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The regime of climate-related disturbance and nutrient enrichment modulate macroalgal invasions in rockpools

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Abstract

Patterns of invasion by the seaweeds Grateloupia turuturu Yamada and Sargassum muticum (Yendo) Fensholt under crossed combinations of the regime (mean intensity and temporal variability) of climate-related mechanical disturbance and constant nutrient enrichment were experimentally examined in rockpools in north Portugal. The cover of both species was larger under high compared to low intensity of disturbance, but this effect was enhanced by events more heterogeneously distributed over a period of 19 months. The invasion by G. turuturu was also larger in enriched pools, but only when disturbance was applied at high intensity. The richness of native taxa was increased by high intensity events of disturbance evenly distributed over time and by low intensity events heterogeneously distributed, while no differences were documented for other treatments. Temporal variability of disturbance and nutrients interactively affected the total cover of native taxa and the availability of bare rock in different directions. Enriched conditions increased the space occupancy by natives and reduced substratum availability only when associated to heterogeneous events of disturbance. At the same time, relatively more variable disturbances caused a reduced cover by native taxa and an increased availability of free space, but only under natural nutrient levels. Present findings contribute to understand the conditions that would be more likely to facilitate the spread of G. turuturu and S. muticum under current and predicted scenarios of compounded environmental changes and in relation to traits of recipient systems that are considered relevant for the success of invasions, including the native richness and the degree of usage of resources, i.e. primarily space.

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References

  • Airoldi L, Beck MW (2007) Loss, status and trends for coastal marine habitats of Europe. Oceanogr Mar Biol 45:345–405

    Google Scholar 

  • Allen MR, Ingram WJ (2002) Constraints on future changes in climate and the hydrologic cycle. Nature 419:224

    CAS  PubMed  Google Scholar 

  • Allen MR, Stott PA, Mitchell JFB, Schnur R, Delworth TL (2000) Quantifying the uncertainty in forecast of anthropogenic climate change. Nature 407:617–620

    CAS  PubMed  Google Scholar 

  • Altman S, Whitlatch RB (2007) Effects of small-scale disturbance on invasion success in marine communities. J Exp Mar Biol Ecol 342:15–29

    Google Scholar 

  • Ambasht RS, Ambasht NK (2003) Modern trends in applied terrestrial ecology. Kluwer Academic, New York

    Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Araújo R, Sousa-Pinto I, Bárbara I, Quintino V (2006) Macroalgal communities of intertidal rock pools in the northwest coast of Portugal. Acta Oecol 30:192–202

    Google Scholar 

  • Araújo R, Violante J, Pereira R, Abreu H, Arenas F, Sousa-Pinto I (2011) Distribution and population dynamics of the introduced seaweed Grateloupia turuturu (Halymeniaceae, Rhodophyta) along the Portuguese coast. Phycologia 50:392–402

    Google Scholar 

  • Arenas F, Sánchez I, Hawkins SJ, Jenkins SR (2006) The invasibility of marine algal assemblages: role of functional diversity and identity. Ecology 87:2851–2861

    PubMed  Google Scholar 

  • Benedetti-Cecchi L (2000) Predicting direct and indirect effects during succession in a mid-littoral rocky shore assemblage. Ecol Monogr 70(1):45–72

  • Benedetti-Cecchi L (2003) The importance of the variance around the mean effect size of ecological processes. Ecology 84:2335–2346

    Google Scholar 

  • Benedetti-Cecchi L, Cinelli F (1994) Recovery of patches in an assemblage of geniculate coralline algae: variability at different successional stages. J Exp Mar Biol Ecol 110:9–18

    Google Scholar 

  • Benedetti-Cecchi L, Cinelli F (1996) Patterns of disturbance and recovery in littoral rock pools: non-hierarchical competition and spatial variability in secondary succession. Mar Ecol Prog Ser 135:145–161

    Google Scholar 

  • Benedetti-Cecchi L, Bertocci I, Vaselli S, Maggi E (2006) Temporal variance reverses the impact of high mean intensity of stress in climate change experiments. Ecology 87:2489–2499

    PubMed  Google Scholar 

  • Benestad RE (2003) What can present climate models tell us about climate change? Clim Change 59:311–331

