Advertisement

Keeping up with introduced marine species at a remote biodiversity hotspot: awareness, training and collaboration across different sectors is key

  • Mareike Huhn
  • Hawis H. Madduppa
  • Miftahul Khair
  • Amri Sabrian
  • Yulina Irawati
  • Nurlita Putri Anggraini
  • Shaun P. Wilkinson
  • Tiffany Simpson
  • Kazuma Iwasaki
  • Davin H. E. Setiamarga
  • P. Joana DiasEmail author
Original Paper
  • 48 Downloads

Abstract

Despite being a well-recognized issue, the introduction of non-native marine species is an underestimated topic in highly biodiverse developing countries. The Indonesian archipelago sits at the center of the Coral Triangle, extending over several biogeographic regions with unique benthic communities, where the extent of non-native species presence is largely unknown. It is also at the center of maritime traffic between Australasia and Asia, and therefore at risk of introduction of species that are carried on the hulls and ballast water of vessels. In the present study, we aimed to raise awareness on marine biological invasions across the Indonesian archipelago by fostering discussions among scientists, educating science students, generating media articles for the public and actively involving island communities. We also aimed to test the suitability of a range of methods commonly used in bioinvasion research (settlement arrays, DNA barcoding and environmental DNA metabarcoding, vessel surveys) to establish a baseline for biofouling species and potential threats, while developing much needed capacity for monitoring and application to other areas. We recorded 66 different non-coral specimens in the fouling communities of a remote group of islands of the Indonesian archipelago, represented mainly by the taxa Porifera, Tunicata and Mollusca, which are known to include notorious invasive species. None of the identified species was known to be invasive in the region but several were cryptogenic and/or were considered to have a very broad global distribution range that can potentially include part, or all, of the Indonesian archipelago. One species, the ascidian Didemnum molle, was found to quickly settle and spread on available blank substrates. While settlement plates (monitored every 5 months) proved suitable for early detection of potential incursions of these organisms, benthic surveys, DNA barcoding and eDNA metabarcoding provide valuable complementary baseline biodiversity information. A combination of sampling methods is therefore recommended for similar studies in understudied high biodiversity areas. Results from vessel surveys highlights the importance of civil society education in helping prevent bioinvasions. This study represents the first marine biological invasions baseline, awareness and capacity development training carried in the Indonesian archipelago. The lessons taken from the variety of methods explored in a simultaneously scientific and educational setting should prove useful and motivate similar work in other areas of the world.

Keywords

Marine education Early warning Invasive Southeast Asia Indonesia 

Notes

Acknowledgements

We would like to acknowledge the assistance of Mr. Tuta at Bluemotion Dive Center Banda in building the settlement arrays and Mr. Taufik Lama from Banda Naira for supervising the arrays in the Banda Islands and for spreading and collecting the vessel questionnaire together with Azwar Razak whom we also thank. Thank you to Miss Pipit Pitriana and Mr Masrur Islami from LIPI in Ambon for assistance with the identification of barnacles and molluscs and to the Banda Islands conservation office BKKPN. Thank you to Beginer Subhan for helping organize the initial workshop at the IPB Laboratory of Marine Biodiversity and Biosystematics, producing the project dissemination video and acting as referee during Mr Amri Sabrian and Mr Miftahul Khair BSc in Marine Science thesis examination. Thank you also to Dr. Neviaty P Zamani and Dr. Endang S. Mariana for also acting as referee during the students’ thesis examination. Further, we would like to thank Seema Fotedar, Sherralee Lukehurst and Andrea Bertram at the Department of Primary Industries and Regional Development Fisheries Division, Government of Western Australia, for assistance in the training of Miss Mutiara Kristina Margaretha and Miss Nurlita P. Anggraeni from Institut Pertanian Bogor (IPB University), within the scope of this project. Finally, thank you to Dr. Mike Bunce and Dr. Nicole White for most valuable eDNA metabarcoding support. Thank you to the Indonesian ministry Ristek Dikti for providing a foreign research permit (425/SIP/FRP/E5/Dit.KI/X/2015). This work was funded by a grant awarded to Hawis H. Madduppa and P. Joana Dias in 2015/16 by the Australian National University (ANU) Indonesia project (http://asiapacific.anu.edu.au/blogs/indonesiaproject/research-grants/research-grants-recipients).

