Advertisement

Biological Invasions

, Volume 19, Issue 10, pp 2851–2867 | Cite as

Bilge water as a vector for the spread of marine pests: a morphological, metabarcoding and experimental assessment

  • Lauren M. Fletcher
  • Anastasija Zaiko
  • Javier Atalah
  • Ingrid Richter
  • Celine M. Dufour
  • Xavier Pochon
  • Susana A. Wood
  • Grant A. Hopkins
Original Paper

Abstract

Vessel movements are considered the primary anthropogenic pathway for the secondary spread of marine non-indigenous species. In comparison to the well-studied mechanisms of hull fouling and ballast water, the importance of bilge water for domestic and cross-regional spread of non-indigenous species is largely unknown and has the potential to compromise the overall effectiveness of biosecurity management actions. In this study, the diversity and abundance of biological material contained in bilge water from 30 small vessels (<20 m) was assessed using traditional and molecular identification tools (metabarcoding of the 18S rRNA gene). Laboratory-based studies were also used to investigate the relationship between voyage duration and propagule success. A large taxonomic diversity in organisms was detected, with 118 and 45 distinct taxa identified through molecular and morphological analyses, respectively. Molecular techniques identified five species recognised as non-indigenous to the study region in 23 of the 30 bilge water samples analysed. Larvae and fragments passed through an experimental bilge pump system relatively unharmed. Time spent in the bilge sump was found to affect discharge success, particularly of short-lived and sensitive larvae, but survival for 3 days was observed. Our findings show that bilge water discharges are likely to pose a non-negligible biosecurity threat and that further research to identify high-risk vessel operating profiles and potential mitigation measures are warranted.

Keywords

Anthropogenic spread Dispersal High-throughput sequencing Non-indigenous species Pathway management Translocation 

Notes

Acknowledgements

We are grateful to Rebecca Stafford-Smith (University of Birmingham), Marc Jary and Patrick Cahill (Cawthron Institute), Megan Carter (NIWA) and Bruce Lines (Diving Services New Zealand Ltd.) for their assistance with various aspects of the laboratory and field studies, as well as Oliver Floerl (Cawthron Institute) for helpful review comments on an earlier version of the manuscript. Sincere thanks are also expressed to Paul Jonkers (Nelmac Ltd.) for assistance with boat arrivals, and the numerous boat operators who allowed access to their vessels. This work was funded by the National Institute of Water and Atmospheric Research Ltd (NIWA) under Coasts and Oceans Research Programme 6, Marine Biosecurity (SCI 2014/15).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10530_2017_1489_MOESM1_ESM.pdf (165 kb)
Supplementary material 1 (PDF 164 kb)
10530_2017_1489_MOESM2_ESM.pdf (66 kb)
Supplementary material 2 (PDF 65 kb)
10530_2017_1489_MOESM3_ESM.pdf (65 kb)
Supplementary material 3 (PDF 65 kb)
10530_2017_1489_MOESM4_ESM.pdf (124 kb)
Supplementary material 4 (PDF 124 kb)
10530_2017_1489_MOESM5_ESM.pdf (187 kb)
Supplementary material 5 (PDF 186 kb)
10530_2017_1489_MOESM6_ESM.pdf (205 kb)
Supplementary material 6 (PDF 205 kb)

