Advertisement

Molecular survey of the red algal family Rhodomelaceae (Ceramiales, Rhodophyta) in Australia reveals new introduced species

  • Cristina Piñeiro-Corbeira
  • Heroen Verbruggen
  • Pilar Díaz-TapiaEmail author
23rd INTERNATIONAL SEAWEED SYMPOSIUM, JEJU

Abstract

Red algae are frequently dominant components of the non-native biotas in coastal areas. They often remain undetected because of morphological similarity between native and introduced species and cryptic diversity. Routine use of DNA barcodes can aid in setting baseline tabulations of native species and for detecting introduced species. We performed an extensive survey of the red algal family Rhodomelaceae in southern Australia, producing a dataset containing more than 1100 rbcL sequences. The objective of this study was to screen that dataset for introduced species of the tribes Polysiphoniaeae and Streblocladieae, and to provide morphological information of presumably introduced species that were not previously recorded in Australia. Molecular data and morphological observations confirmed the presence of five presumably introduced species: Leptosiphonia brodiei, Melanothamnus japonicus, M. strictissimus, Polysiphonia morrowii and P. delicata. Polysiphonia morrowii and M. strictissimus were detected for the first time in Australia, and M. japonicus and P. delicata were found to be more widely distributed than previously known. Somewhat unexpectedly, the distribution range of L. brodiei has apparently shrunk, with our survey suggesting it remains only in Tasmania. Four of these species have been reported as introduced species in other countries, but M. strictissimus is here recorded for the first time outside its native New Zealand. Although all five species can be considered introduced or cryptogenic, only P. morrowii, M. japonicus and M. strictissimus were locally abundant, and further work will be needed to assess their ability to spread and effect negative impacts on native biotas.

Keywords

Cryptic introductions Introduction vectors Melanothamnus Polysiphonia Non-native species Red algae 

Notes

Acknowledgements

We thank Joana Costa, Kyatt Dixon, Margaret Brookes and Guadalupe Bribiesca-Contreras and the Parks Victoria and Bush Blitz teams for assistance in the field.

Funding information

P.D.T. acknowledges support from the postdoctoral program “Axudas de apoio á etapa de formación posdoutoral, Xunta de Galicia” (ED481D2017/011). C.P.C. and P.D.T. received funding from Xunta de Galicia within the program “Axudas para a consolidación e estruturación de unidades de investigación competitivas do SUG” (grants GPC2015/025, ED431D 2017/20, ED431B 2018/49). Funding for the field and molecular work in eastern Victoria, including participation in a Bush Blitz expedition, a Bush Blitz Strategic Taxonomy Grant (TTC216-03) and a National Taxonomy Research Grant (RFL213-08), was provided by the Australian Biological Resources Study. Sampling in Western Australia and Tasmania was made possible through funding from the Holsworth Wildlife Research Endowment.

Supplementary material

10811_2019_1932_MOESM1_ESM.pdf (187 kb)
ESM 1 (PDF 186 kb)