Supplementary material

10530_2019_2126_MOESM1_ESM.xlsx (33 kb)
Supplementary material 1 (XLSX 33 kb)
10530_2019_2126_MOESM2_ESM.png (3.5 mb)
Figure S1. Settlement array structures that were deployed around Banda Naira. The rope was attached to rocks or dead coral heads on the bottom with enough slack given so that the float could keep the panels at a constant depth. (PNG 3539 kb)
10530_2019_2126_MOESM3_ESM.jpg (2 mb)
Figure S2. Colonization of Didemnum molle on ropes that were used to attach settlement structures in the natural harbour of Banda Naira. (JPEG 2055 kb)

References

  1. Albayrak S, Çağlar S (2006) On the presence of Siphonaria belcheri Hanley, 1858 [Gastropoda: Siphonariidae] and Septifer bilocularis (Linnaeus, 1758) [Bivalvia: Mytilidae] in the Iskenderun Bay (SE Turkey). Aquat Invasions 1:292–294.  https://doi.org/10.3391/ai.2006.1.4.15 CrossRefGoogle Scholar
  2. Ammon UV, Wood SA, Laroche O, Zaiko A, Tait L, Lavery S et al (2018) Combining morpho-taxonomy and metabarcoding enhances the detection of non-indigenous marine pests in biofouling communities. Sci Rep 8:16290.  https://doi.org/10.1038/s41598-018-34541-1 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Anzani L, Madduppa HH, Nurjaya IW, Dias PJ (2019) Short Communication: molecular identification of White Sea Squirt Didemnum sp. (Tunicata, Ascidiacea) colonies growing over corals in Raja Ampat Islands, Indonesia. Biodiversitas 20:636–642CrossRefGoogle Scholar
  4. Ardura A, Juanes F, Planes S, Garcia-Vazquez E (2016) Rate of biological invasions is lower in coastal marine protected areas. Sci Rep 6:1–11.  https://doi.org/10.1038/srep33013 CrossRefGoogle Scholar
  5. Arthur T, Arrowsmith L, Parsons S, Summerson R (2015) Monitoring for marine pests: a review of the design and use of Australia’s National Monitoring Strategy and identification of possible improvements. Australian Bureau of Agricultural and Resource Economics and Sciences (ABARES) Client Report, pp 63Google Scholar
  6. Barnes DKA (2017) Marine colonization and biodiversity at Ascension Island and remote islands. J Mar Biol Assoc UK 97:771–782.  https://doi.org/10.1017/S0025315415001526 CrossRefGoogle Scholar
  7. Barnes MA, Turner CR (2016) The ecology of environmental DNA and implications for conservation genetics. Conserv Genet 17:1–17CrossRefGoogle Scholar
  8. Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27:313–323CrossRefGoogle Scholar
  9. Berdej SM, Armitage DR (2016) Bridging organizations drive effective governance outcomes for conservation of Indonesia’s marine systems. PLoS ONE 11:e0147142PubMedPubMedCentralCrossRefGoogle Scholar
  10. Berry TE, Osterrieder K, Murray DC, Coghkan ML, Richardson AJ, Grealy MS, Belder L, Bunce M (2017) DNA metabarcoding for diet analysis and biodiversity: a case study using the endangered Australian sea lion (Neophoca cinerea). Ecol Evol 7:5435–5453PubMedPubMedCentralCrossRefGoogle Scholar
  11. 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. Biotechnol Adv 28:706–714PubMedCrossRefPubMedCentralGoogle Scholar
  12. Bracewell SA, Clark GF, Johnston EL (2018) Habitat complexity effects on diversity and abundance differ with latitude: an experimental study over 20 degrees. Ecology 99(9):1964–1974.  https://doi.org/10.1002/ecy.2408 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Brian JI, Davy SK, Wilkinson SP (2019) Elevated Symbiodiniaceae richness at Atauro Island (Timor-Leste): a highly biodiverse reef system. Coral Reefs 38:123–136CrossRefGoogle Scholar
  14. Bush A, Compson Z, Monk W, Porter TM, Steeves R, Emilson E, Gagne N, Hajibabaei M, Roy M, Baird DJ (2019) Studying ecosystems with DNA metabarcoding: lessons from aquatic biomonitoring. Preprint at https://www.biorxiv.org/content/10.1101/578591v1
  15. Campbell ML, Gould B, Hewitt CL (2007) Survey evaluations to assess marine bioinvasions. Mar Pollut Bull 55:360–378PubMedCrossRefPubMedCentralGoogle Scholar
