicate a flagellate-based diet, even though microscopic analyses identified diatoms as the dominant component of salp gut contents.

Type
Biological Sciences
Copyright
© Antarctic Science Ltd 2014 

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References

Alldredge, A.L. & Madin, L.P. 1982. Pelagic tunicates - unique herbivores in the marine plankton. Bioscience, 32, 655663.Google Scholar
Atkinson, A., Siegel, V., Pakhomov, E. & Rothery, P. 2004. Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature, 432, 100103.Google Scholar
Behnke, A., Barger, K.J., Bunge, J. & Stoeck, T. 2010. Spatio-temporal variations in protistan communities along an O-2/H2S gradient in the anoxic Framvaren Fjord (Norway). FEMS Microbiology Ecology, 72, 89102.Google Scholar
Dalsgaard, J., St John, M., Kattner, G., Müller-Navarra, D. & Hagen, W. 2003. Fatty acid trophic markers in the pelagic marine environment. Advances in Marine Biology, 46, 225340.CrossRefGoogle ScholarPubMed
Diez, B., Massana, R., Estrada, M. & Pedros-Alio, C. 2004. Distribution of eukaryotic picoplankton assemblages across hydrographic fronts in the Southern Ocean, studied by denaturing gradient gel electrophoresis. Limnology and Oceanography, 49, 10221034.Google Scholar
Dubischar, C.D., Pakhomov, E.A., von Harbou, L., Hunt, B.P.V. & Bathmann, U.V. 2012. Salps in the Lazarev Sea, Southern Ocean: II. Biochemical composition and potential prey value. Marine Biology, 159, 1524.Google Scholar
Dunbar, J., Ticknor, L.O. & Kuske, C.R. 2000. Assessment of microbial diversity in four southwestern United States soils by 16S rRNA gene terminal restriction fragment analysis. Applied and Environmental Microbiology, 66, 29432950.Google Scholar
Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C. & Knight, R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics, 27, 21942200.Google Scholar
Finn, R.D., Clements, J. & Eddy, S.R. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Research, 39, W29W37.Google Scholar
Fraser, L., Strzezek, J. & Kordan, W. 2011. Effect of freezing on sperm nuclear DNA. Reproduction in Domestic Animals, 46, 1417.Google Scholar
Garrison, D.L., Buck, K.R. & Gowing, M.M. 1993. Winter plankton assemblage in the ice edge zone of the Weddell and Scotia Seas – composition, biomass and spatial distributions. Deep-Sea Research Part I - Oceanographic Research Papers, 40, 311338.Google Scholar
Joo, S., Lee, S.R. & Park, S. 2010. Monitoring of phytoplankton community structure using terminal restriction fragment length polymorphism (T-RFLP). Journal of Microbiological Methods, 81, 6168.Google Scholar
Kunin, V., Engelbrektson, A., Ochman, H. & Hugenholtz, P. 2010. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environmental Microbiology, 12, 118123.Google Scholar
Margulies, M., Egholm, M., Altman, W.E. et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature, 437, 376380.Google Scholar
Matsen, F.A., Kodner, R.B. & Armbrust, E.V. 2010. pplacer: linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics, 11, 10.1186/1471-2105-11-538.Google Scholar
Medlin, L.K., Metfies, K., Mehl, H., Wiltshire, K. & Valentin, K. 2006. Picoeukaryotic plankton diversity at the Helgoland time series site as assessed by three molecular methods. Microbial Ecology, 52, 5371.Google Scholar
Mendes, C.R.B., Tavano, V.M., Leal, M.C., de Souza, M.S., Brotas, V. & Garcia, C.A.E. 2013. Shifts in the dominance between diatoms and cryptophytes during three late summers in the Bransfield Strait (Antarctic Peninsula). Polar Biology, 36, 537547.Google Scholar
Metfies, K., Gescher, C., Frickenhaus, S., Niestroy, R., Wichels, A., Gerdts, G., Knefelkamp, B., Wiltshire, K. & Medlin, L. 2010. Contribution of the class cryptophyceae to phytoplankton structure in the German Bight. Journal of Phycology, 46, 11521160.Google Scholar
Metfies, K. & Medlin, L.K. 2008. Feasibility of transferring fluorescent in situ hybridization probes to an 18S rRNA gene phylochip and mapping of signal intensities. Applied and Environmental Microbiology, 74, 28142821.Google Scholar
