Biological Invasions

, Volume 17, Issue 3, pp 905–922 | Cite as

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

  • Thierry Comtet
  • Anna Sandionigi
  • Frédérique Viard
  • Maurizio Casiraghi
Molecular Tools

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.

Keywords

DNA barcoding DNA metabarcoding Alien species Early warning Environmental DNA Next generation sequencing High throughput sequencing 

Notes

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”.

References

  1. 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–e237Google Scholar
  2. Andersen K, Bird KL, Rasmussen M, Haile J et al (2012) Metabarcoding of ‘dirt’DNA from soil reflects vertebrate biodiversity. Mol Ecol 21(8):1966–1979PubMedGoogle Scholar
  3. Armstrong K (2010) DNA barcoding: a new module in New Zealand’s plant biosecurity diagnostic toolbox. EPPO Bull 40:91–100Google Scholar
  4. Armstrong KF, Ball SL (2005) DNA barcodes for biosecurity: invasive species identification. Philos Trans R Soc Lond B 360:1813–1823Google Scholar
  5. 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 56:16–20Google Scholar
  6. Ascunce MS, Nigg HN, Clark A (2009) Molecular identification of the economically important invasive citrus root weevil Diaprepes abbreviatus (Coleoptera: Curculionidae). Florida Entomol 92:167–171Google Scholar
  7. Ball SL, Armstrong KF (2006) DNA barcodes for insect pest identification: a test case with tussock moths (Lepidoptera: Lymantriidae). Can J For Res 36:337–350Google Scholar
  8. Bhadury P, Austen MC (2010) Barcoding marine nematodes: an improved set of nematode 18S rRNA primers to overcome eukaryotic co-interference. Hydrobiologia 641:245–251Google Scholar
  9. Bik HM, Porazinska DL, Creer S, Caporaso JG, Knight R, Thomas WK (2012) Sequencing our way towards understanding global eukaryotic biodiversity. Trends Ecol Evol 27:233–243PubMedCentralPubMedGoogle Scholar
  10. 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 15:253–260Google Scholar
  11. 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 360:1935–1943Google Scholar
  12. 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 29:358–367Google Scholar
  13. 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 40:30–33Google Scholar
  14. Bortolus A (2008) Error cascades in the biological sciences: the unwanted consequences of using bad taxonomy in ecology. Ambio 37:114–118PubMedGoogle Scholar
  15. 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 28:706–714Google Scholar
  16. 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 23:465–474PubMedGoogle Scholar
  17. 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 55:2414–2424Google Scholar
  18. 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 56:1929–1939Google Scholar
  19. Briski E, Cristescu ME, Bailey SA, MacIsaac HJ (2011b) Use of DNA barcoding to detect invertebrate invasive species from diapausing eggs. Biol Invasions 13:1325–1340Google Scholar
  20. Bucklin A, Steinke D, Blanco-Bercial L (2011) DNA barcoding of marine metazoa. Annu Rev Mar Sci 3:471–508Google Scholar
  21. Buhay JE (2009) “COI-like” sequences are becoming problematic in molecular systematic and DNA barcoding studies. J Crust Biol 29:96–110Google Scholar
  22. 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 5:31–39Google Scholar
  23. Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr Mar Biol Annu Rev 23:313–371Google Scholar
  24. 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 13–56Google Scholar
  25. Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82Google Scholar
  26. Carstens BC, Pelletier TA, Reid NM, Satler JD (2013) How to fail at species delimitation. Mol Ecol 22:4369–4383PubMedGoogle Scholar
  27. 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 11:440–453PubMedGoogle Scholar
  28. 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 405:234–242PubMedGoogle Scholar
  29. Chauvel B, Dessaint F, Cardinal-Legrand C, Bretagnolle F (2006) The historical spread of Ambrosia artemisiifolia L. in France from herbarium records. J Biogeogr 33:665–673Google Scholar
  30. 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 31:651–655Google Scholar
  31. Civille JC, Sayce K, Smith SD, Strong DR (2005) Reconstructing a century of Spartina alterniflora invasion with historical records and contemporary remote sensing. Ecoscience 12:330–338Google Scholar
  32. 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 PubMedGoogle Scholar