References

  1. Acosta H, Forrest BM (2009) The spread of marine non-indigenous species via recreational boating: a conceptual model for risk assessment based on fault tree analysis. Ecol Model 220:1586–1598CrossRefGoogle Scholar
  2. Brown SP, Veach A, Rigdon-Huss AR, Grond K (2015) Scraping the bottom of the barrel: are rare high throughput sequences artifacts? Fungal Ecol 13:221–225CrossRefGoogle Scholar
  3. Bullard SG, Sedlack B, Reinhardt JF et al (2007) Fragmentation of colonial ascidians: differences in reattachment capability among species. J Exp Mar Biol Ecol 342:166–168CrossRefGoogle Scholar
  4. Cahill P, Heasman K, Jeffs A et al (2012) Preventing ascidian fouling in aquaculture: screening selected allelochemicals for anti-metamorphic properties in ascidian larvae. Biofouling 28:39–49CrossRefPubMedGoogle Scholar
  5. Caporaso J, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentralGoogle Scholar
  6. Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr Mar Biol Ann Rev 23:313–371Google Scholar
  7. Chariton A, Court L, Hartley D et al (2010) Ecological assessment of estuarine sediments by pyrosequencing eukaryotic ribosomal DNA. Front Ecol Environ 8:233–238CrossRefGoogle Scholar
  8. Clarke KR, Gorley RN (2015) PRIMER v7: user manual/tutorial. PRIMER-E, Plymouth, p 296Google Scholar
  9. Clarke KR, Somerfield PJ, Chapman MG (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assembladges. J Exp Mar Biol Ecol 330:55–80CrossRefGoogle Scholar
  10. Clarke LJ, Soubrier J, Weyrich LS, Cooper A (2014) Environmental metabarcodes for insects: in silico PCR reveals potential for taxonomic bias. Mol Ecol Resour 14:1160–1170CrossRefPubMedGoogle Scholar
  11. Coma R, Ribes M, Gili J-M et al (2000) Seasonality in coastal benthic ecosystems. Trends Ecol Evol 15:448–453CrossRefPubMedGoogle Scholar
  12. Coutts AD, Taylor MD (2004) A preliminary investigation of biosecurity risks associated with biofouling on merchant vessels in New Zealand. N Z J Mar Freshw Res 38:215–229CrossRefGoogle Scholar
  13. Darbyson E, Locke A, Hanson JM et al (2009) Marine boating habits and the potential for spread of invasive species in the Gulf of St. Lawrence. Aquat Invasions 4:87–94CrossRefGoogle Scholar
  14. Darling JA, Blum MJ (2007) DNA-based methods for monitoring invasive species: a review and prospectus. Biol Invasions 9:751–765CrossRefGoogle Scholar
  15. Dodgshun TJ, Taylor MD, Forrest BM (2007) Human-mediated pathways of spread for nonindigenous marine species in New Zealand. DOC Research & Development Series 266, Department of Conservation, Wellington, New Zealand. 44 p. plus appendicesGoogle Scholar
  16. Dowle E, Pochon X, Banks J, Shearer K, Wood SA (2015) Targeted gene enrichment and high-throughput sequencing for environmental biomonitoring: a case study using freshwater macroinvertebrates. Mol Ecol Resour 16:1240–1254CrossRefPubMedGoogle Scholar
  17. Edgar R (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefPubMedGoogle Scholar
  18. Edgar R, Flyvbjerg H (2015) Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics 31:3476–3482CrossRefPubMedGoogle Scholar
  19. Edgar R, Haas B, Clemente J et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  20. Ficetola GF, Pansu J, Bonin A, Coissac E, Giguet-Covex C, De Barba M, Gielly L, Lopes CM, Boyer F, Pompanon F, Rayé G, Taberlet P (2015) Replication levels, false presences and the estimation of the presence/absence from eDNA metabarcoding data. Mol Ecol Resour 15:543–556CrossRefPubMedGoogle Scholar
  21. Fletcher LM, Forrest BM, Bell JJ (2013) Impacts of the invasive ascidian Didemnum vexillum on aquaculture of the New Zealand green-lipped mussel, Perna canaliculus. Aquac Environ Interact 4:17–30CrossRefGoogle Scholar
  22. Forrest BM, Hopkins GA (2013) Population control to mitigate the spread of marine pests: insights from management of the Asian kelp Undaria pinnatifida and colonial ascidian Didemnum vexillum. Manag Biol Invasions 4:317–326CrossRefGoogle Scholar
  23. Forrest B, Sinner J (2016) A benefit-cost model for regional marine biosecurity pathway management. Prepared for Northland Regional Council. Cawthron report no. 2779. 23 pGoogle Scholar
  24. Forrest BM, Fletcher LM, Atalah J et al (2013) Predation limits spread of Didemnum vexillum into natural habitats from refuges on anthropogenic structures. PLoS ONE 8:e82229CrossRefPubMedPubMedCentralGoogle Scholar
  25. Galil B, Zenetos A (2002) A sea change—exotics in the Eastern Mediterranean Sea. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species in Europe. Distribution, impacts and management. Kluwer, Dordrecht, pp 325–336CrossRefGoogle Scholar
  26. Gollasch S (2002) The importance of ship hull fouling as a vector of species introductions into the North Sea. Biofouling 18:105–121CrossRefGoogle Scholar