  16. Campbell ML, Keith I, Hewitt CL, Dawson TP, Collins K (2015) Evolving marine biosecurity in the Galapagos islands. Manag Biol Invasions Editor 6:227–230CrossRefGoogle Scholar
  17. Campbell ML, Hewitt CL, Miles J (2016) Marine pests in paradise: capacity building, awareness raising and preliminary introduced species port survey results in the Republic of Palau. Manag Biol Invasions 7:351–363CrossRefGoogle Scholar
  18. Carlton JT (1989) Man’s role in changing the face of the ocean: biological invasions and implications for conservation of near-shore environments. Conserv Biol 3:265–273CrossRefGoogle Scholar
  19. Carlton JT (2011) The inviolate sea? Charles Elton and biological invasions in the world’s oceans. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton. Blackwell Publishing, West Sussex, pp 25–34Google Scholar
  20. Carlton JT, Eldredge LG (2015) Update and revisions of the marine bioinvasions of Hawaii: the introduced and cryptogenic marine and estuarine animals and plants of the Hawaiian archipelago. Bishop Museum Bull Zool 9:25–47Google Scholar
  21. Comtet T, Sandionigi A, Viard F, Casiraghi M (2015) DNA (meta)barcoding of biological invasions: a powerful tool to elucidate invasion processes and help managing aliens. Biol Invasions 17:905–922CrossRefGoogle Scholar
  22. Cordell JR, Levy C, Toft JD (2013) Ecological implications of invasive tunicates associated with artificial structures in Puget Sound, Washington, USA. Biol Invasions 15:1303–1318CrossRefGoogle Scholar
  23. Courchamp F, Fournier A, Bellard C, Bertelsmeier C, Bonnaud E, Jeschke JM, James CR (2017) Invasion biology: specific problems and possible solutions. Trends Ecol Evol 32:13–22PubMedCrossRefPubMedCentralGoogle Scholar
  24. Crombie J, Knight E, Barry S (2008) Marine pest incursions: a tool to predict the cost of eradication based on expert assessments. Australian Government Bureau of Rural Sciences, Commonwealth of Australia, Canberra, p 38Google Scholar
  25. Darling JA, Blum MJ (2007) DNA-based methods for monitoring invasive species: a review and prospectus. Biol Invasions 9:751–765CrossRefGoogle Scholar
  26. Darling JA, Galil BS, Carvalho GR, Rius M, Viard F, Piraino S (2017) Recommendations for developing and applying genetic tools to assess and manage biological invasions in marine ecosystems. Mar Policy 85:54–64CrossRefGoogle Scholar
  27. Deagle BE, Gales NJ, Evans K, Jarman SN, Robinson S, Trebilco R, Hindell MA (2007) Studying seabird diet through genetic analysis of faeces: a case study on macaroni penguins (Eudyptes chrysolophus). PLoS ONE 2:e831.  https://doi.org/10.1371/journal.pone.0000831 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Dias JP, Fotedar S, Muenoz J et al (2017) Establishment of a taxonomic and molecular reference collection to support the identification of species regulated by the Western Australian Prevention List for Introduced Marine Pests. Manag Biol Invasions 8:215–225.  https://doi.org/10.3391/mbi.2017.8.2.09 CrossRefGoogle Scholar
  29. Drew LW (2011) Are we losing the science of taxonomy? Bioscience 61:942–946.  https://doi.org/10.1525/bio.2011.61.12.4 CrossRefGoogle Scholar
  30. Early R, Bradley BA, Dukes JS, Lawler JJ, Olden JD, Blumenthal DM, Gonzalez P, Grosholz ED, Ibañez I, Miller LP, Sorte CJB, Tatem AJ (2017) Global threats from invasive alien species in the twenty-first century and national response capacities. Nat Commun.  https://doi.org/10.1038/ncomms12485 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods.  https://doi.org/10.1038/nmeth.2604 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Evenhuis N, Carlton JT (2015) Lucius G Eldredge III Memorial Volumen: Tribute to a Polymath. Bishop Museum Bulletin in Zoology (vol. 9). Honolulu, Hawaii: Bishop Museum Press. Retrieved from http://hbs.bishopmuseum.org/pubs-online/pdf/bz9-full-online.pdf#page=131
