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DNA as a Dietary Biomarker in Antarctic Krill, Euphausia superba

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Abstract

The diet of Antarctic krill (Euphausia superba) has been studied using a variety of techniques, but current methods still suffer from problems that are difficult to solve. This study examined an alternative approach utilizing DNA as a prey biomarker. Methods were developed for the preservation, extraction, and identification of prey DNA from krill collected in the field. Group-specific polymerase chain reaction (PCR) was used to amplify diatom prey (Phylum: Bacillariophyta) and the results from DNA clone libraries were compared with microscopic diet analysis. DNA analysis was superior to microscopy for prey detection. However, differences in prey relative abundance estimates between the two techniques suggested some bias in the DNA-based estimates. Quantification showed that large amounts of prey DNA had been successfully preserved and extracted. Overall the results suggest that the application of DNA-based diet analysis to krill warrants further investigation, particularly for prey that are difficult to study using other methods.

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References

  • N Agusti SP Shayler JD Harwood IP Vaughan KD Sunderland WOC Symondson (2003) ArticleTitleCollembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers Mol Ecol 12 3467–3475 Occurrence Handle10.1046/j.1365-294X.2003.02014.x

    Article  Google Scholar 

  • SF Altschul W Gish W Miller EW Myers DJ Lipman (1990) ArticleTitleBasic local alignment search tool J Mol Biol 215 403–410 Occurrence Handle10.1006/jmbi.1990.9999

    Article  Google Scholar 

  • A Atkinson R Snyder (1997) ArticleTitleKrill–copepod interactions at South Georgia, Antarctica, I. Omnivory by Euphausia superba Mar Ecol Prog Ser 160 63–76

    Google Scholar 

  • S Becker P Boger R Oehlmann A Ernst (2000) ArticleTitlePCR bias in ecological analysis: a case study for quantitative Taq nuclease assays in analyses of microbial communities Appl Environ Microbiol 66 4945–4953 Occurrence Handle10.1128/AEM.66.11.4945-4953.2000

    Article  Google Scholar 

  • LE Blankenship AA Yayanos (2005) ArticleTitleUniversal primers and PCR of gut contents to study marine invertebrate diets Mol Ecol 14 891–899 Occurrence Handle10.1111/j.1365-294X.2005.02448.x

    Article  Google Scholar 

  • DP Chandler JK Fredrickson FJ Brockman (1997) ArticleTitleEffect of PCR template concentration on the composition and distribution of total community 16S rDNA clone libraries Mol Ecol 6 475–482 Occurrence Handle10.1046/j.1365-294X.1997.00205.x

    Article  Google Scholar 

  • JR Cole B Chai TL Marsh RJ Farris Q Wang SA Kulam S Chandra DM McGarrell TM Schmidt GM Garrity JM Tiedje (2003) ArticleTitleThe Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy Nucleic Acids Res 31 442–443 Occurrence Handle10.1093/nar/gkg039

    Article  Google Scholar 

  • A Cooper HN Poinar (2000) ArticleTitleAncient DNA: do it right or not at all Science 289 1139 Occurrence Handle10.1126/science.289.5482.1139b

    Article  Google Scholar 

  • MN Dawson KA Raskoff DK Jacobs (1998) ArticleTitleField preservation of marine invertebrate tissue for DNA analyses Mol Mar Biol Biotechnol 7 145–152

    Google Scholar 

  • BE Deagle DJ Tollit SN Jarman MA Hindell AW Trites NJ Gales (2005) ArticleTitleMolecular scatology as a tool to study diet: analysis of prey DNA in scats from captive Steller sea lions Mol Ecol 14 1831–1842 Occurrence Handle10.1111/j.1365-294X.2005.02531.x

    Article  Google Scholar 

  • LE Flournoy RP Adams RN Pandy (1996) ArticleTitleInterim and archival preservation of plant specimens in alcohols for DNA studies BioTechniques 20 657–660

    Google Scholar 

  • Z Genhai (1993) ArticleTitleAnalysis of the stomach contents of Antarctic krill, Euphausia superba Dana Antarct Res 4 11–20

    Google Scholar 

  • LJ Gurney PW Froneman EA Pakhomov CD McQuaid (2001) ArticleTitleTrophic positions of three euphausiid species from the Prince Edward Islands (Southern Ocean): implications for the pelagic food web structure Mar Ecol Prog Ser 217 167–174

    Google Scholar 

  • KL Haberman RM Ross LB Quetin M Vernet GA Nevitt W Kozlowski (2002) ArticleTitleGrazing by Antarctic krill Euphausia superba on Phaeocystis antarctica: an immunochemical approach Mar Ecol Prog Ser 241 139–149

    Google Scholar 

  • KL Haberman RM Ross LB Quetin (2003) ArticleTitleDiet of the Antarctic krill (Euphausia superba Dana): II. Selective grazing in mixed phytoplankton assemblages J Exp Mar Biol Ecol 283 97–113 Occurrence Handle10.1016/S0022-0981(02)00467-7