References

  1. Adams NM (1991) The New Zealand species of Polysiphonia Greville. N Z J Bot 29:411–427CrossRefGoogle Scholar
  2. Arenas F, Bishop JDD, Carlton JT, Dyrynda PJ, Farnham WF, González DJ, Jacobs MW, Lambert C, Lambert G, Nielsen SE, Pederson JA, Porter JS, Ward S, Wood CA (2006) Alien species and other notable records from a rapid assessment survey of marinas on the south coast of England. J Mar Biol Assoc UK 86:1329–1337CrossRefGoogle Scholar
  3. Carlton JT, Geller JT (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82CrossRefGoogle Scholar
  4. Casas G, Scrosati R, Luz Piriz M (2004) The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo gulf (Patagonia, Argentina). Biol Invasions 6:411–416CrossRefGoogle Scholar
  5. Croce ME, Parodi ER (2014) The Japanese alga Polysiphonia morrowii (Rhodomelaceae, Rhodophyta) on the South Atlantic Ocean: first report of an invasive macroalga inhabiting oyster reefs. Helgol Mar Res 68:241–252CrossRefGoogle Scholar
  6. Curiel D, Bellemo G, La Rocca B, Scattolin M, Marzocchi M (2002) First report of Polysiphonia morrowii Harvey (Ceramiales, Rhodophyta) in the Mediterranean Sea. Bot Mar 45:66–70CrossRefGoogle Scholar
  7. D'Archino R, Neill KF, Nelson WA (2013) Recognition and distribution of Polysiphonia morrowii (Rhodomelaceae, Rhodophyta) in New Zealand. Bot Mar 56:41–47Google Scholar
  8. Díaz-Tapia P, Kim MS, Secilla A, Bárbara I, Cremades J (2013) Taxonomic reassessment of Polysiphonia foetidissima (Rhodomelaceae, Rhodophyta) and similar species, including P. schneideri, a new introduced species in Europe. Eur J Phycol 48:345–362CrossRefGoogle Scholar
  9. Díaz-Tapia P, Bárbara I, Cremades J, Verbruggen H, Maggs CA (2017a) Three new cryptogenic species in the tribes Polysiphonieae and Streblocladieae (Rhodomelaceae, Rhodophyta). Phycologia 56:605–623CrossRefGoogle Scholar
  10. Díaz-Tapia P, Maggs CA, West JA, Verbruggen H (2017b) Analysis of chloroplast genomes and a supermatrix inform reclassification of the Rhodomelaceae (Rhodophyta). J Phycol 53:920–937PubMedCrossRefGoogle Scholar
  11. Díaz-Tapia P, Maggs CA, Macaya EC, Verbruggen H (2018) Widely distributed red algae often represent hidden introductions, complexes of cryptic species or species with strong phylogeographic structure. J Phycol 54:829–839PubMedCrossRefGoogle Scholar
  12. Díaz-Tapia P, Maggs CA, Nelson W, Macaya EC, Verbruggen H (2019) Reassessment of the genus Lophurella (Rhodomelaceae, Rhodophyta) from Australia and New Zealand reveals four cryptic species. Eur J Phycol in pressGoogle Scholar
  13. Epstein G, Smale DA (2017) Undaria pinnatifida: a case study to highlight challenges in marine invasion ecology and management. Ecol Evol 7:8624–8642PubMedPubMedCentralCrossRefGoogle Scholar
  14. Foster SD, Griffin DA, Dunstan PK (2014) Twenty years of high-resolution sea surface temperature imagery around Australia: inter-annual and annual variability. PLoS One 9:e100762PubMedPubMedCentralCrossRefGoogle Scholar
  15. 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 100:67–71CrossRefGoogle Scholar
  16. Geoffroy A, Destombe C, Kim B, Mauger S, Raffo MP, Kim MS, Le Gall L (2016) Patterns of genetic diversity of the cryptogenic red alga Polysiphonia morrowii (Ceramiales, Rhodophyta) suggest multiple origins of the Atlantic populations. Ecol Evol 6:5635–5647PubMedPubMedCentralCrossRefGoogle Scholar
  17. Gregory LP, Campbell ML, Primo C, Hewitt CL (2012) Biotic and abiotic factors affecting the Tasmanian distribution and density of the introduced New Zealand porcelain crab Petrolisthes elongatus. Aquat Invasions 7:491–501CrossRefGoogle Scholar
  18. Guiry MD, Guiry GM (2019) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. https://www.algaebase.org; searched on 7 June 2019.Google Scholar
  19. Hardin G (1960) The competitive exclusion principle. Science 131:1292–1297PubMedCrossRefGoogle Scholar
  20. Hayes K, Sliwa C, Migus S, McEnnulty F, Dunstan P (2005) National priority pests: part II ranking of Australian marine pests. An independent report undertaken for the Department of Environment and Heritage by CSIRO Marine Research.Google Scholar
  21. Hewitt CL, Campbell ML (2007) Mechanisms for the prevention of marine bioinvasions for better biosecurity. Mar Pollut Bull 55:395–401PubMedCrossRefGoogle Scholar
  22. Huisman JM (2018) Algae of Australia. Marine benthic algae of north-western Australia. 2. Red algae. ABRS and CSIRO Publishing, Canberra and Melbourne. 672 pp.Google Scholar
