Biological Invasions

, Volume 19, Issue 2, pp 537–547 | Cite as

Species, community, and ecosystem-level responses following the invasion of the red alga Dasysiphonia japonica to the western North Atlantic Ocean

  • Christine Ramsay-Newton
  • Annick Drouin
  • A. Randall Hughes
  • Matthew E. S. Bracken
Original Paper


Species invasions have been increasing in frequency worldwide, yet critical gaps remain in our understanding of how invaders affect community structure and ecosystem functioning, particularly during the initial stages of invasion. Even less is known about changes in the invader that may take place immediately following an invasion. This study examined the recent invasion of the red macroalga Dasysiphonia (formerly, Heterosiphonia) japonica to the western North Atlantic Ocean with the aim of filling in gaps in our understanding of the impacts that invasive seaweeds have at the species, community and ecosystem levels immediately following their establishment. Within 5 years of invasion, community composition had changed and biodiversity had decreased to nearly half of pre-invasion levels. In addition, the relative proportion of Dasysiphonia decreased by 35% over our four-year study from initially high levels shortly after establishment. We found evidence that functional traits of this initially aggressive invader changed over time, as it ultimately became a less aggressive, co-inhabiting member of the local algal community, particularly with respect to nutrient uptake and relative abundances, although native diversity remained low relative to pre-invasion levels. Using these realistic changes in community structure, including decreases in biodiversity, we also showed that nutrient uptake of algal assemblages changed over time, suggesting changes in the functional characteristics of invaded communities, with implications for ecosystem-level processes such as nutrient fluxes. This study provides rare empirical evidence about the successional stages occurring at the individual, community, and ecosystem levels during the first 5 years of an invasion.


Invasive species Biodiversity Ecosystem functioning Nutrient uptake Dasysiphonia japonica 



We thank N. Low, V. Perini, I. Rosenfield, and V. Selesnick for diving and laboratory assistance. K. Benes provided additional laboratory assistance. We would also like to acknowledge Northeastern University’s Marine Science Center Diving Program and Diving Safety Officers: L. Bentley-Magee, S. Genovese and T. Lyman. Research described in this publication was supported by the Massachusetts Institute of Technology Sea Grant College Program, under National Oceanic and Atmospheric Administration Grant Number NA14OAR4170077, MIT SG Project Number 2014-R/RCM-37; the National Science Foundation (Award OCE-0963010); Woods Hole Sea Grant (Subaward A100923) to M.E.S.B and C. S. Thornber; and the Fonds québécois de la recherche sur la nature et les technologies (FQRNT). This is contribution number 346 from the Marine Science Center of Northeastern University.

Supplementary material

10530_2016_1323_MOESM1_ESM.doc (72 kb)
Supplementary material 1 (DOC 72 kb)