    Google Scholar 

  • Bertocci I, Araújo R, Incera M, Arenas F, Pereira R, Abreu H, Larsen K, Sousa-Pinto I (2012) Benthic assemblages of rock pools in northern Portugal: seasonal and between-pool variability. Sci Mar 76(4):781–789

  • Bertocci I, Maggi E, Vaselli S, Benedetti-Cecchi L (2005) Contrasting effects of mean intensity and temporal variation of disturbance on a rocky seashore. Ecology 86:2061–2067

    Google Scholar 

  • Bishop MJ, Kelaher BP (2007) Impacts of detrital enrichment on estuarine assemblages: disentangling effects of frequency and intensity of disturbance. Mar Ecol Prog Ser 341:25–36

    Google Scholar 

  • Bossenbroek JM, Kraft CE, Nekola JC (2001) Prediction of long-distance dispersal using gravity-models: zebra mussel invasion of inland lakes. Ecol Appl 11:1778–1788

    Google Scholar 

  • Britton-Simmons KH (2004) Direct and indirect effects of the introduced alga Sargassum muticum on benthic, subtidal communities of Washington State, USA. Mar Ecol Prog Ser 277:61–78

    Google Scholar 

  • Britton-Simmons KH, Abbott KC (2008) Short- and long-term effects of disturbance and propagule pressure on a biological invasion. J Ecol 96:68–77

    Google Scholar 

  • Buckley LB, Kingsolver JG (2012) The demographic impacts of shifts in climate means and extremes on alpine butterflies. Funct Ecol 26:969–977

    Google Scholar 

  • Bulleri F, Balata D, Bertocci I, Tamburello L, Benedetti-Cecchi L (2010) The seaweed Caulerpa racemosa on Mediterranean rocky reefs: from passenger to driver of ecological change. Ecology 91:2205–2212

    PubMed  Google Scholar 

  • Burke MJW, Grime JP (1996) An experimental study of plant community invasibility. Ecology 77:776–790

    Google Scholar 

  • Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139

    PubMed  Google Scholar 

  • Byers JE (2002) Impact of non-indigenous species on natives enhanced by anthropogenic alteration of selection regimes. Oikos 97:449–458

    Google Scholar 

  • Cabioc’h J, Castricfey A, Lhaddyhalos M, Rio A (1997) Grateloupia doryphora and Grateloupia filicina var luxurians (Rhodophyta, Halymeniaceae) from the coasts of Brittany (France). Cryptog Algol 18:117–137

    Google Scholar 

  • Cacabelos E, Olabarria C, Viejo RM, Rubal M, Veiga P, Incera M, Gestoso I, Vaz-Pinto F, Mejia A, Engelen AH, Arenas F (2013) Invasion of Sargassum muticum in intertidal rockpools: patterns along the Atlantic Iberian Peninsula. Mar Environ Res 90:18–26

    CAS  PubMed  Google Scholar 

  • Chapman ARO (1990) Effects of grazing, canopy cover and substratum type on the abundances of common species of seaweeds inhabiting littoral fringe tide pools. Bot Mar 33:319–326

  • Connell JH (1978) Diversity in tropical rain forests and coral reefs—high diversity of trees and corals is maintained only in a nonequilibrium state. Science 199:1302–1310

    CAS  PubMed  Google Scholar 

  • 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 277:1409–1415

    Google Scholar 

  • Costa-Dias S, Sousa R, Antunes C (2010) Ecological quality assessment of the lower Lima estuary. Mar Poll Bull 61:234–239

    CAS  Google Scholar 

  • Costanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon B, Limburg K, Naeem S, O’Neill RV, Paruelo J, Raskin RG, Sutton P, van den Belt M (1997) The value of the world’s ecosystem services and natural capital. Nature 387:253–260

    CAS  Google Scholar 

  • Crawley MJ, Brown SL, Heard MS, Edwards GR (1999) Invasion-resistance in experimental grassland communities: species richness or species identity? Ecol Lett 2:140–148

    Google Scholar 

  • 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 Assoc UK 63:799–811

    Google Scholar 

  • D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle. Annu Rev Ecol Syst 23:63–87

