Jump to ContentJump to Main Navigation
Show Summary Details
More options …

DNA Barcodes

Ed. by Mitchell, Andrew

1 Issue per year

Emerging Science

Open Access
See all formats and pricing
More options …

DNA barcoding increases resolution and changes structure in Canadian boreal shield lake food webs

Timothy J. Bartley
  • Corresponding author
  • Department of Integrative Biology, University of Guelph, 50 Stone Road East, Guelph, Ontario, Canada N1G 2W1
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Heather E. Braid
  • Institute for Applied Ecology New Zealand, Auckland University of Technology, Private Bag 92006, Auckland, New Zealand 1010
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Kevin S. McCann
  • Department of Integrative Biology, University of Guelph, 50 Stone Road East, Guelph, Ontario, Canada N1G 2W1
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Nigel P. Lester
  • Science and Research Branch, Ontario Ministry of Natural Resources, Peterborough, Ontario, Canada K9J 7B8
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Brian J. Shuter
  • Science and Research Branch, Ontario Ministry of Natural Resources, Peterborough, Ontario, Canada K9J 7B8
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Brian J. Shuter / Robert H. Hanner
  • Biodiversity Institute of Ontario, University of Guelph, 50 Stone Road East, Guelph, Ontario, Canada N1G 2W1
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2015-11-26 | DOI: https://doi.org/10.1515/dna-2015-0005


Food webs are important in understanding the structure, function, and behaviour of ecosystems, but, due to methodological limitations, are often poorly resolved in ways that impact food-web properties. Although DNA barcoding has proven useful in determining the diet of consumers, few studies have used this technique to determine food-web structure. These studies report mixed impacts on various food-web properties, but are limited by their taxonomic focus and their failure to evaluate DNA barcoding for both diet analysis and food-web structure. In this study, we show that, when compared to a morphological approach, DNA barcoding increases foodweb resolution by increasing the number and frequency of prey species identified in the stomach contents of eight species of Canadian boreal shield predatory fishes. In addition, we observed differences in food-web structure, such as increased generalism, habitat coupling, and omnivory, that have strong implications for food-web stability and dynamics. We conclude that DNA barcoding is a powerful tool to evaluate how resolution impacts foodweb properties and can help further our understanding of how food webs are structured by identifying feeding interactions in an unprecedented and highly detailed manner.

This article offers supplementary material which is provided at the end of the article.

Keywords: COI; diet analysis; feeding links; morphology; omnivory; predatory fish; prey species; resolution; stomach contents; trophic interactions


  • [1] Rooney N., McCann K.S., Integrating food web diversity, structure and stability, Trends Ecol. Evol., 2012, 27, 40-46CrossrefGoogle Scholar

  • [2] Cohen J.E., Beaver R.A., Cousins S.H., DeAngelis D.L., Goldwasser L., Heong K.L., et al., Improving food webs, Ecology, 1993, 74, 252-258CrossrefGoogle Scholar

  • [3] Pimm S.L., Lawton J.H., Cohen J.E., Food web patterns and their consequences, Nature, 1991, 350, 669-674.Google Scholar

  • [4] May R., The structure of food webs, 1983, Nature, 301, 566-568Google Scholar

  • [5] Martinez N.D., Artifacts or attributes? Effects of resolution on the Little Rock Lake food web, Ecol. Monogr., 1991, 61, 367-392.CrossrefGoogle Scholar

  • [6] Martinez N.D., Effects of resolution on food web structure, Oikos, 1993, 66, 403-412CrossrefGoogle Scholar

  • [7] Martinez N.D., Hawkins B.A., Dawah H.A., Feifarek B.P., Effects of sampling effort on characterization of food-web structure, Ecology, 1999, 80, 1044-1055.Google Scholar

  • [8] Dunne J.A., Williams R.J., Martinez N.D., Food-web structure and network theory: the role of connectance and size, Proc. Natl. Acad. Sci. U.S.A., 2002, 99, 12917-12922.Google Scholar

  • [9] Krause A.E., Frank K.A., Mason D.M., Ulanowicz R.E., Compartments revealed in food-web structure, Nature, 2003, 426, 282-285Google Scholar

  • [10] Yodzis P., Winemiller K.O., In search of operational trophospecies in a tropical aquatic food web, Oikos, 1999, 87, 327-340Google Scholar

  • [11] Polis G.A., Complex trophic interactions in deserts: an empirical critique of food-web theory, Am. Nat., 1991, 138, 123-155Google Scholar

  • [12] Vander Zanden M.J., Rasmussen J.B., Primary consumer δ13C and δ15N and the trophic position of aquatic consumers, Ecology, 1999, 80, 1395-1404Google Scholar

  • [13] Vander Zanden M.J., Vadeboncoeur Y., Fishes as integrators of benthic and pelagic food webs in lakes, Ecology, 2002, 83, 2152-2161Google Scholar

