Biological Invasions

, Volume 15, Issue 8, pp 1833–1846 | Cite as

Functional diversity and climate change: effects on the invasibility of macroalgal assemblages

  • F. Vaz-Pinto
  • C. Olabarria
  • I. Gestoso
  • E. Cacabelos
  • M. Incera
  • F. Arenas
Original Paper


Climate-driven and biodiversity effects on the structure and functioning of ecosystems are increasingly studied as multiple stressors, which subsequently may influence species invasions. We used a mesocosm experiment to test how increases in temperature and CO2 partial pressure (pCO2) interact with functional diversity of resident macroalgal assemblages and affect the invasion success of the non-indigenous macroalga Sargassum muticum. Early settlement of S. muticum germlings was assessed in the laboratory under common environmental conditions across three monocultures and a polyculture of functional groups of native macroalgae, which had previously grown for 3 weeks under crossed treatments of temperature and pCO2. Functional diversity was a key driver shaping early settlement of the invader, with significant identity and richness effects: higher settlement occurred in low-diversity and low-stature assemblages, even after accounting for treatment biomass. Overall, early survivorship of settled germlings responded to an interaction of temperature and pCO2 treatments, with survivorship enhanced in one treatment (high pCO2 at ambient Temperature) after 3 days, and reduced in another (ambient pCO2 at high Temperature) after 10 days, although size was enhanced in this same treatment. After 6 months in the field, legacy effects of laboratory treatments remained, with S. muticum reaching higher cover in most assemblages previously subjected to ambient pCO2, but ephemeral green algae appearing disproportionately after elevated-pCO2 treatment. These results caution that invasion outcomes may change at multiple points in the life cycle under higher-CO2, higher-temperature conditions, in addition to supporting a role for intact, functionally diverse assemblages in limiting invader colonization.


Multiple stressors Invasibility Functional diversity Sargassum muticum pCO2 Temperature 



This research was funded by the Spanish Government through the Ministry of Science and Innovation-FEDER (PROJECT CGL2009-07205), by AXA-Marine Alien and Climate Change project and by FEDER (COMPETE program) and FCT through the project CLEF (PTDC/AAC-AMB/102866/2008). FP is supported by a PhD grant from the Portuguese Foundation for Science and Technology—FCT (SFRH/BD/33393/2008). We would like to thank Rosa Viejo for help with statistical analysis as well as comments and suggestions from two anonymous referees and Jennifer Ruesink as handling editor.


