Skip to main content

Advertisement

Log in

DNA (meta)barcoding of biological invasions: a powerful tool to elucidate invasion processes and help managing aliens

  • Molecular Tools
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Biological invasions are a major threat to the world’s biodiversity with consequences on ecosystem structure and functioning, species evolution, and human well-being (through ecosystem services). Conservation of biological diversity and management of biological resources require multi-level management strategies on non-native species, in order to (1) prevent biological introductions, (2) detect non-native species at an early stage of the introduction, and (3) eradicate or maintain at a low level of population density non-native species that were successfully introduced. A pre-requisite to any control measures on non-native species is the ability to rapidly and accurately identify the putative threatening alien species. DNA barcoding, and its recent extension, DNA metabarcoding are complementary tools that have proved their value in the identification of living beings. Here we review their use in the identification of non-native species at several steps of the introduction processes, and how they can be applied in the control and management of biological introductions. Through examples covering various taxa and ecosystems (terrestrial, freshwater, marine), we highlight the strengths and weaknesses of approaches that we foresee as crucial in the implementation of early warning strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Amaral CRL, Brito PM, Silva DA, Carvalho EF (2013) Border biosecurity and the use of species identification techniques in the ornamental fish trade: the case of the South American freshwater pufferfishes. Forensic Sci Int Genet Suppl Ser 4(1):e236–e237

    Google Scholar 

  • Andersen K, Bird KL, Rasmussen M, Haile J et al (2012) Metabarcoding of ‘dirt’DNA from soil reflects vertebrate biodiversity. Mol Ecol 21(8):1966–1979

    CAS  PubMed  Google Scholar 

  • Armstrong K (2010) DNA barcoding: a new module in New Zealand’s plant biosecurity diagnostic toolbox. EPPO Bull 40:91–100

    Google Scholar 

  • Armstrong KF, Ball SL (2005) DNA barcodes for biosecurity: invasive species identification. Philos Trans R Soc Lond B 360:1813–1823

    CAS  Google Scholar 

  • Armstrong KF, McHugh P, Chinn W, Frampton ER, Walsh PJ (2003) Tussock moth species arriving on imported used vehicles determined by DNA analysis. NZ Plant Prot 56:16–20

    CAS  Google Scholar 

  • Ascunce MS, Nigg HN, Clark A (2009) Molecular identification of the economically important invasive citrus root weevil Diaprepes abbreviatus (Coleoptera: Curculionidae). Florida Entomol 92:167–171

    Google Scholar 

  • Ball SL, Armstrong KF (2006) DNA barcodes for insect pest identification: a test case with tussock moths (Lepidoptera: Lymantriidae). Can J For Res 36:337–350

    CAS  Google Scholar 

  • Bhadury P, Austen MC (2010) Barcoding marine nematodes: an improved set of nematode 18S rRNA primers to overcome eukaryotic co-interference. Hydrobiologia 641:245–251

    CAS  Google Scholar 

  • Bik HM, Porazinska DL, Creer S, Caporaso JG, Knight R, Thomas WK (2012) Sequencing our way towards understanding global eukaryotic biodiversity. Trends Ecol Evol 27:233–243

    PubMed Central  PubMed  Google Scholar 

  • Bishop JDD, Roby C, Yunnie ALE, Wood CA, Lévêque L, Turon X, Viard F (2013) The Southern Hemisphere ascidian Asterocarpa humilis is unrecognised but widely established in NW France and Great Britain. Biol Invasions 15:253–260

    Google Scholar 

  • Blaxter M, Mann J, Chapman T, Thomas F, Whitton C, Floyd R, Abebe E (2005) Defining operational taxonomic units using DNA barcode data. Philos Trans R Soc Lond B 360:1935–1943

    CAS  Google Scholar 

  • Bohmann K, Evans A, Gilbert MTP, Carvalho GR, Creer S, Knapp M et al (2014) Environmental DNA for wildlife biology and biodiversity monitoring. Trends EcolEvol 29:358–367

    Google Scholar 

  • Bonants P, Groenewald E, Rasplus JY, Maes M, de Vos P, Frey J, Boonham N, Nicolaisen M, Bertacini A, Robert V, Barker I, Kox L, Ravnikar M, Tomankova K, Caffier D, Li M, Armstrong K, Freitas-Astúa J, Stefani E, Cubero J, Mostert L (2010) QBOL: a new EU project focusing on DNA barcoding of quarantine organisms. EPPO Bull 40:30–33

    Google Scholar 

  • Bortolus A (2008) Error cascades in the biological sciences: the unwanted consequences of using bad taxonomy in ecology. Ambio 37:114–118

    PubMed  Google Scholar 

  • Bott NJ, Ophel-Keller KM, Sierp MT, Herdina, Rowling KP, McKay AC, Loo MGK, Tanner JE, Deveney MR (2010) Toward routine, DNA-based detection methods for marine pests. Biotech Adv 28:706–714