  • [14] Vander Zanden M.J., Casselman J.M., Rasmussen J.B., Stable isotope evidence for the food web consequences of species invasions in lakes, Nature, 1999, 401, 464-467Google Scholar

  • [15] King R.A., Read D.S., Traugott M., Symondson W.O.C., Molecular analysis of predation: a review of best practice for DNA-based approaches, Mol. Ecol., 2008, 17, 947-963CrossrefGoogle Scholar

  • [16] Pompanon F., Deagle B.E., Symondson W.O.C., Brown D.S., Jarman S.N., Taberlet P., Who is eating what: diet assessment using next generation sequencing, Mol. Ecol., 2012, 21, 1931-1950CrossrefGoogle Scholar

  • [17] Sheppard S.K., Harwood J.D., Advances in molecular ecology: tracking trophic links through predator-prey food-webs, Funct. Ecol., 2005, 19, 751-762CrossrefGoogle Scholar

  • [18] McCann K.S., Protecting biostructure, Nature, 2007, 446, 29Google Scholar

  • [19] Valentini A., Pompanon F., Taberlet P., DNA barcoding for ecologists. Trends Ecol. Evol., 2009, 24, 110-117CrossrefGoogle Scholar

  • [20] Ratnasingham S., Hebert P.D.N., BOLD: The Barcode of Life Data System (http://www.barcodinglife.org), Mol. Ecol. Notes, 2007, 7, 355-364CrossrefGoogle Scholar

  • [21] Hebert P.D.N., Cywinska A., Ball S.L., deWaard J.R., Biological identifications through DNA barcodes, Proc. Biol. Sci., 2003, 270, 313-321Google Scholar

  • [22] Wong E.H.K., Hanner R.H., DNA barcoding detects market substitution in North American seafood, Food Res. Int., 2008, 41, 828-837CrossrefGoogle Scholar

  • [23] Hanner R.H., Becker S., Ivanova N.V., Steinke D., FISH-BOL and seafood identification: geographically dispersed case studies reveal systemic market substitution across Canada, Mitochondrial DNA, 2011, 22, 106-122Google Scholar

  • [24] Clare E.L., Fraser E.E., Braid H.E., Fenton M.B., Hebert P.D.N., Species on the menu of a generalist predator, the eastern red bat (Lasiurus borealis): using a molecular approach to detect arthropod prey, Mol. Ecol., 2009, 18, 2532-2542CrossrefGoogle Scholar

  • [25] Eitzinger B., Traugott M., Which prey sustains cold-adapted invertebrate generalist predators in arable land? Examining prey choices by molecular gut-content analysis. J. Appl. Ecol., 2011, 48, 591-599CrossrefGoogle Scholar

  • [26] Blankenship L.E., Yayanos A.A., Universal primers and PCR of gut contents to study marine invertebrate diets. Mol. Ecol., 2005, 14, 891-899CrossrefGoogle Scholar

  • [27] Braid H.E., Deeds J., DeGrasse S.L., Wilson J.J., Osborne J., Hanner R.H., Preying on commercial fisheries and accumulating paralytic shellfish toxins: a dietary analysis of invasive Dosidicus gigas (Cephalopoda Ommastrephidae) stranded in Pacific Canada, Mar. Biol., 2012, 159, 25-31Google Scholar

  • [28] Bowser A.K., Diamond A.W., Addison J.A., From puffins to plankton: a DNA-Based analysis of a seabird food chain in the northern Gulf of Maine, PLoS One, 2013, 8, e83152Google Scholar

  • [29] Dunn M.R., Szabo A., McVeagh M.S., Smith P.J., The diet of deepwater sharks and the benefits of using DNA identification of prey, Deep Sea Res. Part I Oceanogr. Res. Pap., 2010, 57, 923-930Google Scholar

  • [30] Paquin M.M., Buckley T.W., Hibpshman R.E., Canino M.F., DNA-based identification methods of prey fish from stomach contents of 12 species of eastern North Pacific groundfish. Deep Sea Res. Part I Oceanogr. Res. Pap., 2014, 85, 110-117Google Scholar

  • [31] Zeale M.R.K., Butlin R.K., Barker G.L.A., Lees D.C., Jones G., Taxon-specific PCR for DNA barcoding arthropod prey in bat feces, Mol. Ecol. Resour., 2011, 11, 236-244CrossrefGoogle Scholar

  • [32] Sheppard S.K., Bell J., Sunderland K.D., Fenlon J., Skervin D., Symondson W.O.C., Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators, Mol. Ecol., 2005, 14, 4461-4468CrossrefGoogle Scholar