  1. Åberg P (1990) Measuring size and choosing category size for a transition matrix study of the seaweed Ascophyllum nodosum. Mar Ecol Prog Ser 63:281–287CrossRefGoogle Scholar
  2. Airoldi L (2000) Effects of disturbance, life histories, and overgrowth on coexistence of algal crusts and turfs. Ecology 81:798–814CrossRefGoogle Scholar
  3. Allison G (2004) The influence of species diversity and stress intensity on community resistance and resilience. Ecol Monogr 74:117–134CrossRefGoogle Scholar
  4. Anderson MJ (2001a) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  5. Anderson MJ (2001b) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58:626–639CrossRefGoogle Scholar
  6. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Primer-E, PlymouthGoogle Scholar
  7. Arenas F, Fernández C (1998) Ecology of Sargassam muticum (Phaeophyta) on the North Coast of Spain III. Reproductive ecology. Bot Mar 41:209–216CrossRefGoogle Scholar
  8. Arenas F, Sánchez I, Hawkins SJ, Jenkins SR (2006) The invasibility of marine algal assemblages: role of functional diversity and identity. Ecology 87:2851–2861PubMedCrossRefGoogle Scholar
  9. Bertocci I, Arenas F, Matias M, Vaselli S, Araújo R, Abreu H, Pereira R, Vieira R, Sousa-Pinto I (2010) Canopy-forming species mediate the effects of disturbance on macroalgal assemblages on Portuguese rocky shores. Mar Ecol Prog Ser 414:107–116CrossRefGoogle Scholar
  10. Byers JE (2002) Impact of non-indigenous species on natives enhanced by anthropogenic alteration of selection regimes. Oikos 97:449–458CrossRefGoogle Scholar
  11. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365PubMedCrossRefGoogle Scholar
  12. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992PubMedCrossRefGoogle Scholar
  13. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, PlymouthGoogle Scholar
  14. Connell SD, Russell BD (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc R Soc Lond B Biol Sci 277:1409–1415CrossRefGoogle Scholar
  15. Crawley MJ, Brown SL, Heard MS, Edwards GR (1999) Invasion-resistance in experimental grassland communities: species richness or species identity? Ecol Lett 2:140–148CrossRefGoogle Scholar
  16. Critchley AT, Farnham WF, Morrell SL (1983) A chronology of new European sites of attachment for the invasive brown alga, Sargassum muticum, 1973–1981. J Mar Biol Ass UK 63:799–811CrossRefGoogle Scholar
  17. Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166CrossRefGoogle Scholar
  18. Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecol Lett 11:1278–1286PubMedCrossRefGoogle Scholar
  19. Dethier MN, Graham ES, Cohen S, Tear LM (1993) Visual versus random-point percent cover estimations: ‘objective’ is not always better. Mar Ecol Prog Ser 96:93–100CrossRefGoogle Scholar
  20. Deysher LE (1984) Reproductive phenology of newly introduced populations of the brown alga, Sargassum muticum (Yendo) Fensholt. Hydrobiologia 116–117:403–407CrossRefGoogle Scholar
  21. Deysher L, Norton TA (1982) Dispersal and colonization in Sargassum muticum (Yendo) Fensholt. J Exp Mar Biol Ecol 56:179–195CrossRefGoogle Scholar
  22. Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139PubMedCrossRefGoogle Scholar
  23. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonGoogle Scholar
  24. Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432CrossRefGoogle Scholar
  25. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366PubMedCrossRefGoogle Scholar
  26. Fernández C (1999) Ecology of Sargassum muticum (Phaeophyta) on the North Coast of Spain: IV. Sequence of colonization on a shore. Bot Mar 42:553–562CrossRefGoogle Scholar
  27. Fridley JD, Stachowicz J, Naeem S, Sax DF, Seabloom EW, Smith MD, Stohlgren TJ, Tilman D, Von Holle B (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17PubMedCrossRefGoogle Scholar
  28. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia M-C (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99PubMedCrossRefGoogle Scholar
  29. Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R (2008) A global map of human impact on marine ecosystems. Science 319:948–952PubMedCrossRefGoogle Scholar
  30. Harley CDG, Helmuth BST (2003) Local and regional scale effects of wave exposure, thermal stress, and absolute vs effective shore level on patterns of intertidal zonation. Limnol Oceanogr 48:1498–1508CrossRefGoogle Scholar
  31. Harley CDG, Hughes AR, Hultgren KM, Miner BG, Sorte CJB, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9:228–241PubMedCrossRefGoogle Scholar
  32. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528PubMedCrossRefGoogle Scholar
  33. Hofmann LC, Yildiz G, Hanelt D, Bischof K (2012) Physiological responses of the calcifying rhodophyte, Corallina officinalis (L.), to future CO2 levels. Mar Biol 159:783–792CrossRefGoogle Scholar
  34. Incera M, Olabarria C, Cacabelos E, César J, Troncoso JS (2011) Distribution of Sargassum muticum on the North West coast of Spain: relationships with urbanization and community diversity. Cont Shelf Res 31:488–495CrossRefGoogle Scholar
  35. IPCC (2007) Climate change 2007, the physical science basis. Summary for policymakers. intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  36. Johnson VR, Russell BD, Fabricius KE, Brownlee C, Hall-Spencer JM (2012) Temperate and tropical brown macroalgae thrive, despite decalcification, along natural CO2 gradients. Glob Change Biol. doi: 10.1111/j.1365-2486.2012.02716.x
  37. Kendrick GA (1994) Effects of propagule settlement density and adult canopy on survival of recruits of Sargassum spp. (Sargassaceae: Phaeophyta). Mar Ecol Prog Ser 103:129–140CrossRefGoogle Scholar
  38. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434PubMedCrossRefGoogle Scholar
  39. Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133–137PubMedCrossRefGoogle Scholar
  40. Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol 15:2089–2100CrossRefGoogle Scholar
  41. McDonald JH (2009) Handbook of biological statistics, 2nd edn. Sparky House Publishing, BaltimoreGoogle Scholar