  33. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primersfor amplification of mitochondrial cytochromecoxidase subunit I fromdiverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299Google Scholar
  34. Greenfield P (2017) Greenfield hybrid analysis pipeline (GHAP).v1.CSIRO. Software Collection.  https://doi.org/10.4225/08/59f98560eba25
  35. Guiry MD (2015) Valonia ventricosa J. Agardh, 1887. In: Guiry MD, Guiry GM (2017). AlgaeBase. World-wide electronic publication, National University of Ireland, Galway (taxonomic information republished from AlgaeBase with permission of M.D. Guiry). Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=211680 on 2018-02-02
  36. Guiry MD, Guiry GM (2018) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org on, 02 Feb 2018
  37. Hajibabaei M, Shokralla S, Zhou X, Singer GAC, Baird DJ (2011) Environmental barcoding: a next-generation sequencing approach for biomonitoring applications using river benthos. PLoS ONE 6:e17497.  https://doi.org/10.1371/journal.pone.0017497 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hayes KR, Cannon R, Neil K, Inglis G (2005) Sensitivity and cost considerations for the detection and eradication of marine pests in ports. Mar Pollut Bull 50:823–834PubMedCrossRefPubMedCentralGoogle Scholar
  39. Hewitt CL (2002) Distribution and biodiversity of Australian tropical marine bioinvasions. Pac Sci 56:213–222CrossRefGoogle Scholar
  40. Hoeksema BW (1997) Generic diversity of Scleractinia in Indonesia. In: Tomascik T, Mah AJ, Nontji A, Moosa MK (eds) The ecology of the Indonesian seas, Part I. Periplus, Singapore, pp 308–311Google Scholar
  41. Huffard CL, Erdmann MV, Gunawan TRP (2012) Geographic priorities for marine biodiversity conservation in Indonesia. Ministry of Marine Affairs and Fisheries and Marine Protected Areas Governance Program. Jakarta Indonesia, 105 ppGoogle Scholar
  42. Jaafar Z, Yeo DCJ, Tan H, O’Riordan RM (2012) Status of Estuarine and marine non-Indigenous species in Singapore. The Raffles Bulletin of Zoology Supplement No. 25, 79–92Google Scholar
  43. Jablonski D, Belanger CL, Berke SK, Huang S, Krug AZ, Roy K, Tomasovych A, Valentine JW (2013) Out of the tropics, but how? Fossils, bridge species, and thermal ranges in the dynamics of the marine latitudinal diversity gradient. Proc Natl Acad Sci USA 110:10487–10494.  https://doi.org/10.1073/pnas.1308997110 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Januari HI, Zamani NP, Soedharma D, Chasanah E (2017) Cembranoids of soft coral sarcophyton from acidified coral reef environment at shallow water CO2 vents in Volcano Island, Banda Neira, Indonesia. Squalen Bulletin.  https://doi.org/10.15578/squalen.v12i1.276
  45. Jeunen GJ, Knapp M, Spencer HG, Taylor HR, Lamare MD, Stat M, Bunce M, Gemmel NJ (2018) Species-level biodiversity assessment using marine environmental DNA metabarcoding requires protocol optimization and standardization. Ecol Evol 1–13Google Scholar
  46. Jeunen GJ, Knapp M, Spencer HG, Lamare MD, Taylor HR, Stat M, Bunce M, Gemmell NJ (2019) Environmental DNA (eDNA) metabarcoding reveals strong discrimination among diverse marine habitats connected by water movement. Mol Ecol Resour 19:426–438.  https://doi.org/10.1111/1755-0998.12982 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Klein J, Verlaque M (2008) The Caulerpa racemosa invasion: a critical review. Mar Pollut Bull 56:205–225.  https://doi.org/10.1016/j.marpolbul.2007.09.043 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Koziol A, Stat M, Simpson T, Jarman S, DiBattista JD, Harvey ES, Marnane M, McDonald J, Bunce M (2018) Environmental DNA metabarcoding studies are critically affected by substrate selection. Mol Ecol Resour 19:366–376.  https://doi.org/10.1111/1755-0998.12971 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Lovei GL, Lewinsohn TM (2012) Megadiverse developing countries face huge risks from invasives. Trends Ecol Evol Lett 27:2–3CrossRefGoogle Scholar