    CAS  Google Scholar 

  • Breton S, Doucet Beaupré H, Stewart DT, Hoeh WR, Blier PU (2007) The unusual system of doubly uniparental inheritance of mtDNA: Isn’t one enough? Trends Genet 23:465–474

    CAS  PubMed  Google Scholar 

  • Briski E, Bailey SA, Cristescu ME, MacIsaac HJ (2010) Efficacy of ‘saltwater flushing’ in protecting the Great Lakes from biological invasions by invertebrate eggs in ships’ ballast sediment. Freshw Biol 55:2414–2424

    Google Scholar 

  • Briski E, Bailey SA, MacIsaac HJ (2011a) Invertebrates and their dormant eggs transported in ballast sediments of ships arriving to the Canadian coasts and the Laurentian Great Lakes. Limnol Oceanogr 56:1929–1939

    Google Scholar 

  • Briski E, Cristescu ME, Bailey SA, MacIsaac HJ (2011b) Use of DNA barcoding to detect invertebrate invasive species from diapausing eggs. Biol Invasions 13:1325–1340

    Google Scholar 

  • Bucklin A, Steinke D, Blanco-Bercial L (2011) DNA barcoding of marine metazoa. Annu Rev Mar Sci 3:471–508

    Google Scholar 

  • Buhay JE (2009) “COI-like” sequences are becoming problematic in molecular systematic and DNA barcoding studies. J Crust Biol 29:96–110

    Google Scholar 

  • Callahan AG, Deibel D, McKenzie CH, Hall JR, Rise ML (2010) Survey of harbours in Newfoundland for indigenous and non-indigenous ascidians and an analysis of their cytochrome c oxidase I gene sequences. Aquat Inv 5:31–39

    Google Scholar 

  • Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr Mar Biol Annu Rev 23:313–371

    Google Scholar 

  • Carlton JT (2009) Deep invasion ecology and the assembly of communities in historical time. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer-Verlag, Berlin, pp 13–56

    Google Scholar 

  • Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82

    Google Scholar 

  • Carstens BC, Pelletier TA, Reid NM, Satler JD (2013) How to fail at species delimitation. Mol Ecol 22:4369–4383

    PubMed  Google Scholar 

  • Casiraghi M, Labra M, Ferri E, Galimberti A, De Mattia F (2010) DNA barcoding: a six-question tour to improve users’ awareness about the method. Brief Bioinform 11:440–453

    CAS  PubMed  Google Scholar 

  • Chapin FS III, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Diaz S (2000) Consequences of changing biodiversity. Nature 405:234–242

    CAS  PubMed  Google Scholar 

  • Chauvel B, Dessaint F, Cardinal-Legrand C, Bretagnolle F (2006) The historical spread of Ambrosia artemisiifolia L. in France from herbarium records. J Biogeogr 33:665–673

    Google Scholar 

  • Chown SL, Sinclair BJ, Jansen van Vuuren B (2008) DNA barcoding and the documentation of alien species establishment on sub-Antarctic Marion Island. Polar Biol 31:651–655

    Google Scholar 

  • Civille JC, Sayce K, Smith SD, Strong DR (2005) Reconstructing a century of Spartina alterniflora invasion with historical records and contemporary remote sensing. Ecoscience 12:330–338

    Google Scholar 

  • Clarke LJ, Soubrier J, Weyrich LS, Cooper A (2014) Environmental metabarcodes for insects: in silico PCR reveals potential for taxonomic bias. Mol Ecol Resour 14:1160–1170. doi:10.1111/1755-0998.12265

    CAS  PubMed  Google Scholar 

  • Coissac E, Riaz T, Puillandre N (2012) Bioinformatic challenges for DNA metabarcoding of plants and animals. Mol Ecol 21:1834–1847

    CAS  PubMed  Google Scholar 

  • Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10(2):135–141

    Google Scholar 

  • Collins RA, Armstrong KF, Meier R, Yi Y, Brown SDJ, Cruickshank RH, Keeling S, Johnston C (2012) Barcoding and border biosecurity: identifying cyprinid fishes in the aquarium trade. PLoS One 7:e28381

    PubMed Central  CAS  PubMed  Google Scholar 

  • Collins RA, Armstrong KF, Holyoake AJ, Keeling S (2013) Something in the water: biosecurity monitoring of ornamental fish imports using environmental DNA. Biol Invasions 15:1209–1215

    Google Scholar 

  • Cook CN, Mascia MB, Schwartz MW, Possingham HP, Fuller RA (2013) Achieving conservation science that bridges the knowledge–action boundary. Conserv Biol 27:669–678

  • Cristescu ME (2014) From barcoding single individuals to metabarcoding biological communities: towards an integrative approach to the study of global biodiversity. Trends Ecol Evol 29:566–571