  27. Gregg MD, Rigby G, Hallegraeff GM (2009) Review of two decades of progress in the development of management options for reducing or eradicating phytoplankton, zooplankton and bacteria in ship’s ballast water. Aquat Invasions 4:521–565CrossRefGoogle Scholar
  28. Griniene ES, Mazeikaite S, Gasiunaite ZR (2011) Inventory of the taxonomical composition of the plankton ciliates in the Curonian Lagoon (SE Baltic Sea). Oceanol Hydrobiol Stud 40:86–95CrossRefGoogle Scholar
  29. Guillou L, Bachar D, Audic S et al (2013) The protist ribosomal reference database (PR2): a catalogue of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res 41:D597–D604CrossRefPubMedGoogle Scholar
  30. Hopkins GA, Forrest BM (2010) A preliminary assessment of biofouling and non-indigenous marine species associated with commercial slow-moving vessels arriving in New Zealand. Biofouling J Bioadhesion Biofilm Res 26:613–621CrossRefGoogle Scholar
  31. Hopkins GA, Forrest BM, Jiang W et al (2011) Successful eradication of a non-indigenous marine bivalve from a subtidal soft-sediment environment. J Appl Ecol 48:424–431CrossRefGoogle Scholar
  32. Inglis GJ, Floerl O, Ahyong S, et al (2010) The biosecurity risks associated with biofouling on international vessels arriving in New Zealand: summary of the patterns and predictors of fouling. Biosecurity New Zealand Technical Paper No: 2008. A report prepared for MAF Biosecurity New Zealand Policy and Risk Directorate Project FP0811321 No. 182Google Scholar
  33. Johnson LE, Ricciardi A, Carlton JT (2001) Overland dispersal of aquatic invasive species: a risk assessment of transient recreational boating. Ecol Appl 11:1789–1799CrossRefGoogle Scholar
  34. Kelly RP, Closek CJ, O’Donnell JL, Kralj JE, Shelton AO, Samhouri JF (2017) Genetic and manual survey methods yield different and complementary views of an ecosystem. Front Mar Sci 3:283CrossRefGoogle Scholar
  35. Knowler DJ (2005) Reassessing the costs of biological invasion: Mnemiopsis leidyi in the Black Sea. Ecol Econ 52:187–199CrossRefGoogle Scholar
  36. Kozich J, Westcott S, Baxter N et al (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120CrossRefPubMedPubMedCentralGoogle Scholar
  37. Laroche O, Wood SA, Tremblay LA, Ellis JI, Lejzerowicz F, Pawlowski J, Lear G, Atalah J, Pochon X (2016) First evaluation of foraminiferal metabarcoding for monitoring environmental impact from an offshore oil drilling site. Mar Environ Res 120:225–235CrossRefPubMedGoogle Scholar
  38. Laroche O, Wood SA, Tremblay LA, Lear G, Ellis JI, Pochon X (2017) Metabarcoding monitoring analysis: the pros and cons of using co-extracted environmental DNA and RNA data to assess offshore oil production impacts on benthic communities. PeerJ 5:e3347CrossRefPubMedPubMedCentralGoogle Scholar
  39. Leary DH, Li RW, Hamdan LJ et al (2014) Integrated metagenomics and metaproteomic analyses of marine biofilm communities. Biofouling 30:1211–1223CrossRefPubMedGoogle Scholar
  40. Levin LA (1990) A review of methods for labelling and tracking marine invertebrate larvae. Mar Biol 146:1119–1129Google Scholar
  41. Marshall DJ, Pechenik JA, Keough MJ (2003) Larval activity levels and delayed metamorphosis affect post-larval performance in the colonial ascidian Diplosoma listerianum. Mar Ecol Prog Ser 291:159–161Google Scholar
  42. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297CrossRefGoogle Scholar
  43. McMahon RF (2011) Quagga mussel (Dreissena rostriformis bugensis) population structure during the early invasion of Lakes Mead and Mohave January–March 2007. Aquat Invasions 6:131–140CrossRefGoogle Scholar
  44. Mineur F, Johnson M, Maggs C (2008) Macroalgal introductions by hull fouling on recreational vessels: seaweeds and sailors. Environ Manag 42:667–676CrossRefGoogle Scholar
  45. Molnar JL, Gamboa RL, Revenga C et al (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492CrossRefGoogle Scholar
  46. NZOR (2016) The New Zealand Organisms Register. http://www.nzor.org.nz
  47. Oksanen J, Blanchet FG, Kindt R, et al (2014) Vegan: community ecology package. R package version 2.2-0. http://CRAN.R-project.org/package=vegan. Accessed 8 Jan 2015
  48. Ondov B, Bergman N, Phillippy A (2011) Interactive metagenomic visualization in a web browser. BMC Inform 12:385Google Scholar
  49. Pochon X, Bott NJ, Smith KF, Wood SA (2013) Evaluating detection limits of the next-generation sequencing for the surveillance and monitoring of international marine pests. PLoS ONE 8:e73935CrossRefPubMedPubMedCentralGoogle Scholar
  50. Pochon X, Zaiko A, Hopkins G et al (2015) Early detection of eukaryotic communities from marine biofilm using high-throughput sequencing: an assessment of different sampling devices. Biofouling 31:241–251CrossRefPubMedGoogle Scholar