    Article  Google Scholar 

  • W Hagen G Kattner A Terbruggen ES Vleet ParticleVan (2001) ArticleTitleLipid metabolism of the Antarctic krill Euphausia superba and its ecological implications Mar Biol 139 95–104 Occurrence Handle10.1007/s002270000527

    Article  Google Scholar 

  • GL Harper RA King CS Dodd JD Harwood DM Glen MW Bruford WOC Symondson (2005) ArticleTitleRapid screening of invertebrate predators for multiple prey DNA targets Mol Ecol 14 819–827 Occurrence Handle10.1111/j.1365-294X.2005.02442.x

    Article  Google Scholar 

  • TJ Hart (1934) ArticleTitleOn the phytoplankton of the south-west Atlantic and Bellingshausen Sea, 1929–31 Disc Rep 8 1–268

    Google Scholar 

  • L Hendriks R Baere ParticleDe Y Peer ParticleVan de J Neefs A Goris R Wachter ParticleDe (1991) ArticleTitleThe evolutionary position of the Rhodophyte Porphyra umbilicalis and the Basidiomycete Leucosporidium scotii among other eukaryotes as deduced from complete sequences of small ribosomal subunit RNA J Mol Evol 32 167–177 Occurrence Handle10.1007/BF02515389

    Article  Google Scholar 

  • Hoogendoorn M, Heimpel GE (2001) PCR-based gut content analysis of insect predators, using ribosomal ITS-1 fragments from prey to estimate predation frequency. Mol Ecol 10, 2059–2067

    Google Scholar 

  • SN Jarman B Deagle NJ Gales (2004) ArticleTitleGroup-specific polymerase chain reaction for DNA-based analysis of species diversity and identity in dietary samples Mol Ecol 13 1313–1322 Occurrence Handle10.1111/j.1365-294X.2004.02109.x

    Article  Google Scholar 

  • ML Kasper AF Reeson SJB Cooper KD Perry AD Austin (2004) ArticleTitleAssessment of prey overlap between a native (Polistes humilis) and an introduced (Vespula germanica) social wasp using morphology and phylogenetic analyses of 16S rDNA Mol Ecol 13 2037–2048 Occurrence Handle10.1111/j.1365-294X.2004.02193.x

    Article  Google Scholar 

  • S Kumar K Tamura IB Jakobsen M Nei (2001) ArticleTitleMEGA2, Molecular Evolutionary Genetics Analysis Software Bioinformatics 17 1244–1245 Occurrence Handle10.1093/bioinformatics/17.12.1244

    Article  Google Scholar 

  • V Loeb V Siegel O Holm Hansen R Hewitt W Fraser W Trivelpiece S Trivelpiece (1997) ArticleTitleEffects of sea-ice extent and krill or salp dominance on the Antarctic food web Nature 387 897–900 Occurrence Handle10.1038/43174

    Article  Google Scholar 

  • J Marr (1962) ArticleTitleThe natural history and geography of the Antarctic krill (Euphausia superba Dana) Disc Rep 32 33–464

    Google Scholar 

  • L Masner (1994) ArticleTitleEffect of low temperature on preservation and quality of insect specimens stored in alcohol Insect Collect News 9 14–15

    Google Scholar 

  • CP Meyer G Paulay (2005) ArticleTitleDNA barcoding: error rates based on comprehensive sampling Plos Biol 3 2229–2238

    Google Scholar 

  • JC Nejstgaard ME Frischer CL Raule R Gruebel KE Kohlberg PG Verity (2003) ArticleTitleMolecular detection of algal prey in copepod guts and fecal pellets Limnol Oceanogr Meth 1 29–38

    Google Scholar 

  • EA Pakhomov R Perissinotto PW Froneman DGM Miller (1997) ArticleTitleEnergetics and feeding dynamics of Euphausia superba in the South Georgia region during the summer of 1994 J Plankton Res 19 399–423

    Google Scholar 

  • R Perissinotto L Gurney EA Pakhomov (2000) ArticleTitleContribution of heterotrophic material to diet and energy budget of Antarctic krill, Euphausia superba Mar Biol 136 129–135 Occurrence Handle10.1007/s002270050015

    Article  Google Scholar 

  • CF Phleger MM Nelson BD Mooney PD Nichols (2002) ArticleTitleInterannual and between species comparison of the lipids, fatty acids and sterols of Antarctic krill from the US AMLR Elephant Island survey area Comp Biochem Phys B 131 733–747 Occurrence Handle10.1016/S1096-4959(02)00021-0

    Article  Google Scholar 

  • MF Polz CM Cavanaugh (1998) ArticleTitleBias in template-to-product ratios in multitemplate PCR Appl Environ Microbiol 64 3724–3730