    PubMed  Google Scholar 

  • Darling J, Blum M (2007) DNA-based methods for monitoring invasive species: a review and prospectus. Biol Invasions 9:751–765

    Google Scholar 

  • Darling JA, Mahon AR (2011) From molecules to management: adopting DNA-based methods for monitoring biological invasions in aquatic environments. Environ Res 111:978–988

    CAS  PubMed  Google Scholar 

  • Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85:407–415

    Google Scholar 

  • Deagle BE, Bax N, Hewitt CL, Patil JG (2003) Development and evaluation of a PCR-based test for detection of Asterias (Echinodermata: Asteroidea) larvae in Australian plankton samples from ballast water. Mar Freshw Res 54:709–719

    CAS  Google Scholar 

  • Deagle BE, Jarman SN, Coissac E, Pompanon F, Taberlet P (2014) DNA metabarcoding and the cytochrome c oxidase subunit I marker: not a perfect match. Biol Lett 10(9):20140562

    PubMed  Google Scholar 

  • Dejean T, Valentini A, Duparc A, Pellier-Cuit S, Pompanon F, Taberlet P, Miaud C (2011) Persistence of environmental DNA in freshwater ecosystems. PLoS One 6:e23398

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dejean T, Valentini A, Miquel C, Taberlet P, Bellemain E, Miaud C (2012) Improved detection of an alien invasive species through environmental DNA barcoding: the example of the American bullfrog Lithobates catesbeianus. J Appl Ecol 49:953–959

    Google Scholar 

  • deWaard JR, Landry J-F, Schmidt C, Derhousoff J, McLean JA, Humble LM (2009) In the dark in a large urban park: DNA barcodes illuminate cryptic and introduced moth species. Biodivers Conserv 18:3825–3839

    Google Scholar 

  • Egan SP, Barnes MA, Hwang C-T, Mahon AR, Feder JL, Ruggiero ST, Tanner CE, Lodge DM (2013) Rapid invasive species detection by combining environmental DNA with light transmission spectroscopy. Conserv Lett 6:402–409

    Google Scholar 

  • Ensing DJ, Moffat CE, Pither J (2013) Taxonomic identification errors generate misleading ecological niche model predictions of an invasive hawkweed. Botany 91:137–147

    Google Scholar 

  • Epp LS, Boessenkool S, Bellemain EP, Haile J, Esposito A, Riaz T, Erséus C, Gusarov VI, Edwards ME, Johnsen A, Stenøien HK, Hassel K, Kauserud H, Yoccoz NG, Bråthen KA, Willerslev E, Taberlet P, Coissac E, Brochmann C (2012) New environmental metabarcodes for analysing soil DNA: potential for studying past and present ecosystems. Mol Ecol 21:1821–1833

    CAS  PubMed  Google Scholar 

  • Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: Why, how and so what? Mol Ecol 19(19):4113–4130

    PubMed  Google Scholar 

  • Evans BS, White RWG, Ward RD (1998) Genetic identification of asteroid larvae from Tasmania, Australia, by PCR-RFLP. Mol Ecol 7:1077–1082

    CAS  Google Scholar 

  • Faber PM (2000) Grass wars. Good intentions gone awry—why would anyone bring an alien cordgrass into S.F. Bay? Calif Coast Ocean 16:14–17

    Google Scholar 

  • Ferri E, Barbuto M, Bain O, Galimberti A, Uni S, Guerrero R, et al (2009) Integrated taxonomy: traditional approach and DNA barcoding for the identification of filarioid worms and related parasites (Nematoda). Front Zool 6:1

  • Ficetola GF, Miaud C, Pompanon F, Taberlet P (2008) Species detection using environmental DNA from water samples. Biol Lett 4:423–425

    PubMed Central  PubMed  Google Scholar 

  • Ficetola GF, Pansu J, Bonin A, Coissac E, Giguet-Covex C, De Barba M et al (2014) Replication levels, false presences, and the estimation of presence/absence from eDNA metabarcoding data. Mol Ecol Resour. doi:10.1111/1755-0998.12338

    PubMed  Google Scholar 

  • Fisher C, Skibinski DOF (1990) Sex-biased mitochondrial DNA heteroplasmy in the marine mussel Mytilus. Proc R Soc Lond B Biol Sci 242(1305):149–156

    Google Scholar 

  • Floyd R, Abebe E, Papert A, Blaxter M (2002) Molecular barcodes for soil nematode identification. Mol Ecol 11:839–850

    CAS  PubMed  Google Scholar 

  • Floyd R, Lima J, deWaard J, Humble L, Hanner R (2010) Common goals: policy implications of DNA barcoding as a protocol for identification of arthropod pests. Biol Invasions 12:2947–2954

    Google Scholar 

  • Folmer O, Black MB, Hoeh WR, Lutz RA, Vrijenhoek RC (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Frischer ME, Wyllie JA, Hansen AS, Nierzwicki-Bauer SA (1997) Development and utilization of genetic probes for studying zebra mussel veligers. In: Paper presented at the proceedings of the 1997 Georgia water resources conference, Athens, Georgia