    Google Scholar 

  • D’Antonio CM, Dudley TL, Mack M (1999) Disturbance and biological invasions: direct effects and feedbacks. In: Walker LR (ed) Ecosystems of the World 16: ecosystems of disturbed ground. Elsevier, Amsterdam, pp 413–452

    Google Scholar 

  • D’Archino R, Nelson WA, Zuccarello GC (2007) Invasive marine red alga introduced to New Zealand waters: first record of Grateloupia turuturu (Halymeniaceae, Rhodophyta). N Z J Mar Freshw Res 40:599–604

    Google Scholar 

  • Dalsgaard T (2003) Benthic primary production and nutrient cycling in sediments with benthic microalgae and transient accumulation of macroalgae. Limnol Oceanogr 48:2138–2150

    CAS  Google Scholar 

  • Darling ES, Côté IM (2008) Quantifying the evidence for ecological synergies. Ecol Lett 11:1278–1286

    PubMed  Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. J Ecol 88:528–534

    Google Scholar 

  • Dayton PK, Currie V, Gerrodette T, Keller BD, Rosenthal R, Ven Tresca D (1984) Patch dynamics and stability of some California kelp communities. Ecol Monogr 54:253–289

    Google Scholar 

  • 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 96:93–100

  • Dias JMA, Gonzalez R, Garcia C, Diaz-del-Rio V (2002) Sediment distribution patterns on the Galicia-Minho continental shelf. Prog Oceanogr 52:215–231

    Google Scholar 

  • Diez JM, D’Antonio CM, Dukes JS et al (2012) Will extreme climatic events facilitate biological invasions? Front Ecol Environ 10:249–257

    Google Scholar 

  • Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139

    PubMed  Google Scholar 

  • Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Sci 289:2068–2074

  • Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London, UK

    Google Scholar 

  • Engelen AH, Åberg P, Olsen JL, Stam WT, Breeman AM (2005) Effects of wave exposure and depth on biomass, density and fertility of the fucoid seaweed Sargassum polyceratium (Phaeophyta, Sargassaceae). Eur J Phycol 40:149–158

    Google Scholar 

  • 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 305:362–366

    CAS  PubMed  Google Scholar 

  • French PW (1997) Coastal and estuarine management. Routledge, London

    Google Scholar 

  • Gray JS (1997) Marine biodiversity: patterns, threats and conservation needs. Biodiv Conserv 6:153–175

    Google Scholar 

  • Grevstad FS (1999) Experimental invasions using biological control introductions: the influence of release size on the chance of population establishment. Biol Inv 1:313–323

    Google Scholar 

  • Gross KL, Mittelbach GG, Reynolds HL (2005) Grassland invasibility and diversity: responses to nutrients, seed input, and disturbance. Ecology 86:476–486

    Google Scholar 

  • Gutschick VP, BassiriRad H (2003) Extreme events as shaping physiology, ecology, and evolution of plants: toward a unified definition and evaluation of their consequences. New Phytol 160:21–42

    Google Scholar 

  • Halpern BS, Selkoe KA, Micheli F, Kappel CV (2007) Evaluating and ranking the vulnerability of global marine ecosystems to anthropogenic threats. Conserv Biol 21:1301–1315

    PubMed  Google Scholar 

  • Halpern BS, Walbridge S, Selkoe KA et al (2008) A global map of human impact on marine ecosystems. Science 319:948–952

    CAS  PubMed  Google Scholar 

  • 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 9:228–241

    PubMed  Google Scholar 

  • Harlin MM, Villalard-Bohnsack MV (2001) Seasonal dynamics and recruitment strategies of the invasive seaweed Grateloupia doryphora (Halymeniaceae, Rhodophyta) in Naragansett Bay and Rhode Island Sound, Rhode Island, USA. Phycologia 40:468–474

    Google Scholar 

  • Higgins SI, Richardson DM (1998) Pine invasions in the southern hemisphere: modelling interactions between organism, environment and disturbance. Plant Ecol 135:79–93

    Google Scholar 

  • Hill SJ, Tung PJ, Leishman MR (2005) Relationships between anthropogenic disturbance, soil properties and plant invasion in endangered Cumberland plain woodland, Australia. Aust Ecol 30:775–788