  42. Monteiro C, Engelen AH, Serrão EA, Santos R (2009) Habitat differences in the timing of reproduction of the invasive alga Sargassum muticum (Phaeophyta, Sargassaceae) over tidal and lunar cycles. J Phycol 45:1–7CrossRefGoogle Scholar
  43. Morris S, Taylor AC (1983) Diurnal and seasonal variation in physico-chemical conditions within intertidal rock pools. Estuar Coast Shelf Sci 17:339–355CrossRefGoogle Scholar
  44. Norton TA (1977) The growth and development of Sargassum muticum (Yendo) Fensholt. J Exp Mar Biol Ecol 26:41–53CrossRefGoogle Scholar
  45. O’Connor MI (2009) Warming strengthens an herbivore–plant interaction. Ecology 90:388–398PubMedCrossRefGoogle Scholar
  46. Pérez-Cirera JL, Cremades J, Bárbara I (1989) Precisiones sistemáticas y sinecológicas sobre algunas algas nuevas para Galicia o para las costas atlánticas de la Península Ibérica. An Jard Bot Madr 46:35–45Google Scholar
  47. Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Biol Ecol 400:278–287CrossRefGoogle Scholar
  48. Roleda MY, Morris JN, McGraw CM, Hurd CL (2012) Ocean acidification and seaweed reproduction: increased CO2 ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae). Glob Change Biol 18:854–864CrossRefGoogle Scholar
  49. Rueness J (1989) Sargassum muticum and other introduced japanese macroalgae: biological pollution of european coasts. Mar Pollut Bull 20:173–176CrossRefGoogle Scholar
  50. Ruiz GM, Fofonoff PW, Hines AH, Grosholz ED (1999) Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnol Oceanogr 44:950–972CrossRefGoogle Scholar
  51. Russell BD, Thompson J-AI, Falkenberg LJ, Connell SD (2009) Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats. Glob Change Biol 15:2153–2162CrossRefGoogle Scholar
  52. Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DW (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774PubMedCrossRefGoogle Scholar
  53. Sanford E (1999) Regulation of keystone predation by small changes in ocean temperature. Science 283:2095–2097PubMedCrossRefGoogle Scholar
  54. Schaffelke B, Hewitt CL (2007) Impacts of introduced seaweeds. Bot Mar 50:397–417CrossRefGoogle Scholar
  55. Schaffelke B, Smith JE, Hewitt CL (2006) Introduced macroalgae—a growing concern. J Appl Phycol 18:529–541CrossRefGoogle Scholar
  56. Schiel DR, Foster MS (2006) The population biology of large brown seaweeds: ecological consequences of multiphase life histories in dynamic coastal environments. Annu Rev Ecol Evol Syst 37:343–372CrossRefGoogle Scholar
  57. Schiel DR, Lilley SA (2011) Impacts and negative feedbacks in community recovery over eight years following removal of habitat-forming macroalgae. J Exp Mar Biol Ecol 407:108–115CrossRefGoogle Scholar
  58. Sorte CJB, Williams SL, Zerebecki RA (2010) Ocean warming increases threat of invasive species in a marine fouling community. Ecology 91:2198–2204PubMedCrossRefGoogle Scholar
  59. Sorte CJB, Jones SJ, Miller LP (2011) Geographic variation in temperature tolerance as an indicator of potential population responses to climate change. J Exp Mar Biol Ecol 400:209–217CrossRefGoogle Scholar
  60. Sousa WP (1979) Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Ecol Monogr 49:227–254CrossRefGoogle Scholar
  61. Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579PubMedCrossRefGoogle Scholar
  62. Stachowicz JJ, Fried H, Osman RW, Whitlatch RB (2002a) Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83:2575–2590CrossRefGoogle Scholar
  63. Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002b) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci 99:15497–15500PubMedCrossRefGoogle Scholar
  64. Steen H (2003) Intraspecific competition in Sargassum muticum (Phaeophyceae) germlings under various density, nutrient and temperature regimes. Bot Mar 46:36–43CrossRefGoogle Scholar
  65. Steen H, Scrosati R (2004) Intraspecific competition in Fucus serratus and F. evanescens (Phaeophyceae: Fucales) germlings: effects of settlement density, nutrient concentration, and temperature. Mar Biol 144:61–70CrossRefGoogle Scholar
  66. Steneck RS, Dethier MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498CrossRefGoogle Scholar
  67. Tait LW, Schiel DR (2011) Legacy effects of canopy disturbance on ecosystem functioning in macroalgal assemblages. PLoS ONE 6:e26986PubMedCrossRefGoogle Scholar
  68. Thomsen MS, Wernberg T, Tuya F, Silliman BR (2009) Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J Phycol 45:812–819CrossRefGoogle Scholar
  69. Tilman D (1997) Community invasibility, recruitment limitation, and grassland biodiversity. Ecology 78:81–92CrossRefGoogle Scholar
  70. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance, 9th edn. Cambridge University Press, CambridgeGoogle Scholar
  71. Vadas RL Sr, Johnson S, Norton TA (1992) Recruitment and mortality of early post-settlement stages of benthic algae. Eur J Phycol 27:331–351CrossRefGoogle Scholar
  72. White LF, Shurin JB (2007) Diversity effects on invasion vary with life history stage in marine macroalgae. Oikos 116:1193–1203CrossRefGoogle Scholar
  73. Widdicombe S, Spicer JI (2008) Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us? J Exp Mar Biol Ecol 366:187–197CrossRefGoogle Scholar
  74. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Ann Rev Ecol Evol Syst 38:327–359CrossRefGoogle Scholar
  75. Yendo K (1907) The Fucaceae of Japan. J Coll Sci Imp Univ Tokyo 21:1–174Google Scholar
  76. Zeebe RE, Wolf-Gladrow D (2001) CO2 in seawater: equilibrium, kinetics, isotopes, vol 65. Elsevier, New YorkGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • F. Vaz-Pinto
    • 1
    • 2
  • C. Olabarria
    • 3
  • I. Gestoso
    • 3
  • E. Cacabelos
    • 1
    • 5
  • M. Incera
    • 4
  • F. Arenas
    • 1
  1. 1.Laboratory of Coastal Biodiversity, CIIMAR, Centro Interdisciplinar de Investigação Marinha e AmbientalUniversidade do PortoPortoPortugal
  2. 2.ICBAS, Instituto de Ciências Biomédicas Abel SalazarUniversidade do PortoPortoPortugal
  3. 3.Departamento de Ecología y Biología Animal, Facultad de Ciencias del MarUniversidad de VigoVigoSpain
  4. 4.Centro Tecnológico del Mar, Fundación CETMARVigoSpain
  5. 5.Centro Tecnológico del Mar, Fundación CETMARVigoSpain

Personalised recommendations