Moline, M.A., Claustre, H., Frazer, T.K., Schofield, O. & Vernet, M. 2004. Alteration of the food web along the Antarctic Peninsula in response to a regional warming trend. Global Change Biology, 10, 19731980.Google Scholar
Nichols, P.D., Skerratt, J.H., Davidson, A., Burton, H. & McMeekin, T.A. 1991. Lipids of cultured Phaeocystis pouchetii – signatures for food-web, biochemical and environmental studies in Antarctica and the Southern Ocean. Phytochemistry, 30, 32093214.Google Scholar
Nickrent, D.L. & Sargent, M.L. 1991. An overview of the secondary structure of the V4-region of eukaryotic small subunit ribosomal RNA. Nucleic Acids Research, 19, 227235.Google Scholar
Nicol, S., Worby, A. & Leaper, R. 2008. Changes in the Antarctic sea ice ecosystem: potential effects on krill and baleen whales. Marine and Freshwater Research, 59, 361382.Google Scholar
Ono, A. & Moteki, M. 2013. Spatial distributions and population dynamics of two salp species, Ihlea racovitzai and Salpa thompsoni, in the waters north of Lutzow-Holm Bay (East Antarctica) during austral summers of 2005 and 2006. Polar Biology, 36, 807817.Google Scholar
Pakhomov, E.A., Dubischar, C.D., Strass, V., Brichta, M. & Bathmann, U.V. 2006. The tunicate Salpa thompsoni ecology in the Southern Ocean. I. Distribution, biomass, demography and feeding ecophysiology. Marine Biology, 149, 609623.Google Scholar
Pakhomov, E.A., Froneman, P.W. & Perissinotto, R. 2002. Salp/krill interactions in the Southern Ocean: spatial segregation and implications for the carbon flux. Deep-Sea Research Part II - Topical Studies in Oceanography, 49, 18811907.Google Scholar
Pakhomov, E.A., Hall, J., Williams, M.J.M., Hunt, B.P.V. & Stevens, C.J. 2011. Biology of Salpa thompsoni in waters adjacent to the Ross Sea, Southern Ocean, during austral summer 2008. Polar Biology, 34, 257271.CrossRefGoogle Scholar
Perissinotto, R., Mayzaud, P., Nichols, P.D. & Labat, J.P. 2007. Grazing by Pyrosoma atlanticum (Tunicata, Thaliacea) in the south Indian Ocean. Marine Ecology Progress Series, 330, 111.Google Scholar
Smetacek, V., Assmy, P. & Henjes, J. 2004. The role of grazing in structuring Southern Ocean pelagic ecosystems and biogeochemical cycles. Antarctic Science, 16, 541558.CrossRefGoogle Scholar
Tanimura, A., Kawaguchi, S., Oka, N., Nishikawa, J., Toczko, S., Takahashi, K.T., Terazaki, M., Odate, T., Fukuchi, M. & Hosie, G. 2008. Abundance and grazing impacts of krill, salps and copepods along the 140 degrees E meridian in the Southern Ocean during summer. Antarctic Science, 20, 365379.Google Scholar
Tobe, K., Meyer, B. & Fuentes, V. 2010. Detection of zooplankton items in the stomach and gut content of larval krill, Euphausia superba, using a molecular approach. Polar Biology, 33, 407414.Google Scholar
Vargas, C.A. & Madin, L.P. 2004. Zooplankton feeding ecology: clearance and ingestion rates of the salps Thalia democratica, Cyclosalpa affinis and Salpa cylindrica on naturally occurring particles in the Mid-Atlantic Bight. Journal of Plankton Research, 26, 827833.CrossRefGoogle Scholar
Von Bodungen, B., Noëthig, E.M. & Sui, Q. 1988. New production of phytoplankton and sedimentation during summer 1985 in the south eastern Weddell Sea. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 90, 475487.Google Scholar
von Harbou, L., Dubischar, C.D., Pakhomov, E.A., Hunt, B.P.V., Hagen, W. & Bathmann, U.V. 2011. Salps in the Lazarev Sea, Southern Ocean: I. Feeding dynamics. Marine Biology, 158, 20092026.Google Scholar
Woese, C.R. 1987. Bacterial evolution. Microbiological Reviews, 51, 221271.Google Scholar
Wolf, C., Frickenhaus, S., Kilias, E.S., Peeken, I. & Metfies, K. 2013. Regional variability in eukaryotic protist communities in the Amundsen Sea. Antarctic Science, 25, 741751.CrossRefGoogle Scholar
Zhu, F., Massana, R., Not, F., Marie, D. & Vaulot, D. 2005. Mapping of picoeucaryotes in marine ecosystems with quantitative PCR of the 18S rRNA gene. FEMS Microbiology Ecology, 52, 7992.Google Scholar
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