    Google Scholar 

  • Hillebrand H (2003) Opposing effects of grazing and nutrients on diversity. Oikos 100:592–600

    Google Scholar 

  • Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337

    Google Scholar 

  • Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328:1523–1528

    CAS  PubMed  Google Scholar 

  • Huston M (1994) Biological diversity. Cambridge University Press, Cambridge, UK

  • Incera M, Olabarria C, Troncoso JS, López J (2009) Response of the invader Sargassum muticum to variability in nutrient supply. Mar Ecol Prog Ser 377:91–101

    Google Scholar 

  • Incera M, Bertocci I, Benedetti-Cecchi L (2010) Effects of mean intensity and temporal variability of disturbance on the invasion of Caulerpa racemosa var. cylindracea (Caulerpales) in rock pools. Biol Inv 12:501–514

    Google Scholar 

  • 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 31:488–495

    Google Scholar 

  • Janiak DS, Whitlatch RB (2012) Epifaunal and algal assemblages associated with the native Chondrus crispus (Stackhouse) and the non-native Grateloupia turuturu (Yamada) in eastern Long Island Sound. J Exp Mar Biol Ecol 413:38–44

    Google Scholar 

  • Katz RW, Brown BG (1992) Extreme events in a changing climate—variability is more important than averages. Clim Change 21:289–302

    Google Scholar 

  • Keough MJ (1984) Effects of patch size on the abundance of sessile marine invertebrates. Ecology 65:423–437

    Google Scholar 

  • Kneitel JM, Perrault D (2006) Disturbance-induced changes in community composition increase species invasion success. Commun Ecol 7:245–252

    Google Scholar 

  • Lake JC, Leishman MR (2004) Invasion success of exotic plants in natural ecosystems: the role of disturbance, plant attributes and freedom from herbivores. Biol Conserv 117:215–226

    Google Scholar 

  • Larson DL (2003) Native weeds and exotic plants: relationships to disturbance in mixed-grass prairie. Plant Ecol 169:317–333

    Google Scholar 

  • Leishman MR, Thomson VP (2005) Experimental evidence for the effects of additional water, nutrients and physical disturbance on invasive plants in low fertility Hawkesbury Sandstone soils, Sydney. Aust J Ecol 93:38–49

    Google Scholar 

  • Lemos RT, Pires HE (2004) The upwelling regime off the west Portuguese coast, 1941–2000. Int J Climatol 24:511–524

    Google Scholar 

  • Levine J, Adler P, Yelenik S (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989

    Google Scholar 

  • Lima FP, Queiroz N, Ribeiro PA, Hawkins SJ, Santos AM (2006) Geographic expansion of a marine gastropod, Patella rustica Linnaeus, 1758, and its relation with unusual climatic events. J Biogeogr 33:812–822

    Google Scholar 

  • Liu F, Pang SJ (2010) Stress tolerance and antioxidant enzymatic activities in the metabolism of the reactive oxygen species in two intertidal red algae Grateloupia turuturu and Palmaria palmata. J Exp Mar Biol Ecol 382:82–87

    CAS  Google Scholar 

  • Lonsdale WM (1999) Global patterns of plant invasions and the concept of invasibility. Ecology 80:1522–1536

    Google Scholar 

  • Loreau M (2000) Biodiversity and ecosystem functioning: recent theoretical advances. Oikos 91:3–17

    Google Scholar 

  • Maestre FT, Salguero-Gómez R, Quero JL (2012) It is getting hotter in here: determining and projecting the impacts of global environmental change on drylands. Phil Trans R Soc B 367:3062–3075

    PubMed Central  PubMed  Google Scholar 

  • Magalhães CM, Joye SB, Moreira RM, Wiebe WJ, Bordalo AA (2005) Effect of salinity and inorganic nitrogen concentrations on nitrification and denitrification rates in intertidal sediments and rocky biofilms of the Douro River estuary, Portugal. Water Res 39:1783–1794

    PubMed  Google Scholar 

  • Maggi E, Bulleri F, Bertocci I, Benedetti-Cecchi L (2012) Competitive ability of macroalgal canopies overwhelms the effects of variable regimes of disturbance. Mar Ecol Prog Ser 465:99–109

    Google Scholar 

  • Martin S, Gattuso J-P (2009) Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob Change Biol 15:2089–2100