  • [33] Kaartinen R., Stone G.N., Hearn J., Lohse K., Roslin T., Revealing secret liaisons: DNA barcoding changes our understanding of food webs, Ecol. Entomol., 2010, 35, 623-638CrossrefGoogle Scholar

  • [34] Smith M.A., Eveleigh E.S., McCann K.S., Merilo M.T., McCarthy P.C., Van Rooyen K.I., Barcoding a quantified food web: crypsis, concepts, ecology and hypotheses, PLoS One, 2011, 6, e14424Google Scholar

  • [35] Wirta H.K., Hebert P.D.N., Kaartinen R., Prosser S.W., Varkonyi G., Roslin T., Complementary molecular information changes our perception of food web structure, Proc. Natl. Acad. Sci. U.S.A., 2014, 111, 1885-1890CrossrefGoogle Scholar

  • [36] Hebert P.D.N., Penton E.H., Burns J.M., Janzen D.H., Hallwahs W., Ten species in one: DNA barcoding reveals cryptic species in the Neotropical skipper butterfly Astraptes fulgerator, Proc. Natl. Acad. Sci. U.S.A., 2004, 101, 14812-14817Google Scholar

  • [37] Smith M.A., Wood D.M., Janzen D.H., Hallwachs W., Hebert P.D.N., DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists, Proc. Natl. Acad. Sci. U.S.A., 2007, 104, 4967-4972Google Scholar

  • [38] Tunney T.D., McCann K.S., Lester N.P., Shuter B.P., Effects of differential habitat warming on complex communities, Proc. Natl. Acad. Sci. U.S.A., 2014, 111, 8077-8082Google Scholar

  • [39] Dolson R., McCann K.S., Rooney N., Ridgway M., Lake morphometry predicts the degree of habitat coupling by a mobile predator, Oikos, 2009, 118, 1230-1238CrossrefGoogle Scholar

  • [40] Post D.M., Pace M.L., Hairston N.G., Ecosystem size determines food-chain length in lakes. Nature, 2000, 405, 1047-1049Google Scholar

  • [41] Scott W.B., Crossman E.J., Freshwater fishes of Canada, Fisheries Research Board of Canada, Ottawa, Ontario, Canada, 1973Google Scholar

  • [42] Sandstrom S., Rawson M., Lester N., Manual of instructions for broad-scale fish community monitoring; using North American (NA1) and Ontario small mesh (ON2) gillnets, Queen’s printer for Ontario, Peterborough, Ontario, Canada, 2013Google Scholar

  • [43] Holm E., Mandrak N., Burridge M., The ROM field guide to freshwater fishes of Ontario, Royal Ontario Museum, Toronto, Ontario, Canada, 2009Google Scholar

  • [44] Martin R.E., Pine R.H., DeBlase A.F., A manual of mammalogy with keys to the families of the world, McGraw Hill, Boston, Massachusetts, USA, 2000Google Scholar

  • [45] Marshall S., Insects: their natural history and diversity, Firefly Books, Richmond Hill, Ontario, Canada, 2007Google Scholar

  • [46] Key to freshwater macroinvertebrates in Ontario, St. Lawrence River Institute of Environmental Sciences, 2005Google Scholar

  • [47] Pennak R.W., Fresh-water invertebrates of the United States, Wiley, Toronto, Ontario, Canada, 1989Google Scholar

  • [48] Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R., DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates, Mol. Marine Biol. Biotechnol., 1994, 3, 294-299Google Scholar

  • [49] Ivanova N.V., Zemlak T.S., Hanner R.H., Hebert P.D.N., Universal primer cocktails for fish DNA barcoding, Mol. Ecol. Notes, 2007, 7, 544-548CrossrefGoogle Scholar

  • [50] Messing J., New M13 vectors for cloning, Meth. Enzymol., 1983, 101, 20-78.Google Scholar

  • [51] Ratnasingham S., Hebert P.D.N., A DNA-based registry for all animal species: the Barcode Index Number (BIN) system, PLoS One, 2013, 8, e66213Google Scholar

  • [52] Colwell R.K., EstimateS: Statistical estimation of species richness and shared species from samples, Version 9, 2013, Persistent URL: <http://purl.oclc.org/estimates>Google Scholar

  • [53] Ward R.D., Hanner R.H., Hebert P.D.N., The campaign to DNA barcode all fishes, FISH-BOL, J. Fish Biol., 2009, 74, 329-356CrossrefGoogle Scholar

  • [54] Murray D.C., Bunce M., Cannell B.L., Oliver R., Houston J., White N.E., et al., DNA-based faecal dietary analysis: a comparison of qPCR and high throughput sequencing approaches. PLoS One, 2011, 6, e25776Google Scholar

  • [55] McCann K.S., Hastings A., Huxel G.R., Weak trophic interactions and the balance of nature, Nature, 1998, 395, 794-798Google Scholar