  • Galimberti A, Spada M, Russo D, Mucedda M, Agnelli P, Crottini A, Ferri E, Martinoli A, Casiraghi M (2012) Integrated operational taxonomic units (IOTUs) in echolocating bats: a bridge between molecular and traditional taxonomy. PLoS ONE 7:e40122

    PubMed Central  CAS  PubMed  Google Scholar 

  • Galimberti A, de Mattia F, Losa A, Bruni I, Federici S, Casiraghi M, Martellos S, Labra M (2013) DNA barcoding as a new tool for food traceability. Food Res Int 50:55–63

    CAS  Google Scholar 

  • Galtier N, Nabholz B, Glémin S, Hurst GDD (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18:4541–4550

    CAS  PubMed  Google Scholar 

  • Geller J, Meyer C, Parker M, Hawk H (2013) Redesign of PCR primers for mitochondrial cytochrome c oxidase subunit I for marine invertebrates and application in all-taxa biotic surveys. Mol Ecol Resour 13:851–861

    CAS  PubMed  Google Scholar 

  • Genovesi P, Shine C (2011) European strategy on invasive alien species. Council of Europe, Strasbourg

    Google Scholar 

  • Geoffroy A, Le Gall L, Destombe C (2012) Cryptic introduction of the red alga Polysiphonia morrowii Harvey (Rhodomelaceae, Rhodophyta) in the North Atlantic ocean highlighted by a DNA barcoding approach. Aquat Bot 100:67–71

    CAS  Google Scholar 

  • Ghahramanzadeh R, Esselink G, Kodde LP, Duistermaat H, van Valkenburg JLCH, Marashi SH, Smulders MJM, van de Wiel CCM (2013) Efficient distinction of invasive aquatic plant species from non-invasive related species using DNA barcoding. Mol Ecol Resour 13:21–31

    CAS  PubMed  Google Scholar 

  • Glenn TC (2011) Field guide to next-generation DNA sequencers. Mol Ecol Resour 11:759–769

    CAS  PubMed  Google Scholar 

  • Gollasch S, MacDonald E, Belson S, Botnen H, Christensen JT, Hamer JP, Houvenaghel G, Jelmert A, Lucas I, Masson D, McCollin T, Olenin S, Persson A, Wallentinus I, Wetsteyn LPMJ, Wittling T (2002) Life in ballast tanks. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe distribution, impacts and management. Kluwer Academic Publishers, Dordrecht, pp 217–231

    Google Scholar 

  • Hajibabaei M, Smith MA, Janzen DH, Rodriguez JJ, Whitfield JB, Hebert PDN (2006) A minimalist barcode can identify a specimen whose DNA is degraded. Mol Ecol Notes 6:959–964

    CAS  Google Scholar 

  • Hajibabaei M, Shokralla S, Zhou H, Singer GAC, Baird DJ (2011) Environmental barcoding: a next-generation sequencing approach for biomonitoring applications using river benthos. PLoS One 6:e17497

    PubMed Central  CAS  PubMed  Google Scholar 

  • Harvey JBJ, Hoy MS, Rodriguez RJ (2009) Molecular detection of native and invasive marine invertebrate larvae present in ballast and open water environmental samples collected in Puget Sound. J Exp Mar Biol Ecol 369:93–99

    CAS  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003a) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321

    CAS  Google Scholar 

  • Hebert PDN, Ratnasingham S, deWaard JR (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond B Suppl 270:96–99

    Google Scholar 

  • Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004a) Identification of birds through DNA barcodes. PLoS Biol 2:1657–1663

    CAS  Google Scholar 

  • Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004b) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812–14817

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hoareau TB, Boissin E (2010) Design of phylum-specific hybrid primers for DNA barcoding: addressing the need for efficient COI amplification in the Echinodermata. Mol Ecol Resour 10:960–967

    CAS  PubMed  Google Scholar 

  • Hollingsworth PM, Forrest LL, Spouge JL et al (2009) A DNA barcode for land plants. Proc Natl Acad Sci USA 106:12794–12797

    PubMed Central  CAS  Google Scholar 

  • Hollingsworth PM, Graham SW, Little DP (2011) Choosing and using a plant DNA barcode. PLoS One 6:e19254

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hoos PM, Miller AW, Ruiz GM, Vrijenhoek RC, Geller JB (2010) Genetic and historical evidence disagree on likely sources of the Atlantic amethyst gem clam Gemma gemma (Totten, 1834) in California. Divers Distrib 16:582–592

    Google Scholar 

  • Huang D, Meier R, Todd PA, Chou LM (2008) Slow mitochondrial COI sequence evolution at the base of the metazoan tree and its implications for DNA barcoding. J Mol Evol 66:167–174