  33. Coissac E, Riaz T, Puillandre N (2012) Bioinformatic challenges for DNA metabarcoding of plants and animals. Mol Ecol 21:1834–1847PubMedGoogle Scholar
  34. Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10(2):135–141Google Scholar
  35. 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:e28381PubMedCentralPubMedGoogle Scholar
  36. Collins RA, Armstrong KF, Holyoake AJ, Keeling S (2013) Something in the water: biosecurity monitoring of ornamental fish imports using environmental DNA. Biol Invasions 15:1209–1215Google Scholar
  37. Cook CN, Mascia MB, Schwartz MW, Possingham HP, Fuller RA (2013) Achieving conservation science that bridges the knowledge–action boundary. Conserv Biol 27:669–678Google Scholar
  38. Cristescu ME (2014) From barcoding single individuals to metabarcoding biological communities: towards an integrative approach to the study of global biodiversity. Trends Ecol Evol 29:566–571PubMedGoogle Scholar
  39. Darling J, Blum M (2007) DNA-based methods for monitoring invasive species: a review and prospectus. Biol Invasions 9:751–765Google Scholar
  40. Darling JA, Mahon AR (2011) From molecules to management: adopting DNA-based methods for monitoring biological invasions in aquatic environments. Environ Res 111:978–988PubMedGoogle Scholar
  41. Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85:407–415Google Scholar
  42. 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 54:709–719Google Scholar
  43. 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):20140562PubMedGoogle Scholar
  44. 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:e23398PubMedCentralPubMedGoogle Scholar
  45. 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 49:953–959Google Scholar
  46. 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 18:3825–3839Google Scholar
  47. 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 6:402–409Google Scholar
  48. Ensing DJ, Moffat CE, Pither J (2013) Taxonomic identification errors generate misleading ecological niche model predictions of an invasive hawkweed. Botany 91:137–147Google Scholar
  49. 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 21:1821–1833PubMedGoogle Scholar
  50. Estoup A, Guillemaud T (2010) Reconstructing routes of invasion using genetic data: Why, how and so what? Mol Ecol 19(19):4113–4130PubMedGoogle Scholar
  51. Evans BS, White RWG, Ward RD (1998) Genetic identification of asteroid larvae from Tasmania, Australia, by PCR-RFLP. Mol Ecol 7:1077–1082Google Scholar
  52. Faber PM (2000) Grass wars. Good intentions gone awry—why would anyone bring an alien cordgrass into S.F. Bay? Calif Coast Ocean 16:14–17Google Scholar
  53. 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 6:1Google Scholar
  54. Ficetola GF, Miaud C, Pompanon F, Taberlet P (2008) Species detection using environmental DNA from water samples. Biol Lett 4:423–425PubMedCentralPubMedGoogle Scholar
  55. 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 PubMedGoogle Scholar
  56. Fisher C, Skibinski DOF (1990) Sex-biased mitochondrial DNA heteroplasmy in the marine mussel Mytilus. Proc R Soc Lond B Biol Sci 242(1305):149–156Google Scholar
  57. Floyd R, Abebe E, Papert A, Blaxter M (2002) Molecular barcodes for soil nematode identification. Mol Ecol 11:839–850PubMedGoogle Scholar
  58. 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 12:2947–2954Google Scholar
  59. 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 3:294–299PubMedGoogle Scholar
  60. 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, GeorgiaGoogle Scholar
  61. 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:e40122PubMedCentralPubMedGoogle Scholar
  62. 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 50:55–63Google Scholar
  63. Galtier N, Nabholz B, Glémin S, Hurst GDD (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18:4541–4550PubMedGoogle Scholar
  64. 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 13:851–861PubMedGoogle Scholar
  65. Genovesi P, Shine C (2011) European strategy on invasive alien species. Council of Europe, StrasbourgGoogle Scholar
  66. 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 100:67–71Google Scholar
  67. 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 13:21–31PubMedGoogle Scholar
  68. Glenn TC (2011) Field guide to next-generation DNA sequencers. Mol Ecol Resour 11:759–769PubMedGoogle Scholar
  69. 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 217–231Google Scholar
  70. 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 6:959–964Google Scholar