  1. Barr NG, Kloeppel A, Rees AV, Scherer C, Taylor RB, Wenzel A (2008) Wave surge increases rates of growth and nutrient uptake in the green seaweed Ulva pertusa maintained at low bulk flow velocities. Aquat Biol 3:179–186CrossRefGoogle Scholar
  2. Bjaerke MR, Rueness J (2004) Effects of temperature and salinity on growth, reproduction and survival in the introduced red alga Heterosiphonia japonica (Ceramiales, Rhodophyta). Bot Mar 47:373–380CrossRefGoogle Scholar
  3. Bracken MES, Williams SL (2013) Realistic changes in seaweed biodiversity affect multiple ecosystem functions on a rocky shore. Ecology 94:1944–1954CrossRefPubMedGoogle Scholar
  4. Bracken MES, Friberg SE, Gonzalez-Dorantes CA, Williams SL (2008) Functional consequences of realistic biodiversity changes in a marine ecosystem. Proc Natl Acad Sci USA 105:924–928CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bracken MES, Jones E, Williams SL (2011) Herbivores, tidal elevation, and species richness simultaneously mediate nitrate uptake by seaweed assemblages. Ecology 92:1083–1093CrossRefPubMedGoogle Scholar
  6. Butchart SHM, Walpole M, Collen B, van Strien A, Scharlemann JPW, Almond REA, Baillie JEM, Bomhard B, Brown C, Bruno JF, Carpenter KE, Carr GM, Chanson J, Chenery AM, Csirke J, Davidson NC, Dentener F, Foster M, Galli A, Galloway JN, Genovesi P, Gregory RD, Hockings M, Kapos V, Lamarque J-F, Leverington F, Loh J, McGeoch MA, McRae L, Minasyan A, Morcillo MH, Oldfield TEE, Pauly D, Quader S, Revenga C, Sauer JR, Skolnik B, Spear D, Stanwell-Smith D, Stuart SN, Symes A, Tiemey M, Tyrrell TD, Vie J-C, Watson R (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168CrossRefPubMedGoogle Scholar
  7. Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis. Ecol Lett 14:419–431CrossRefPubMedGoogle Scholar
  8. Davidson AD, Campbell ML, Hewitt CL, Schaffelke B (2015) Assessing the impacts of nonindigenous marine macroalgae: an update of current knowledge. Bot Mar 58:55–79Google Scholar
  9. Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80CrossRefGoogle Scholar
  10. Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27CrossRefGoogle Scholar
  11. Hayes KR, Barry SC (2008) Are there any consistent predictors of invasion success? Biol Invasions 10:483–506CrossRefGoogle Scholar
  12. Jones E, Thornber CS (2010) Effects of habitat-modifying invasive macroalgae on epiphytic algal communities. Mar Ecol Prog Ser 400:87–100CrossRefGoogle Scholar
  13. Katsanevakis S, Wallentinus I, Zenetos A, Leppakoski E, Cinar ME, Ozturk B, Grabowski M, Golam D, Cardoso AC (2014) Impacts of invasive alien marine species on ecosystem services and biodiversity: a pan-European review. Aquat Invasions 9:391–423CrossRefGoogle Scholar
  14. Loreau M (1998) Biodiversity and ecosystem functioning: a mechanistic model. Proc Natl Acad Sci USA 95:5632–5636CrossRefPubMedPubMedCentralGoogle Scholar
  15. Low NHN, Drouin A, Marks CJ, Bracken MES (2015) Invader traits and community context contribute to the recent invasion success of the macroalga Heterosiphonia japonica on New England rocky reefs. Biol Invasions 17:257–271CrossRefGoogle Scholar
  16. 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
  17. Naeem S, Duffy JE, Zavaleta E (2012) The functions of biological diversity in an age of extinction. Science 336:1401–1406CrossRefPubMedGoogle Scholar
  18. Newton C, Bracken MES, McConville M, Rodrigue K, Thornber CS (2013) Invasion of the red seaweed Heterosiphonia japonica spans biogeographic provinces in the Western North Atlantic Ocean. PLOS ONE 8:e62261CrossRefPubMedPubMedCentralGoogle Scholar
  19. Ojaveer H, Galil BS, Minchin D, Olenin S, Amorim A, Canning-Clode J, Chainho P, Copp GH, Collasch S, Jelmert A, Lehtiniemi M, McKenzie C, Mikus J, Miossec L, Occhipinti-Ambrogi A, Pecarevic M, Pederson JR, Quilez-Badia G, Wijsman JWM, Zenetos A (2014) Ten recommendations for advancing the assessment and management of non-indigenous species in marine ecosystems. Mar Policy 44:160–165CrossRefGoogle Scholar
  20. Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, Williamson MH, Von Holle B, Moyle PB, Byers JE, Goldwasser L (1999) Impact: toward a framework for understanding the ecological effects of invaders. Biol Invasions 1:3–19CrossRefGoogle Scholar
  21. Perini V, Bracken MES (2014) Nitrogen availability limits phosphorus uptake in an intertidal macroalga. Oecologia 175:667–676CrossRefPubMedGoogle Scholar
  22. Power LD, Cardinale BJ (2009) Species richness enhances both algal biomass and rates of oxygen production in aquatic microcosms. Oikos 118:1703–1711CrossRefGoogle Scholar
  23. Savoie AM, Saunders GW (2013) First record of the invasive red alga Heterosiphonia japonica (Ceramiales, Rhodophyta) in Canada. BioInvasion Rec 2:27–32CrossRefGoogle Scholar
  24. Schaffelke B, Hewitt CL (2007) Impacts of introduced seaweeds. Bot Mar 50:397–417CrossRefGoogle Scholar
  25. Schneider CW (2010) Report of a new invasive alga in the Atlantic United States: “Heterosiphonia” japonica in Rhode Island. J Phycol 46:653–657CrossRefGoogle Scholar
  26. Simberloff D (2011) How common are invasion-induced ecosystem impacts? Biol Invasions 13:1255–1268CrossRefGoogle Scholar
  27. Simberloff D, Gibbons L (2004) Now you see them, now you don’t!—population crashes of established introduced species. Biol Invasions 6:161–172CrossRefGoogle Scholar
  28. Sousa R, Morais P, Dias E, Antunes C (2011) Biological invasions and ecosystem functioning: time to merge. Biol Invasions 2011:1055–1058CrossRefGoogle Scholar
  29. Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci USA 99:15497–15500CrossRefPubMedPubMedCentralGoogle Scholar
  30. Strayer DL (2012) Eight questions about invasions and ecosystem functioning. Ecol Lett 15:1199–1210CrossRefPubMedGoogle Scholar
  31. Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651CrossRefPubMedGoogle Scholar
  32. Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273CrossRefPubMedGoogle Scholar
  33. Thomsen MS, Wernberg T, Tuya F, Silliman BR (2009) Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J Phycol 45:812–918CrossRefPubMedGoogle Scholar
  34. Thomsen MS, Wernberg T, Engelen AH, Tuya F, Vanderklift MA, Holmer M, McGlathery KJ, Arenas F, Kotta J, Silliman BR (2012) A meta-analysis of seaweed impacts on seagrasses: generalities and knowledge gaps. PlOS ONE: Biol 7:e28595CrossRefGoogle Scholar
  35. Vila M, Espinar JL, Hejda M, Hulme PE, Jarosik V, Maron JL, Pergl J, Schaffner U, Sun Y, Pysek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708CrossRefPubMedGoogle Scholar
  36. 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

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Christine Ramsay-Newton
    • 1
    • 2
  • Annick Drouin
    • 3
  • A. Randall Hughes
    • 2
  • Matthew E. S. Bracken
    • 4
  1. 1.Department of Life SciencesMitchell CollegeNew LondonUSA
  2. 2.Department of Ecology, Evolution, and Marine Biology, Marine Science CenterNortheastern UniversityNahantUSA
  3. 3.Institut Maurice LamontagneFisheries and Océans CanadaQuébecCanada
  4. 4.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaIrvineUSA

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