  50. Madduppa H, Schupp PJ, Faisal MR, Sastria MY, Thoms C (2017) Persistent outbreaks of the ‘black disease’ sponge Terpios hoshinota in Indonesian coral reefs. Mar Biodivers 47:149–151CrossRefGoogle Scholar
  51. Marraffini ML, Ashton GV, Brown CW, Chang AL, Ruiz GM (2017) Settlement plates as monitoring devices for non-indigenous species in marine fouling communities. Manag Biol Invasions 8:559–566.  https://doi.org/10.3391/mbi.2017.8.4.11 CrossRefGoogle Scholar
  52. McGeoch MA, Genovesi P, Bellingham PJ, Costello MJ, McGrannachan C, Sheppard A (2016) Prioritizing species, pathways, and sites to achieve conservation targets for biological invasion. Biol Invasions 18:299–314CrossRefGoogle Scholar
  53. McManus JW (1997) Tropical marine fisheries and the future of coral reefs: a brief review with emphasis on Southeast Asia. Coral Reef 2:129–134Google Scholar
  54. Meinesz A, Belsher T, Thibaut T et al (2001) The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean. Biol Invasions 3:201–210.  https://doi.org/10.1023/A:1014549500678 CrossRefGoogle Scholar
  55. MolluscaBase (2019). Mollusca base. Pinctada margaritifera (Linnaeus, 1758). Accessed through: World Register of Marine Species at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=207899 on 2019-08-25
  56. Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6(9):485–492CrossRefGoogle Scholar
  57. Morales M (2017) sciplot: Scientific graphing functions for factorial designs. R Development Core Team online at https://cran.r-project.org/web/packages/sciplot/index.html
  58. Mous PJ (2002) Report on a rapid ecological assessment of the Banda Islands, Maluku, Eastern Indonesia, held April 28–May 5 2002, Nature Conservancy, 153 pp, Sanur, Bali, IndonesiaGoogle Scholar
  59. Murray DC, Coghlan ML, Bunce M (2015) From benchtop to desktop: important considerations when designing amplicon sequencing workflows. PLoS ONE 10:e0124671PubMedPubMedCentralCrossRefGoogle Scholar
  60. Nunez MA, Pauchard A (2010) Biological invasions in developing and developed countries: does one model fit all? Biol Invasions 12:707–714CrossRefGoogle Scholar
  61. Ojaveer H, Galil BS, Carlton JT, Alleway H, Goulletquer P, Lehtiniemi M et al (2018) Historical baselines in marine bioinvasions: implications for policy and management. PLoS ONE 13:e0202383PubMedPubMedCentralCrossRefGoogle Scholar
  62. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017). Vegan: community ecology package. R package version 2.4-5. https://CRAN.R-project.org/package=vegan
  63. Otani M, Oumi T, Uwai S, Hanyuda T, Prabowo RE, Yamaguchi T, Kawai H (2007) Occurrence and diversity of barnacles on international ships visiting Osaka Bay, Japan, and the risk of their introduction. Biofouling 23:277–286.  https://doi.org/10.1080/08927010701315089 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Papacostas KJ, Rielly-Carroll EW, Georgian SE et al (2017) Biological mechanisms of marine invasions. Mar Ecol Prog Ser 565:251–268.  https://doi.org/10.3354/meps12001 CrossRefGoogle Scholar
  65. Peh KSH (2010) Invasive species in Southeast Asia: the knowledge so far. Biodivers Conserv 19:1083–1099CrossRefGoogle Scholar
  66. Piola RF, Johnston EL (2008) Pollution reduces native diversity and increases invader dominance in marine hard-substrate communities. Divers Distrib 14:329–342.  https://doi.org/10.1111/j.1472-4642.2007.00430.x CrossRefGoogle Scholar
  67. Pochon X, Bott NJ, Smith KF, Wood S (2013) Evaluating detection limits of next-generation sequencing for the surveillance and monitoring of international marine pests. PLoS ONE 8:e73935PubMedPubMedCentralCrossRefGoogle Scholar