    Google Scholar 

  • CD Prokopowich TR Gregory TJ Crease (2003) ArticleTitleThe correlation between rDNA copy number and genome size in eukaryotes Genome Res 46 48–50 Occurrence Handle10.1139/g02-103

    Article  Google Scholar 

  • LB Quetin RM Ross (1991) ArticleTitleBehavioral and physiological characteristics of the Antarctic krill, Euphausia superba Am Zool 31 49–63

    Google Scholar 

  • S Rozen HJ Skaletsky (2000) Primer3 on the WWW for general users and for biologist programmers S Krawetz S Misener (Eds) Bioinformatics Methods and Protocols (Methods in Molecular Biology) Humana Press Totowa, NJ 365–386

    Google Scholar 

  • D Rubinoff S Cameron K Will (2006) ArticleTitleAre plant DNA barcodes a search for the Holy Grail? Trends Ecol Evol 21 1–2 Occurrence Handle10.1016/j.tree.2005.10.019

    Article  Google Scholar 

  • K Schmidt A Atkinson D Stubing JW McClelland JP Montoya M Voss (2003) ArticleTitleTrophic relationships among Southern Ocean copepods and krill: some uses and limitations of a stable isotope approach Limnol Oceanogr 48 277–289 Occurrence Handle10.4319/lo.2003.48.1.0277

    Article  Google Scholar 

  • D Steinke M Vences W Salzburger A Meyer (2005) ArticleTitleTaxl, a software tool for DNA barcoding using distance methods Philos Trans Roy Soc B 360 1975–1980 Occurrence Handle10.1098/rstb.2005.1729

    Article  Google Scholar 

  • WM Strauss (1998) Preparation of genomic DNA from mammalian tissue FM Ausubel RE Brent DD Kingston JG Moore JA Seidman KS Smith (Eds) Current Protocols in Molecular Biology John Wiley & Sons New York 221–223

    Google Scholar 

  • D Stubing W Hagen K Schmidt (2003) ArticleTitleOn 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 Occurrence Handle10.4319/lo.2003.48.4.1685

    Article  Google Scholar 

  • M Suzuki MS Rappe SJ Giovannoni (1998) ArticleTitleKinetic bias in estimates of coastal picoplankton community structure obtained by measurements of small-subunit rRNA gene PCR amplicon length heterogeneity Appl Environ Microbiol 64 4522–4529

    Google Scholar 

  • WO Symondson (2002) ArticleTitleMolecular identification of prey in predator diets Mol Ecol 11 627–641 Occurrence Handle10.1046/j.1365-294X.2002.01471.x

    Article  Google Scholar 

  • K Tamura M Nei (1993) ArticleTitleEstimation of the number of nucleotide substitutions in the control region of mitochondrial-DNA in humans and chimpanzees Mol Biol Evol 10 512–526

    Google Scholar 

  • JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe ClustalX windows interface, flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 24 4876–4882 Occurrence Handle10.1093/nar/25.24.4876

    Article  Google Scholar 

  • RH Zaidi Z Jaal NJ Hawkes J Hemingway WO Symondson (1999) ArticleTitleCan multiple-copy sequences of prey DNA be detected amongst the gut contents of invertebrate predators? Mol Ecol 8 2081–2087 Occurrence Handle10.1046/j.1365-294x.1999.00823.x

    Article  Google Scholar 

  • Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comp Biol 7, 203–214

    Google Scholar 

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Acknowledgments

We thank the captain and crew of RSV Aurora Australis for their assistance in collecting krill samples; Andrew Pankowski for supply of diatom cultures; and Bruce Deagle, Adam Smolenski, Andrew Pankowski, and Andrew Bissett for their valuable insight and discussion. This work was funded by the Australian Antarctic Division as part of the Antarctic Marine Living Resources (AMLR) Program.

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Authors and Affiliations

  1. Institute of Antarctic and Southern Ocean Studies, University of Tasmania, Private Bag 77, Hobart, Tasmania, 7001, Australia

    A. J. Passmore & A. McMinn

  2. Department of the Environment and Heritage, Australian Antarctic Division, Channel Highway, Kingston, Tasmania, 7050, Australia

    S. N. Jarman, S. Kawaguchi & S. Nicol

  3. Zoology Department, University of Tasmania, Private Bag 5, Hobart, Tasmania, 7001, Australia

    K. M. Swadling

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  1. A. J. Passmore
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  2. S. N. Jarman
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  3. K. M. Swadling
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  4. S. Kawaguchi
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  5. A. McMinn
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  6. S. Nicol
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Correspondence to A. J. Passmore.

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Passmore, A.J., Jarman, S.N., Swadling, K.M. et al. DNA as a Dietary Biomarker in Antarctic Krill, Euphausia superba . Mar Biotechnol 8, 686–696 (2006). https://doi.org/10.1007/s10126-005-6088-8

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  • DOI: https://doi.org/10.1007/s10126-005-6088-8

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