  71. 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:e17497PubMedCentralPubMedGoogle Scholar
  72. 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 369:93–99Google Scholar
  73. Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003a) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321Google Scholar
  74. 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 270:96–99Google Scholar
  75. Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004a) Identification of birds through DNA barcodes. PLoS Biol 2:1657–1663Google Scholar
  76. 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 101:14812–14817PubMedCentralPubMedGoogle Scholar
  77. 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 10:960–967PubMedGoogle Scholar
  78. Hollingsworth PM, Forrest LL, Spouge JL et al (2009) A DNA barcode for land plants. Proc Natl Acad Sci USA 106:12794–12797PubMedCentralGoogle Scholar
  79. Hollingsworth PM, Graham SW, Little DP (2011) Choosing and using a plant DNA barcode. PLoS One 6:e19254PubMedCentralPubMedGoogle Scholar
  80. 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 16:582–592Google Scholar
  81. 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 66:167–174PubMedGoogle Scholar
  82. Jerde CL, Mahon AR, Chadderton WL, Lodge DM (2011) “Sight-unseen” detection of rare aquatic species using environmental DNA. Conserv Lett 4:150–157Google Scholar
  83. 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 16:1245–1257PubMedGoogle Scholar
  84. 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 328:136–145Google Scholar
  85. 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 12:3277–3288Google Scholar
  86. 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):e53451PubMedCentralPubMedGoogle Scholar
  87. 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 154:1–17Google Scholar
  88. 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 9:322–328Google Scholar
  89. 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 10:34PubMedCentralPubMedGoogle Scholar
  90. 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 375–416Google Scholar
  91. Lindeque PK, Parry HE, Harmer RA, Somerfield PJ, Atkinson A (2013) Next generation sequencing reveals the hidden diversity of zooplankton assemblages. PLoS One 8:e81327PubMedCentralPubMedGoogle Scholar
  92. 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 30:434–439PubMedGoogle Scholar
  93. 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 12Google Scholar
  94. 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 7:181–191Google Scholar
  95. 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 PubMedCentralPubMedGoogle Scholar
  96. 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 10:20120637PubMedCentralGoogle Scholar
  97. 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 31:423–433Google Scholar
  98. 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 10:51–57Google Scholar
  99. McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10(4):e1003531PubMedCentralPubMedGoogle Scholar
  100. 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 55:715–728PubMedGoogle Scholar
  101. Metzker ML (2010) Sequencing technologies—the next generation. Nat Rev Genet 11:31–46PubMedGoogle Scholar
  102. Meyer CP, Paulay G (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biol 3:e422PubMedCentralPubMedGoogle Scholar
  103. 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 11:35–46PubMedGoogle Scholar
  104. 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 49:104–113Google Scholar
  105. 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 77:207–223PubMedGoogle Scholar
  106. 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 ZealandGoogle Scholar
  107. Naylor RL, Williams SL, Strong DR (2001) Aquaculture-a gateway for exotic species. Science 294:1655–1656PubMedGoogle Scholar
  108. Neigel J, Stake ADJ (2007) DNA barcoding as a tool for coral reef conservation. Coral Reefs 26:487–499Google Scholar
  109. 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:e130PubMedCentralPubMedGoogle Scholar
  110. 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 18:23–28Google Scholar
  111. 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:e73935PubMedCentralPubMedGoogle Scholar
  112. 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 9:1439–1450PubMedGoogle Scholar
  113. 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 10:666–676PubMedGoogle Scholar
  114. 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 15:899–910Google Scholar