  68. Quas TC, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl Acids Res 41:D590–D596CrossRefGoogle Scholar
  69. Reaka ML, Rodgers PJ, Kudla AU (2008) Patterns of biodiversity and endemism on Indo-West Pacific coral reefs. Proc Natl Acad Sci 105:11474–11481.  https://doi.org/10.1073/pnas.0802594105 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Ruiz G, Carlton J (2003) Invasion vectors: a conceptual framework for management. In: Ruiz G, Carlton J (eds) Invasive species vectors and management strategies. Island Press, Washington, pp 459–504Google Scholar
  71. Ruiz G, Freestone A, Fofonoff P, Simkanin C (2009) Habitat distribution and heterogeneity in marine invasion dynamics: the importance of hard substrate and artificial structure. In: Wahl M (ed) Marine hardbottom communities. Springer, Berlin.  https://doi.org/10.1007/b76710_23 CrossRefGoogle Scholar
  72. Saunders GW, Kucera H (2010) An evaluation of rbcL, tufA, UPA, LSU and ITS as DNA barcode markers for the marine macroalgae. Cryptogam Algol 31:487–528Google Scholar
  73. Schmidt A, Wehrmann A, Dittmann S (2008) Population dynamics of the invasive Pacific oyster Crassostrea gigas during the early stages of an outbreak in the Wadden Sea (Germany). Helgol Mar Res 62:367–376CrossRefGoogle Scholar
  74. Seebens H, Gastner MT, Blasius B (2013) The risk of marine bioinvasion caused by global shipping. Ecol Lett 16:782–790.  https://doi.org/10.1111/ele.12111 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Seebens H, Blackburn TM, Dyer EE et al (2017) No saturation in the accumulation of alien species worldwide. Nat Commun 8:14435.  https://doi.org/10.1038/ncomms14435 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Shenkar N, Gittenberger A, Lambert G, Rius M, Moreira Da Rocha R, Swalla BJ, Turon X (2019). Ascidiacea World database. Accessed through: World Register of Marine Species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=212513 on 2019-08-25
  77. Simberloff D, Martin J, 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 28:58–66PubMedCrossRefPubMedCentralGoogle Scholar
  78. Sokołowski A, Ziółkowska M, Balazy P, Kukliński P, Plichta I (2017) Seasonal and multi-annual patterns of colonisation and growth of sessile benthic fauna on artificial substrates in the brackish low-diversity system of the Baltic Sea. Hydrobiologia 790:183–200.  https://doi.org/10.1007/s10750-016-3043-9 CrossRefGoogle Scholar
  79. Sorte CJB, Williams SL, Zerebrcki RA (2010) Ocean warming increases threat of invasive species in a marine fouling community. Ecology 91:2198–2204PubMedCrossRefPubMedCentralGoogle Scholar
  80. Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Sci New Ser 286:1577–1579.  https://doi.org/10.1126/science.286.5444.1577 CrossRefGoogle Scholar
  81. Stat M, Huggett MJ, Bernasconi R, DiBattista JD, Berry TE, Newman SJ, Harvey E, Bunce M (2017a) Ecosystem biomonitoring with eDNA: metabarcoding across the tree of life in a tropical marine environment. Sci Rep 7:12240.  https://doi.org/10.1038/s41598-017-12501-5 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Stat M, Huggett MJ, Bernasconi R, DiBattista JD, Berry TE, Newman SJ, Harvey ES, Bunce M (2017b) Ecosystem biomonitoring with eDNA: metabarcoding across the tree of life in a tropical marine environment. Sci Rep 7:12240.  https://doi.org/10.1038/s41598-017-12501-5 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Stefaniak L, Lambert G, Gittenberger A, Zhang H, Lin S, Whitlatch RB (2009) Genetic conspecificity of the worldwide populations of Didemnum vexillum Kott, 2002. Aquat Invasions 4:29–44CrossRefGoogle Scholar
  84. Summerson R, Skirtun M, Mazur K, Arthur T, Curtotti R, Smart R (2013) Economic evaluation of the costs of biosecurity response options to address an incursion of Mytilopsis sallei (blackstriped mussel) into Australia, ABARES Report to client prepared for Plant Health Australia, CanberraGoogle Scholar