    Google Scholar 

  • Molinos JG, Donohue I (2011) Temporal variability within disturbance events regulates their effects on natural communities. Oecologia 166:795–806

    Google Scholar 

  • Moore JL, Mouquet N, Lawton JH, Loreau M (2001) Coexistence, saturation and invasion resistance in simulated plant assemblages. Oikos 94:303–314

    Google Scholar 

  • Morel FMM (1987) Kinetics of nutrient uptake and growth in phytoplankton. J Phycol 23:137–150

    CAS  Google Scholar 

  • Mouquet N, Moore JL, Loreau M (2002) Plant species richness and community productivity: why the mechanism that promotes coexistence matters. Ecol Lett 5:56–66

    Google Scholar 

  • Moyle PB, Light T (1996) Fish invasions in California: do abiotic factors determine success? Ecology 77:1666–1670

    Google Scholar 

  • Muller RA, Stone GW (2001) A climatology of tropical storm and hurricane strikes to enhance vulnerability prediction for the southeast U.S. coast. J Coast Res 17:949–956

    Google Scholar 

  • Naeem S, Knops J, Tilman D, Howe K, Kennedy T, Gale S (2000) Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors. Oikos 91:97–108

    Google Scholar 

  • Nielsen KJ (2001) Bottom-up and top-down forces in tide pools: test of a food chain model in an intertidal community. Ecol Monogr 71:187–217

    Google Scholar 

  • Olabarria C, Arenas F, Viejo RM, Gestoso I, Vaz-Pinto F, Incera M, Rubal M, Cacabelos E, Veiga P, Sobrino C (2013) Response of macroalgal assemblages from rockpools to climate change: effects of persistent increase in temperature and CO2. Oikos 122:1065–1079

    CAS  Google Scholar 

  • Paine RT, Tegner MJ, Johnson EA (1998) Compounded perturbations yield ecological surprises. Ecosystems 1:535–545

    Google Scholar 

  • Pauly D, Watson R, Adler J (2005) Global trends in world fisheries: impacts on marine ecosystems and food security. Philos T R Soc Lon B 360:5–12

    Google Scholar 

  • Pausas JG, Lloret F, Vilà M (2006) Simulating the effects of different disturbance regimes on Cortaderia selloana invasion. Biol Conserv 128:128–135

    Google Scholar 

  • 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 46:35–45

    Google Scholar 

  • Pincebourde S, Sanford E, Casas J, Helmuth B (2012) Temporal coincidence of environmental stress events modulates predation rates. Ecol Lett 15:680–688

    PubMed  Google Scholar 

  • Porzio L, Buia MC, Hall-Spencer JM (2011) Effects of ocean acidification on macroalgal communities. J Exp Mar Biol Ecol 400:278–287

    CAS  Google Scholar 

  • Prieur-Richard A, Lavorel S (2000) Invasions: the perspective of diverse plant communities. Aust Ecol 25:1–7

    Google Scholar 

  • Prieur-Richard A-H, Lavorel S, Grigulis K, dos Santos A (2000) Plant community diversity and invasibility by exotics: invasion of Mediterranean old fields by Conyza bonariensis and Conyza canadensis. Ecol Lett 3:412–422

    Google Scholar 

  • Rubal M, Veiga P, Vieira R, Sousa-Pinto I (2011) Seasonal patterns of tidepool macroalgal assemblages in the North of Portugal. Consistence between species and functional group approaches. J Sea Res 66:187–194

    Google Scholar 

  • Ruiz GM, Fofonoff PW, Hines AH, Grosholz ED (1999) Nonindigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnol Oceanogr 44:950–972

    Google Scholar 

  • 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 15:2153–2162

    Google Scholar 

  • Sala OE, Chapin FS, Armesto JJ et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774

    CAS  PubMed  Google Scholar 

  • Sánchez I, Fernández C (2006) Resource availability and invasibility in an intertidal macroalgal assemblage. Mar Ecol Prog Ser 313:85–94

    Google Scholar 

  • Saunders GW, Withall RD (2006) Collections of the invasive species Grateloupia turuturu (Halymeniales, Rhodophyta) from Tasmania, Australia. Phycologia 45:711–714