  115. 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 18:817–833PubMedGoogle Scholar
  116. 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
  117. 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):181–187PubMedGoogle Scholar
  118. Radulovici AE, Archambault P, Dufresne F (2010) DNA barcodes for marine biodiversity: moving fast forward? Diversity 2:450–472Google Scholar
  119. Ratnasingham S, Hebert PDN (2007) BOLD: The barcode of life data system (www.barcodinglife.org). Mol Ecol Notes 7:355–364PubMedCentralPubMedGoogle Scholar
  120. 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):e13674PubMedCentralPubMedGoogle Scholar
  121. 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 32:305–332Google Scholar
  122. 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):140–150PubMedGoogle Scholar
  123. 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 360:1805–1811Google Scholar
  124. Scheffer SJ, Lewis ML, Joshi RC (2006) DNA barcoding applied to invasive leafminers (Diptera: Agromyzidae) in the Philippines. Ann Entomol Soc Am 99:204–210Google Scholar
  125. 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 55:421–438PubMedGoogle Scholar
  126. Shearer TL, Coffroth MA (2008) Barcoding corals: limited by interspecific divergence, not intraspecific variation. Mol Ecol Resour 8:247–255PubMedGoogle Scholar
  127. Shendure J, Ji H (2008) Next-generation DNA sequencing. Nat Biotechnol 26(10):1135–1145PubMedGoogle Scholar
  128. Shokralla S, Spall JL, Gibson JF, Hajibabaei M (2012) Next-generation sequencing technologies for environmental DNA research. Mol Ecol 21:1794–1805PubMedGoogle Scholar
  129. 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 14:892–901PubMedCentralPubMedGoogle Scholar
  130. Simberloff D (2014) Biological invasions: What’s worth fighting and what can be won? Ecol Eng 65:112–121Google Scholar
  131. Simberloff D, Parker IM, Windle PN (2005) Introduced species policy, management, and future research needs. Front Ecol Environ 3:12–20Google Scholar
  132. 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 28:58–66PubMedGoogle Scholar
  133. Smale DA, Childs S (2012) The occurrence of a widespread marine invader, Didemnum perlucidum (Tunicata, Ascidiacea) in Western Australia. Biol Invasions 14:1325–1330Google Scholar
  134. Smith RD, Aradottir GI, Taylor A, Lyal C (2008) Invasive species management—what taxonomic support is needed?. Global Invasive Species Programme, NairobiGoogle Scholar
  135. 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 30:195–216Google Scholar
  136. Swetnam TW, Allen CD, Betancourt JL (1999) Applied historical ecology: using the past to manage for the future. Ecol Appl 9:1189–1206Google Scholar
  137. Taberlet P, Coissac E, Pompanon F, Brochmann C, Willerslev E (2012) Towards next-generation biodiversity assessment using DNA metabarcoding. Mol Ecol 21:2045–2050PubMedGoogle Scholar
  138. 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 5:174–183Google Scholar
  139. 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 21:2565–2573PubMedGoogle Scholar
  140. Valentini A, Pompanon F, Taberlet P (2009) DNA barcoding for ecologists. Trends Ecol Evol 24:110–117PubMedGoogle Scholar
  141. 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 2:5PubMedCentralPubMedGoogle Scholar
  142. Wiemers M, Fiedler K (2007) Does the DNA barcoding gap exist?—a case study in blue butterflies (Lepidoptera: Lycaenidae). Front Zool 4:8PubMedCentralPubMedGoogle Scholar
  143. Yoccoz NG (2012) The future of environmental DNA in ecology. Mol Ecol 21:2031–2038PubMedGoogle Scholar
  144. 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 21:3647–3655PubMedGoogle Scholar
  145. 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 3:613–623Google Scholar
  146. 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 4:558–565Google Scholar
  147. 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 14:1049–1059PubMedGoogle Scholar
  148. 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:e96928PubMedCentralPubMedGoogle Scholar
  149. 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 2:4PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Thierry Comtet
    • 1
  • Anna Sandionigi
    • 2
  • Frédérique Viard
    • 1
  • Maurizio Casiraghi
    • 2
  1. 1.Sorbonne Universités, CNRS, UMR 7144, Station Biologique de RoscoffUPMC Univ Paris 06Roscoff CedexFrance
  2. 2.ZooPlantLab, Department of Biotechnology and BiosciencesUniversity of Milan-BicoccaMilanItaly

Personalised recommendations