  23. Hutchings P (2013) Why are taxonomists often regarded as second class citizens? A misclassification that threatens the basic infrastructure of biodiversity. In: Lunney D, Hutchings P, Recher H (eds) Grumpy scientists. Royal Zoological Society of New South Wales, Mosman, pp 26–30CrossRefGoogle Scholar
  24. Hutchings P (2018) Marine introduced species in Australia, where to from here? A personal perspective from a practising taxonomist. Mar Pollut Bull 136:477–480PubMedCrossRefGoogle Scholar
  25. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649PubMedPubMedCentralCrossRefGoogle Scholar
  26. Kim M-S, Yang EC, Mansilla A, Boo SM (2004) Recent introduction of Polysiphonia morrowii (Ceramiales, Rhodophyta) to Punta Arenas, Chile. Bot Mar 47:389–394CrossRefGoogle Scholar
  27. Krueger-Hadfield SA, Kollars NM, Strand AE, Byers JE, Shainker SJ, Terada R, Greig TW, Hammann M, Murray DC, Weinberger F, Sotka EE (2016) The identification of source and vector of a prolific marine invader. Ecol Evol 7:4432–4447CrossRefGoogle Scholar
  28. Lohrer AM, Whitlatch RB (2002) Interactions among aliens: apparent replacement of one exotic species by another. Ecology 83:719–732CrossRefGoogle Scholar
  29. Manghisi A, Miladi R, Armeli Minicante S, Genovese G, Le Gall L, Abdelkafi S, Saunders GW, Morabito M (2019) DNA barcoding sheds light on novel records in the Tunisian red algal flora. Cryptogam Algol 40:5–27CrossRefGoogle Scholar
  30. Maggs CA, Hommersand M (1993) Seaweeds of the British Isles. Volume 1. Rhodophyta. Part 3A. Ceramiales. HMSO, London. pp. 444.Google Scholar
  31. Maggs CA, Stegenga H (1998) Red algal exotics on North Sea coasts. Helgol Meeresunters 52:243–258CrossRefGoogle Scholar
  32. McIvor L, Maggs CA, Provan J, Stanhope MJ (2001) rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi. Mol Ecol 10:911–919PubMedCrossRefGoogle Scholar
  33. Meynard A, Zapata J, Salas N, Betancourtt C, Pérez‐Lara G, Castañeda F, Ramírez ME, Contador CB, Guillemin M-L, Contreras‐Porcia L, Müller K (2019) Genetic and morphological differentiation of and species (Bangiales, Rhodophyta) coexisting in a rocky intertidal in Central Chile . J Phycol 55 (2):297-313Google Scholar
  34. Mineur F, Belsher T, Johnson MP, Maggs CA, Verlaque M (2007a) Experimental assessment of oyster transfers as a vector for macroalgal introductions. Biol Conserv 137:237–247CrossRefGoogle Scholar
  35. Mineur F, Johnson MP, Maggs CA (2008) Macroalgal introductions by hull fouling on recreational vessels: seaweeds and sailors. Environ Manag 42:667–676CrossRefGoogle Scholar
  36. Mineur F, Johnson MP, Maggs CA, Stegenga H (2007b) Hull fouling on commercial ships as a vector of macroalgal introduction. Mar Biol 151:1299–1307CrossRefGoogle Scholar
  37. Mineur F, Le Roux A, Maggs CA, Verlaque M (2014) Positive feedback loop between introductions of non-native marine species and cultivation of oysters in Europe. Conserv Biol 28:1667–1676PubMedCrossRefGoogle Scholar
  38. Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492CrossRefGoogle Scholar
  39. Mobsby D, Koduah A (2017) Australian fisheries and aquaculture statistics 2016, Fisheries Research and Development Corporation project 2017-095. ABARES, CanberraGoogle Scholar
  40. Nam KW, Kang PJ (2012) Algal flora of Korea. Volume 4, number 4. Rhodophyta: Ceramiales: Rhodomelaceae: 18 genera including Herposiphonia. National Institute of Biological Resources, Incheon, p 178Google Scholar
  41. Nelson WA (1999) A revised checklist of marine algae naturalised in New Zealand. N Z J Bot 37:355–359CrossRefGoogle Scholar
  42. Nelson WA (2013) New Zealand seaweeds. An illustrated guide. Te Papa Press, Wellington, p 328Google Scholar
  43. Nelson WA, Maggs CA (1996) Records of adventive marine algae in New Zealand: Antithamnionella ternifolia, Polysiphonia senticulosa (Ceramiales, Rhodophyta) and Striaria attenuata (Dictyosiphonales, Phaeophyta). N Z J Mar Freshwat Res 30:449–453CrossRefGoogle Scholar
  44. Oliveira MC, Repetti SI, Iha C, Jackson CJ, Diaz-Tapia P, Magalhaes K, Cassano V, Costa JF, MCM C, Marcelino VR, Verbruggen H (2018) High–throughput sequencing for algal systematics. Eur J Phycol 53:256–272CrossRefGoogle Scholar
  45. Ogburn DM (2007) Environmental impacts in Australian aquaculture. In: Bert TM (ed) Ecological and genetic implications of aquaculture activities. Springer, Dordrecht, pp 177–189CrossRefGoogle Scholar
  46. Saunders GW, McDevit DC (2012) Methods for DNA barcoding photosynthetic protists emphasizing the macroalgae and diatoms. In: Kress W, Erickson D (eds) DNA barcodes. Methods in molecular biology. Methods and protocols. Humana Press, Totowa, pp 207–222CrossRefGoogle Scholar