    CAS  PubMed  Google Scholar 

  • IMO (2004) International Convention for the Control and Management of Ships’ Ballast water and sediments.http://www.imo.org/About/Conventions/ListOfConventions/Pages/International-Convention-for-the-Control-and-Management-of-Ships%27-Ballast-Water-and-Sediments-%28BWM%29.aspx

  • Jerde CL, Mahon AR, Chadderton WL, Lodge DM (2011) “Sight-unseen” detection of rare aquatic species using environmental DNA. Conserv Lett 4:150–157

    Google Scholar 

  • Ji Y, Ashton L, Pedley SM, Edwards DP, Tang Y, Nakamura A, Kitching R, Dolman PM, Woodcock P, Edwards FA, Larsen TH, Hsu WW, Benedick S, Hamer KC, Wilcove DS, Bruce C, Wang X, Levi T, Lott M, Emerson BC, Yu DW (2013) Reliable, verifiable and efficient monitoring of biodiversity via metabarcoding. Ecol Lett 16:1245–1257

    PubMed  Google Scholar 

  • Johnson SB, Geller JB (2006) Larval settlement can explain the adult distribution of Mytilus californianus Conrad but not of M. galloprovincialis Lamarck or M. trossulus Gould in Moss Landing, central California: evidence from genetic identification of spat. J Exp Mar Biol Ecol 328:136–145

    Google Scholar 

  • Kaplan L, Kendell D, Robertson D, Livdahl T, Khatchikian C (2010) Aedes aegypti and Aedes albopictus in Bermuda: extinction, invasion, invasion and extinction. Biol Invasions 12:3277–3288

    Google Scholar 

  • Ko HL, Wang YT, Chiu TS, Lee MA, Leu MY, Chang KZ et al (2013) Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS One 8(1):e53451

    PubMed Central  CAS  PubMed  Google Scholar 

  • Le Roux J, Wieczorek AM (2009) Molecular systematics and population genetics of biological invasions: towards a better understanding of invasive species management. Ann Appl Biol 154:1–17

    Google Scholar 

  • Lees DC, Lack HW, Rougerie R, Hernandez-Lopez A, Raus T, Avtzis ND, Augustin S, Lopez-Vaamonde C (2011) Tracking origins of invasive herbivores through herbaria and archival DNA: the case of the horse-chestnut leaf miner. Front Ecol Environ 9:322–328

    Google Scholar 

  • Leray M, Yang JY, Meyer CP, Mills SC, Agudelo N, Ranwez V, Boehm JT, Machida RJ (2013) A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Front Zool 10:34

    PubMed Central  PubMed  Google Scholar 

  • Levy L, Shiel P, Dennis G, Lévesque C A, Clover G, Bennypaul H, et al (2014) Molecular diagnostic techniques and biotechnology in plant biosecurity. In: Gordh G, McKirdy S (eds) The handbook of plant biosecurity. Springer, Netherlands, pp 375–416

  • Lindeque PK, Parry HE, Harmer RA, Somerfield PJ, Atkinson A (2013) Next generation sequencing reveals the hidden diversity of zooplankton assemblages. PLoS One 8:e81327

    PubMed Central  CAS  PubMed  Google Scholar 

  • Loman NJ, Misra RV, Dallman TJ, Constantinidou C, Gharbia SE, Wain J, Pallen MJ (2012) Performance comparison of benchtop high-throughput sequencing platforms. Nat Biotechnol 30:434–439

    CAS  PubMed  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species: a selection from the global invasive species database. Invasive Species Specialist Group, Species Survival Commission, World Conservation Union (IUCN), Auckland, New Zealand, p 12

    Google Scholar 

  • Lützen J, Faasse M, Gittenberger A, Glenner H, Hoffmann E (2012) The Japanese oyster drill Ocinebrellus inornatus (Récluz, 1851) (Mollusca, Gastropoda, Muricidae), introduced to the Limfjord, Denmark. Aquat Invasions 7:181–191

    Google Scholar 

  • Mackie JA, Darling JA, Geller JB (2012) Ecology of cryptic invasions: latitudinal segregation among Watersipora (Bryozoa) species. Sci Rep 2:871. doi:10.1038/srep00871

    PubMed Central  PubMed  Google Scholar 

  • Mahon AR, Barnes MA, Li F, Egan SP, Tanner CE, Ruggiero ST, Feder JL, Lodge DM (2013) DNA-based species detection capabilities using laser transmission spectroscopy. J R Soc Interface 10:20120637

    PubMed Central  Google Scholar 

  • Manghisi A, Morabito M, Bertuccio C, Le Gall L, Couloux A, Cruaud C, Genovese G (2010) Is routine DNA barcoding an efficient tool to reveal introductions of alien macroalgae? A case study of Agardhiella subulata (Solieriaceae, Rhodophyta) in Cape Peloro lagoon (Sicily, Italy). Cryptogam Algol 31:423–433