  85. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
  86. Thomsen PF, Kielgast J, Iversen LL, Moller PR, Rasmussen M, Willerslev E (2012) Detection of a diverse marine fish fauna using environmental DNA from seawater samples. PLoS ONE 7:e41732PubMedPubMedCentralCrossRefGoogle Scholar
  87. UNEP (2011) The strategic plan for biodiversity 2011–2020 and the Aichi biodiversity targets. UNEP/CBD/COP/DEC/X/2, 29 October 2010, Nagoya, Japan. COP CBD Tenth MeetingGoogle Scholar
  88. Valentini A, Taberlet P, Miaud C, Civade R, Herder J, Thomsen PF, Bellemain E et al (2016) Next-generation monitoring of aquatic biodiversity using environmental DNA metabarcoding. Mol Ecol 25:929–942.  https://doi.org/10.1111/mec.13428 CrossRefPubMedPubMedCentralGoogle Scholar
  89. van Soest R (2008) Petrosia (Petrosia) ficiformis (Poiret, 1789). In: Van Soest RWM, Boury-Esnault N, Hooper JNA, Rützler K, de Voogd NJ, Alvarez B, Hajdu E, Pisera AB, Manconi R, Schönberg C, Klautau M, Picton B, Kelly M, Vacelet J, Dohrmann M, Díaz MC, Cárdenas P, Carballo JL, Rios P, Downey R (2017). World Porifera database. Accessed through: World Register of Marine Species at http://marinespecies.org/aphia.php?p=taxdetails&id=166837 on 2018-02-02
  90. van Soest R (2009) Monanchora clathrata Carter, 1883. In: Van Soest RWM, Boury-Esnault N, Hooper JNA, Rützler K, de Voogd NJ, Alvarez B, Hajdu E, Pisera AB, Manconi R, Schönberg C, Klautau M, Picton B, Kelly M, Vacelet J, Dohrmann M, Díaz MC, Cárdenas P, Carballo JL, Rios P, Downey R (2017). World Porifera database. Accessed through: World Register of Marine Species 169017 at http://www.marinespecies.org/aphia.php?p=taxdetails&id=169017 on 2018-02-02
  91. van Soest RWM, Boury-Esnault N, Vacelet J, Dohrmann M, Erpenbeck D, de Voogd NJ, Santodomingo N, Vanhoorne B, Kelly M, Hooper JNA (2012) Global diversity of sponges (Porifera). PLoS ONE 7:e35105PubMedPubMedCentralCrossRefGoogle Scholar
  92. Welly M, Djohani R, Suharsono, Green A, Muljadi A, Korebima M, Hehuat Y, Alik R, Rijoli N (2012) Kajian Cepat Kelautan Kepulauan Banda, Maluku Tengah, Indonesia. Coral Triangle Center, Report, 173 ppGoogle Scholar
  93. Wilkinson SP, Davy SK, Bunce M, Stat M (2018) Taxonomic identification of environmental DNA with informatic sequence classification trees. PeerJ.  https://doi.org/10.7287/peerj.preprints.26812v1 CrossRefGoogle Scholar
  94. Wyatt ASJ, Hewitt CL, Walker DI, Ward TJ (2005) Marine introductions in the Shark Bay World Heritage Property, Western Australia: a preliminary assessment. Divers Distrib 11:33–44CrossRefGoogle Scholar
  95. Zaiko A, Samuiloviene A, Ardura A, Garcia-Vazquez E (2015) Metabarcoding approach for nonindigenous species surveillance in marine coastal waters. Mar Pollut Bull 100:53–59PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Mareike Huhn
    • 1
    • 2
  • Hawis H. Madduppa
    • 1
  • Miftahul Khair
    • 1
  • Amri Sabrian
    • 1
  • Yulina Irawati
    • 1
  • Nurlita Putri Anggraini
    • 1
  • Shaun P. Wilkinson
    • 3
  • Tiffany Simpson
    • 4
  • Kazuma Iwasaki
    • 5
  • Davin H. E. Setiamarga
    • 5
  • P. Joana Dias
    • 6
    Email author
  1. 1.Department of Marine Science and Technology, Faculty of Fisheries and Marine ScienceInstitut Pertanian Bogor (IPB University)BogorIndonesia
  2. 2.Department of General Zoology and NeurobiologyRuhr-University BochumBochumGermany
  3. 3.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand
  4. 4.Trace and Environmental DNA (TrEnD) Laboratory, Department of Environment and AgricultureCurtin UniversityPerthAustralia
  5. 5.Department of Applied Chemistry and Biochemistry, National Institute of TechnologyWakayama CollegeGoboJapan
  6. 6.NRC Research AssociateNOAA Northwest Fisheries Science CenterSeattleUSA

Personalised recommendations