  51. Pradillon F, Schmidt A, Peplies J et al (2007) Species identification of marine invertebrate early stages by whole-larvae in situ hybridisation of 18S ribosomal DNA. Mar Ecol Prog Ser 333:1103–1106CrossRefGoogle Scholar
  52. Quast C, Priuesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596CrossRefPubMedGoogle Scholar
  53. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  54. Ratnasingham S, Hebert PDN (2013) A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS ONE 8:e66213CrossRefPubMedPubMedCentralGoogle Scholar
  55. Rognes T (2015) VSEARCH GitHub repository. https://github.com/torognes/vsearch
  56. Ruiz GM, Carlton JT, Grosholz ED et al (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632CrossRefGoogle Scholar
  57. Ruiz GM, Rawlings TK, Dobbs FC et al (2000) Global spread of microorganisms by ships—Ballast water discharged from vessels harbours a cocktail of potential pathogens. Nature 408:49–50CrossRefPubMedGoogle Scholar
  58. Salter SJ, Cox MJ, Turek EM et al (2014) Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol 12:87CrossRefPubMedPubMedCentralGoogle Scholar
  59. Sant N, Delgado O, Rodriguez-Prieto C et al (1996) The spreading of the introduced seaweed Caulerpa taxifolia (Vahl) C. Agardh in the Mediterranean Sea: testing the boat transportation hypothesis. Bot Mar 39:427–430CrossRefGoogle Scholar
  60. Schaffelke B, Deane D (2005) Desiccation tolerance of the introduced marine green alga Codium fragile ssp. tomentosoides—clues for likely transport vectors? Biol Invasions 7:577–587CrossRefGoogle Scholar
  61. Seebens H, Gastner MT, Blasius B (2013) The risk of marine bioinvasion caused by global shipping. Ecol Lett 16:782–790CrossRefPubMedGoogle Scholar
  62. Simberloff D, Martin J-L, Genovesi P et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66CrossRefPubMedGoogle Scholar
  63. Smith KF, Wood SA, Mountfort D, Cary SC (2012) Development of a real-time PCR assay for the detection of the invasive clam, Corbula amurensis, in environmental samples. J Exp Mar Biol Ecol 412:52–57CrossRefGoogle Scholar
  64. Sreemanta P, Honghua L (2002) Direct detection of insertion/deletion polymorphisms in an autosomal region by anlayzing high-density markers in individual spermatozoa. Am J Hum Genet 71:305–313Google Scholar
  65. Valentini A, Taberlet P, Miaud C, Civade R, Herder J, Thomsen PF et al (2015) Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding. Mol Ecol 25:929–942CrossRefGoogle Scholar
  66. Wang Q, Garrity G, Tiedje J et al (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefPubMedPubMedCentralGoogle Scholar
  67. Wanless R, Scott S, Sauer W et al (2010) Semi-submersible rigs: a vector transporting entire marine communities around the world. Biol Invasions 12:2573–2583CrossRefGoogle Scholar
  68. Wong W, Gerstenberger S (2011) Quagga mussels in the western United States: monitoring and management. Aqu Invasions 6:125CrossRefGoogle Scholar
  69. Wong YH, Arellano SM, Zhang H, Ravasi T, Qian P-Y (2010) Dependency on de novo protein synthesis and proteomic changes during metamorphosis of the marine bryozoan Bugula neritina. Proteome Sci 8:25CrossRefPubMedPubMedCentralGoogle Scholar
  70. Wood SA, Smith KF, Banks JC et al (2013) Molecular genetic tools for environmental monitoring of New Zealand’s aquatic habitats, past, present and the future. N Z J Mar Freshw Res 47:90–119CrossRefGoogle Scholar
  71. Zaiko A, Samulioviene A, Ardura A et al (2015) Metabarcoding approach for non-indigenous species surveillance in marine coastal waters. Mar Pollut Bull 100:53–59CrossRefPubMedGoogle Scholar
  72. Zaiko A, Schimanski KB, Pochon X et al (2016) Metabarcoding improves detection of eukaryotes from early biofouling communities: implications for pest monitoring and pathway management. Biofouling 32:671–684CrossRefPubMedGoogle Scholar
  73. Zhan A, Hulak M, Sylvester F et al (2013) High sensitivity of 454 pyrosequencing for detection of rare species in aquatic communities. Methods Ecol Evol 4:558–565CrossRefGoogle Scholar
  74. Zuur AF, Hilbe JM, Ieno EN (2013) A beginner’s guide to GLM and GLMM with R: a Frequentist and Bayesian perspective for ecologists. Highland Statistics Ltd., NewburghGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Lauren M. Fletcher
    • 1
  • Anastasija Zaiko
    • 1
    • 2
  • Javier Atalah
    • 1
  • Ingrid Richter
    • 1
  • Celine M. Dufour
    • 1
  • Xavier Pochon
    • 1
    • 3
  • Susana A. Wood
    • 1
    • 4
  • Grant A. Hopkins
    • 1
  1. 1.Cawthron InstituteNelsonNew Zealand
  2. 2.Marine Science and Technology CenterKlaipeda UniversityKlaipedaLithuania
  3. 3.Institute of Marine ScienceUniversity of AucklandAucklandNew Zealand
  4. 4.Environmental Research InstituteUniversity of WaikatoHamiltonNew Zealand

Personalised recommendations