    Google Scholar 

  • McGlashan D, Ponniah M, Cassey P, Viard F (2008) Clarifying marine invasions with molecular markers: an illustration based on mtDNA from mistaken calyptraeid gastropod identifications. Biol Invasions 10:51–57

    Google Scholar 

  • McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10(4):e1003531

    PubMed Central  PubMed  Google Scholar 

  • Meier R, Shiyang K, Vaidya G, Ng PKL (2006) DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Syst Biol 55:715–728

    PubMed  Google Scholar 

  • Metzker ML (2010) Sequencing technologies—the next generation. Nat Rev Genet 11:31–46

    CAS  PubMed  Google Scholar 

  • Meyer CP, Paulay G (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biol 3:e422

    PubMed Central  PubMed  Google Scholar 

  • Migheli Q, Balmas V, Komoñ-Zelazowska M, Scherm B, Fiori S, Kopchinskiy AG, Kubicek CP, Druzhinina IS (2009) Soils of a Mediterranean hot spot of biodiversity and endemism (Sardinia, Tyrrhenian Islands) are inhabited by pan-European, invasive species of Hypocrea/Trichoderma. Environ Microbiol 11:35–46

    CAS  PubMed  Google Scholar 

  • Mitchell A, Maddox C (2010) Bark beetles (Coleoptera: Curculionidae: Scolytinae) of importance to the Australian macadamia industry: an integrative taxonomic approach to species diagnostics. Aust J Entomol 49:104–113

    Google Scholar 

  • Moss JA, Burreson EM, Cordes JF, Dungan CF, Brown GD, Wang A, Wu X, Reece KS (2007) Pathogens in Crassostrea ariakensis and other Asian oyster species: implications for non-native oyster introduction to Chesapeake Bay. Dis Aquat Org 77:207–223

    CAS  PubMed  Google Scholar 

  • Mountfort D and Hayden B (2006) Techniques for detection and enumeration of marine biosecurity risk species and compliance testing. In: Proceedings of a workshop on molecular technologies for the detection of marine pests, Wellington, New Zealand

  • Naylor RL, Williams SL, Strong DR (2001) Aquaculture-a gateway for exotic species. Science 294:1655–1656

    CAS  PubMed  Google Scholar 

  • Neigel J, Stake ADJ (2007) DNA barcoding as a tool for coral reef conservation. Coral Reefs 26:487–499

    Google Scholar 

  • Parameswaran P, Jalili R, Tao L, Shokralla S, Gharizadeh B, Ronaghi M, Fire AZ (2007) A pyrosequencing-tailored nucleotide barcode design unveils opportunities for large-scale sample multiplexing. Nucleic Acids Res 35:e130

    PubMed Central  PubMed  Google Scholar 

  • Pieterse W, Muller DL, Jansen van Vuuren B (2010) A molecular identification approach for five species of mealybug (Hemiptera: Pseudococcidae) on citrus fruit exported from South Africa. Afr Entomol 18:23–28

    Google Scholar 

  • Pochon X, Bott NJ, Smith KF, Wood SA (2013) Evaluating detection limits of next-generation sequencing for the surveillance and monitoring of international marine pests. PLoS One 8:e73935

    PubMed Central  CAS  PubMed  Google Scholar 

  • Porazinska DL, Giblin-Davis RM, Faller L, Farmerie W, Kanzaki N, Morris K, Powers TO, Tucker AE, Sung W, Thomas WK (2009) Evaluating high-throughput sequencing as a method for metagenomic analysis of nematode diversity. Mol Ecol Resour 9:1439–1450

    CAS  PubMed  Google Scholar 

  • Porazinska DL, Sung W, Giblin-Davis RM, Thomas WK (2010) Reproducibility of read numbers in high-throughput sequencing analysis of nematode community composition and structure. Mol Ecol Resour 10:666–676

    CAS  PubMed  Google Scholar 

  • Porco D, Decaëns T, Deharveng L, James SW, Skarżyński D, Erséus C, Butt KR, Richard B, Hebert PDN (2013) Biological invasions in soil: DNA barcoding as a monitoring tool in a multiple taxa survey targeting European earthworms and springtails in North America. Biol Invasions 15:899–910

    Google Scholar 

  • Pringle A, Adams RI, Cross HB, Bruns TD (2009) The ectomycorrhizal fungus Amanita phalloides was introduced and is expanding its range on the west coast of North America. Mol Ecol 18:817–833

    CAS  PubMed  Google Scholar 

  • Pyšek P, Hulme PE, Meyerson LA, Smith GF, Boatwright JS, Crouch NR, Figueiredo E, Foxcroft LC, Jarošík V, Richardson DM, Suda J, Wilson JRU (2013) Hitting the right target: taxonomic challenges for, and of, plant invasions. AoB Plants. doi:10.1093/aobpla/plt1042