  • [56] de Ruiter P.C., Neutel A.M., Moore J.C., Energetics, patterns of interaction strengths and stability in real ecosystems, Science, 1995, 269, 1257-1260 Google Scholar

  • [57] Clare E. L., Molecular detection of trophic interactions: emerging trends, distinct advantages, significant considerations an conservation applications, Evol. Appl., 2014, 7, 1144-1157CrossrefGoogle Scholar

  • [58] McCann K.S., Rasmussen J.B., Umbanhowar J., The dynamics of spatially coupled food webs. Ecol. Lett., 2005, 8, 513-523.CrossrefGoogle Scholar

  • [59] Rooney N., McCann K.S., Gellner G., Moore J.C., Structural asymmetry and the stability of diverse food webs, Nature, 2006, 442, 265-269Google Scholar

  • [60] Martinez N.D., Constant connectance in community food webs, Am. Nat., 1992, 139, 1208-1218Google Scholar

  • [61] Dunne J.A., The network structure of food webs, In: Pascual M., Dunne J.A. (Eds.), Ecological networks: linking structure to dynamics in food webs, Oxford University Press, city, country, 2006Google Scholar

  • [62] Gellner G., McCann K.S., Reconciling the omnivory-stability debate, Am. Nat., 2012, 179, 22-37Google Scholar

  • [63] Milo R., Shen-Orr S., Itzkovitz S., Kashtan N., Chklovskii D., Alon U., Network motifs: simple building blocks of complex networks, Science, 2002, 298, 824-827Google Scholar

  • [64] Bascompte J., Melian C.J., Simple trophic modules for complex food webs, Ecology, 2005, 86, 2868-2873CrossrefGoogle Scholar

  • [65] Stouffer D., Bascompte J., Understanding food-web persistence from local to global scales, Ecol. Lett., 2009, 13, 154-161.Google Scholar

  • [66] Rip J.M.K., McCann K.S., Lynn D.H., Fawcett S., An experimental test of a fundamental food web motif, Proc. Biol. Sci., 2010, 277, 1743-1749Google Scholar

  • [67] Wood M.J., Parasites entangled in food webs, Trends Parasitol., 2007, 23, 8-10CrossrefGoogle Scholar

  • [68] Lafferty K.D., Allesina S., Arim M., Briggs C.J., De Leo G., Dobson A.P., et al., Parasites in food webs: the ultimate missing links. Ecol. Lett., 2008, 11, 533-546CrossrefGoogle Scholar

  • [69] Pimm A. L., Food webs, The University of Chicago Press, Chicago, Illinois, USA, 2002Google Scholar

  • [70] Post D. M., The long and short of food-chain length, Trends Ecol. Evol., 2002, 17, 269-277CrossrefGoogle Scholar

  • [71] Paine R. T., Food web complexity and species diversity, Am. Nat., 1966, 100, 65-75CrossrefGoogle Scholar

  • [72] Lindeman R. L., The trophic-dynamic aspect of ecology, Ecology, 1942, 23, 399-417CrossrefGoogle Scholar

  • [73] Yodzis P., The stability of real ecosystems, Nature, 1981, 289, 674-676Google Scholar

  • [74] Berlow E. L., Neutel A. M., Cohen J. E., De Ruiter P. C., Ebenman B., Emmerson M., et al., Interaction strengths in food webs: issues and opportunities, J. Anim. Ecol., 2004, 73, 585-598CrossrefGoogle Scholar

  • [75] Wootton J. T., Emmerson M., Measurement of interaction strength in nature, Annu. Rev. Ecol. Evol. Syst., 2005, 36, 419-444CrossrefGoogle Scholar

  • [76] Pimm S. L., The balance of nature?: ecological issues in the conservation of species and communities, Chicago, Illinois, USA, 1991Google Scholar

  • [77] Pimm S. L., Lawton J. H., Are food webs divided into compartments?, J. Anim. Ecol., 1980, 49, 879-898CrossrefGoogle Scholar

  • [78] Pimm. S. L., Lawton J. H. On feeding on more than one trophic level, Nature, 1978, 275, 542-544 Google Scholar

About the article

Received: 2014-12-12

Accepted: 2015-06-08

Published Online: 2015-11-26

Published in Print: 2015-01-01

Citation Information: DNA Barcodes, ISSN (Online) 2299-1077, DOI: https://doi.org/10.1515/dna-2015-0005.

Export Citation

© 2015. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Supplementary Article Materials

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

Tyler D. Tunney, Stephen R. Carpenter, and M. Jake Vander Zanden
Ecology, 2017, Volume 98, Number 7, Page 1859
Tomas Roslin, Sanna Majaneva, and Elizabeth Clare
Genome, 2016, Volume 59, Number 9, Page 603

Comments (0)

Please log in or register to comment.
Log in