  47. Saunders GW, Moore TE (2013) Refinements for the amplification and sequencing of red algal DNA barcode and RedToL phylogenetic markers: a summary of current primers, profiles and strategies. Algae 28:31–43CrossRefGoogle Scholar
  48. Saunders GW, Huisman JM, Vergés A, Kraft GT, Le G (2017) Phylogenetic analyses support recognition of ten new genera, ten new species and 16 new combinations in the family Kallymeniaceae (Gigartinales, Rhodophyta). Cryptogam Algol 28:79–132CrossRefGoogle Scholar
  49. Savoie AM, Saunders GW (2015) Evidence for the introduction of the Asian red alga Neosiphonia japonica and its introgression with Neosiphonia harveyi (Ceramiales, Rhodophyta) in the Northwest Atlantic. Mol Ecol 24:5927–2937PubMedCrossRefGoogle Scholar
  50. Savoie AM, Saunders GW (2016) A molecular phylogenetic and DNA barcode assessment of the tribe Pterosiphonieae (Ceramiales, Rhodophyta) emphasizing the Northeast Pacific. Botany 94:917–939CrossRefGoogle Scholar
  51. Savoie AM, Saunders GW (2019) A molecular assessment of species diversity and generic boundaries in the red algal tribes Polysiphonieae and Streblocladieae (Rhodomelaceae, Rhodophyta) in Canada. Eur J Phycol 54:1–25CrossRefGoogle Scholar
  52. Scheibling RE, Gagnon P (2006) Competitive interactions between the invasive green alga Codium fragile ssp tomentosoides and native canopy-forming seaweeds in Nova Scotia (Canada). Mar Ecol Prog Ser 325:1–14CrossRefGoogle Scholar
  53. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313PubMedPubMedCentralCrossRefGoogle Scholar
  54. Steen F, Aragay J, Zuljevic A, Verbruggen H, Mancuso FP, Bunker F, Vitales D, Gómez Garreta A, De Clerck O (2017) Tracing the introduction history of the brown seaweed Dictyota cyanoloma (Phaeophyceae, Dictyotales) in Europe. Eur J Phycol 52:31–42CrossRefGoogle Scholar
  55. Thomsen MS, Wernberg T, South PM, Schiel DR (2016) Non-native seaweeds drive changes in marine coastal communities around the world. In: Hu Z-M, Fraser C (eds) Seaweed phylogeography: adaptation and evolution of seaweeds under environmental change. Springer, Dordrecht, pp 147–185CrossRefGoogle Scholar
  56. Verbruggen H, Brookes MJL, Costa JF (2017) DNA barcodes and morphometric data indicate that Codium fragile (Bryopsidales, Chlorophyta) may consist of two species. Phycologia 56:54–62CrossRefGoogle Scholar
  57. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359CrossRefGoogle Scholar
  58. Wolf MA, Buosi A, Juhmani A-SF, Sfriso A (2018) Shellfish import and hull fouling as vectors for new red algal introductions in the Venice lagoon. Estuar Coast Shelf Sci 215:30–38CrossRefGoogle Scholar
  59. Womersley HBS (1979) Southern Australian species of Polysiphonia Greville (Rhodophyta). Aust J Bot 27:459–528CrossRefGoogle Scholar
  60. Womersley HBS (1990) Biogeography of Australasian marine macroalgae. In: Clayton MN, King RJ (eds) Biology of marine plants. Longman, Melbourne, pp 367–381Google Scholar
  61. Womersley HBS (1994) The marine benthic flora of southern Australia - part IIIA Bangiophyceae and Florideophyceae (Acrochaetiales, Nemaliales, Gelidiales, Hildenbrandiales and Gigartinales sensu lato). Australian Biological Resources Study and State Herbarium of South Australia, Canberra and Adelaide. pp. 508Google Scholar
  62. Womersley HBS (1996) The marine benthic flora of southern Australia - part IIIB Gracilariales, Rhodymeniales, Corallinales and Bonnemaisoniales. Australian Biological Resources Study and State Herbarium of South Australia, Canberra and Adelaide. pp. 392Google Scholar
  63. Womersley HBS (1998) The marine benthic flora of southern Australia - part IIIC Ceramiales - Ceramiaceae, Dasyaceae. Australian Biological Resources Study and State Herbarium of South Australia, Canberra and Adelaide. pp. 535Google Scholar
  64. Womersley HBS (2003) The marine benthic flora of southern Australia - part IIID Ceramiales - Delesseriaceae, Sarcomeniaceae, Rhodomelaceae. Australian Biological Resources Study and State Herbarium of South Australia, Canberra and Adelaide. pp. 533Google Scholar
  65. Zuccarello GC, West J, Rueness J (2002) Phylogeography of the cosmopolitan red alga Caulacanthus ustulatus (Caulacanthaceae, Gigartinales). Phycol Res 50:163–172CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Coastal Biology Research Group, Faculty of Sciences and Centre for Advanced Scientific Research (CICA)University of A CoruñaA CoruñaSpain
  2. 2.School of BioSciencesUniversity of MelbourneMelbourneAustralia

Personalised recommendations