    Google Scholar 

  • Radulovici AE, Sainte-Marie B, Dufresne F (2009) DNA barcoding of marine crustaceans from the Estuary and Gulf of St Lawrence: a regional-scale approach. Mol Ecol Resour 9(Suppl. 1):181–187

    CAS  PubMed  Google Scholar 

  • Radulovici AE, Archambault P, Dufresne F (2010) DNA barcodes for marine biodiversity: moving fast forward? Diversity 2:450–472

    CAS  Google Scholar 

  • Ratnasingham S, Hebert PDN (2007) BOLD: The barcode of life data system (www.barcodinglife.org). Mol Ecol Notes 7:355–364

    PubMed Central  CAS  PubMed  Google Scholar 

  • Roy S, Tyagi A, Shukla V, Kumar A, Singh UM, Chaudhary LB, Datt B, Tuli R (2010) Universal plant DNA barcode loci may not work in complex groups: a case study with Indian Berberis species. PLoS One 5(10):e13674

    PubMed Central  PubMed  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Google Scholar 

  • Saunders GW (2009) Routine DNA barcoding of Canadian Gracilariales (Rhodophyta) reveals the invasive species Gracilaria vermiculophylla in British Columbia. Mol Ecol Resour 9(Suppl 1):140–150

    CAS  PubMed  Google Scholar 

  • Savolainen V, Cowan RS, Vogler AP, Roderick GK, Lane R (2005) Towards writing the encyclopaedia of life: an introduction to DNA barcoding. Philos Trans R Soc Lond B 360:1805–1811

    CAS  Google Scholar 

  • Scheffer SJ, Lewis ML, Joshi RC (2006) DNA barcoding applied to invasive leafminers (Diptera: Agromyzidae) in the Philippines. Ann Entomol Soc Am 99:204–210

    CAS  Google Scholar 

  • Schlick-Steiner BC, Steiner FM, Seifert B, Stauffer C, Christian EC, Crozier RH (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annu Rev Entomol 55:421–438

    CAS  PubMed  Google Scholar 

  • Shearer TL, Coffroth MA (2008) Barcoding corals: limited by interspecific divergence, not intraspecific variation. Mol Ecol Resour 8:247–255

    CAS  PubMed  Google Scholar 

  • Shendure J, Ji H (2008) Next-generation DNA sequencing. Nat Biotechnol 26(10):1135–1145

    CAS  PubMed  Google Scholar 

  • Shokralla S, Spall JL, Gibson JF, Hajibabaei M (2012) Next-generation sequencing technologies for environmental DNA research. Mol Ecol 21:1794–1805

    CAS  PubMed  Google Scholar 

  • Shokralla S, Gibson JF, Nikbakht H, Janzen DH, Hallwachs W, Hajibabaei M (2014) Next-generation DNA barcoding: using next-generation sequencing to enhance and accelerate DNA barcode capture from single specimens. Mol Ecol Resour 14:892–901

    PubMed Central  CAS  PubMed  Google Scholar 

  • Simberloff D (2014) Biological invasions: What’s worth fighting and what can be won? Ecol Eng 65:112–121

    Google Scholar 

  • Simberloff D, Parker IM, Windle PN (2005) Introduced species policy, management, and future research needs. Front Ecol Environ 3:12–20

    Google Scholar 

  • Simberloff D, Martin J-L, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vilà M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66

    PubMed  Google Scholar 

  • Smale DA, Childs S (2012) The occurrence of a widespread marine invader, Didemnum perlucidum (Tunicata, Ascidiacea) in Western Australia. Biol Invasions 14:1325–1330

    Google Scholar 

  • Smith RD, Aradottir GI, Taylor A, Lyal C (2008) Invasive species management—what taxonomic support is needed?. Global Invasive Species Programme, Nairobi

    Google Scholar 

  • Sweeney BW, Battle JM, Jackson JK, Dapkey T (2011) Can DNA barcodes of stream macroinvertebrates improve descriptions of community structure and water quality? J N Am Benthol Soc 30:195–216

    Google Scholar 

  • Swetnam TW, Allen CD, Betancourt JL (1999) Applied historical ecology: using the past to manage for the future. Ecol Appl 9:1189–1206

    Google Scholar 

  • Taberlet P, Coissac E, Pompanon F, Brochmann C, Willerslev E (2012) Towards next-generation biodiversity assessment using DNA metabarcoding. Mol Ecol 21:2045–2050

    CAS  PubMed  Google Scholar 

  • Thomas M, Raharivololoniaina L, Glaw F, Vences M, Vieites DR (2005) Montane tadpoles in Madagascar: molecular identification and description of the larval stages of Mantidactylus elegans, Mantidactylus madecassus, and Boophis laurenti from the Andringitra Massif. Copeia 5:174–183

    Google Scholar 

  • Thomsen PF, Kielgast J, Iversen LL, Wiuf C, Rasmussen M, Gilbert MTP, Orlando L, Willerslev E (2012) Monitoring endangered freshwater biodiversity using environmental DNA. Mol Ecol 21:2565–2573

    CAS  PubMed  Google Scholar 

  • Valentini A, Pompanon F, Taberlet P (2009) DNA barcoding for ecologists. Trends Ecol Evol 24:110–117

    PubMed  Google Scholar 

  • Vences M, Thomas M, van der Meijden A, Chiari Y, Vieites DR (2005) Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Front Zool 2:5

    PubMed Central  PubMed  Google Scholar 

  • Wiemers M, Fiedler K (2007) Does the DNA barcoding gap exist?—a case study in blue butterflies (Lepidoptera: Lycaenidae). Front Zool 4:8

    PubMed Central  PubMed  Google Scholar 

  • Yoccoz NG (2012) The future of environmental DNA in ecology. Mol Ecol 21:2031–2038

    PubMed  Google Scholar 

  • Yoccoz NG, Bråthen KA, Gielly L, Haile J, Edwards ME, Goslar T, Von Stedingk H, Brysting AK, Coissac E, Pompanon F, Sønstebø JH, Miquel C, Valentini A, De Bello F, Chave J, Thuiller W, Wincker P, Cruaud C, Gavory F, Rasmussen M, Gilbert MTP, Orlando L, Brochmann C, Willerslev E, Taberlet P (2012) DNA from soil mirrors plant taxonomic and growth form diversity. Mol Ecol 21:3647–3655

    CAS  PubMed  Google Scholar 

  • Yu DW, Ji Y, Emerson BC, Wang X, Ye C, Yang C, Ding Z (2012) Biodiversity soup: metabarcoding of arthropods for rapid biodiversity assessment and biomonitoring. Methods Ecol Evol 3:613–623

    Google Scholar 

  • Zhan A, Hulák M, Sylvester F, Huang X, Adebayo AA, Abbott CL, Adamowicz SJ et al (2013) High sensitivity of 454 pyrosequencing for detection of rare species in aquatic communities. Methods Ecol Evol 4:558–565

    Google Scholar 

  • Zhan A, Bailey SA, Heath DD, MacIsaac HJ (2014a) Performance comparison of genetic markers for high-throughput sequencing-based biodiversity assessment in complex communities. Mol Ecol Resour 14:1049–1059

    CAS  PubMed  Google Scholar 

  • Zhan A, Xiong W, He S, MacIsaac HJ (2014b) Influence of artifact removal on rare species recovery in natural complex communities using high-throughput sequencing. PLoS One 9:e96928

    PubMed Central  PubMed  Google Scholar 

  • Zhou X, Li Y, Liu S, Yang Q, Su X, Zhou L, Tang M, Fu R, Li J, Huang Q (2013) Ultra-deep sequencing enables high-fidelity recovery of biodiversity for bulk arthropod samples without PCR amplification. GigaScience 2:4

    PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Stefano Piraino, John Darling, Esther Lubzens and Gary Carvalho for inviting us to contribute to this special issue. The publication of this paper is supported by CoNISMa (Italian National Interuniversity Consortium for Marine Sciences), which received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013) for the project VECTORS (http://www.marine-vectors.eu). This paper stems from the International workshop MOLTOOLS (Molecular Tools for Monitoring Marine Invasive Species), held in Lecce, Italy, in September 2012. We thank the two anonymous reviewers for their comments and suggestions that improved the manuscript. This review benefited from insights and outcomes from various projects we would like to acknowledge: the Interreg IVa Marinexus; the AXA Research Fund (AXA Marine Aliens and Climate Change Project); the Bibliothèque du Vivant sequencing programme; Programmi di ricerca scientifica di rilevante interesse nazionale 2007 (PRIN 2007): “Nuova metodica per l’analisi della biodiversità: un’applicazione del pirosequenziamento allo studio degli organismi del suolo”; the following grants funded by Fondazione Cariplo: “Dai geni all’ecosistema: il DNA barcoding come supporto innovativo per la protezione della biodiversità e l’analisi della funzionalità delle reti ecologiche”; “Le connessioni ecologiche nelle selve castanili nel Parco Regionale Campo dei Fiori: valutazione e sviluppo di sistemi di gestione”; “Il corridoio ecologico del Lambro: interventi per il consolidamento e l’implementazione della connettività e della biodiversità”; “Seminare biodiversità: il ruolo dell’avifauna migratrice nell’implementazione della biodiversità del Parco Monte Barro”.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maurizio Casiraghi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Comtet, T., Sandionigi, A., Viard, F. et al. DNA (meta)barcoding of biological invasions: a powerful tool to elucidate invasion processes and help managing aliens. Biol Invasions 17, 905–922 (2015). https://doi.org/10.1007/s10530-015-0854-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-015-0854-y

Keywords

Navigation