    Google Scholar 

  • Schaffelke B, Hewitt CL (2007) Impacts of introduced seaweeds. Bot Mar 50:397–417

  • Schaffelke B, Smith JE, Hewitt CL (2006) Introduced macroalgae—a growing concern. J Appl Phycol 18:529–541

    Google Scholar 

  • Shumway SW, Bertness MD (1994) Patch size effects on marsh plant secondary succession mechanisms. Ecology 75:564–568

    Google Scholar 

  • Sigmon DE, Cahoon LB (1997) Comparative effects of benthic microalgae and phytoplankton on dissolved silica fluxes. Aquat Microb Ecol 13:275–284

    Google Scholar 

  • Sorte CJB, Williams SL, Zerebecki RA (2010) Ocean warming increases threat of invasive species in a marine fouling community. Ecology 91:2198–2204

    PubMed  Google Scholar 

  • Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579

    CAS  PubMed  Google Scholar 

  • Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002a) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci USA 99:15497–15500

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stachowicz JJ, Fried H, Osman RW, Whitlatch RB (2002b) Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83:2575–2590

    Google Scholar 

  • Steen H (2003) Intraspecific competition in Sargassum muticum (Phaeophyceae) germlings under various density, nutrient and temperature regimes. Bot Mar 46:36–43

  • Stuart-Smith RD, Barrett N, Stevenson DG, Graham JE (2010) Stability in temperate reef communities over a decadal time scale despite concurrent ocean warming. Glob Change Biol 16:122–134

    Google Scholar 

  • Thomsen MS, Wernberg T, Tuya F, Silliman BR (2009) Evidence for impacts of nonindigenous macroalgae: a meta-analysis of experimental field studies. J Phycol 45:812–819

    Google Scholar 

  • Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Underwood AJ (1998) Grazing and disturbance: an experimental analysis of patchiness in recovery from a severe storm by the intertidal alga Hormosira banksii on rocky shores in New South Wales. J Exp Mar Biol Ecol 231:291–306

    Google Scholar 

  • Vaselli S, Bertocci I, Maggi E, Benedetti-Cecchi L (2008) Effects of mean intensity and temporal variance of sediment scouring events on assemblages of rocky shores. Mar Ecol Prog Ser 364:57–66

    Google Scholar 

  • Vaz-Pinto F, Olabarria C, Arenas F (2012) Propagule pressure and functional diversity: interactive effects on a macroalgal invasion process. Mar Ecol Prog Ser 471:51–60

    Google Scholar 

  • Vaz-Pinto F, Olabarria C, Gestoso I, Cacabelos E, Incera M, Arenas F (2013a) Functional diversity and climate change: effects on the invasibility of macroalgal assemblages. Biol Inv 15:1833–1846

    Google Scholar 

  • Vaz-Pinto F, Olabarria C, Arenas F (2013b) Role of top-down and bottom-up forces on the invasibility of intertidal macroalgal assemblages. J Sea Res 76:178–186

    Google Scholar 

  • Villalard-Bohnsack M, Harlin MM (1997) The appearance of Grateloupia doryphora (Halymeniaceae, Rhodophyta) on the northeast coast of North America. Phycologia 36:324–328

    Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth’s ecosystems. Science 277:494–499

    CAS  Google Scholar 

  • Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob Change Biol 18:1491–1498

    Google Scholar 

  • 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 366:187–197

    Google Scholar 

  • Wilcove DS, Rothstein D, Bubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. Bioscience 48:607–615

    Google Scholar 

  • Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359

    Google Scholar 

  • Worm B, Lotze HK, Sommer U (2000) Coastal food web structure, carbon storage, and nitrogen retention regulated by consumer pressure and nutrient loading. Limnol Oceanogr 45:339–349

    CAS  Google Scholar 

  • Worm B, Barbier EB, Beaumont N et al (2006) Impacts of biodiversity loss on ocean ecosystem services. Science 314:787–790

    CAS  PubMed  Google Scholar 

  • Zavaleta ES, Shaw MR, Chiariello NR, Mooney HA, Field CB (2003) Additive effects of simulated climate changes, elevated CO2, and nitrogen deposition on grassland diversity. Proc Natl Acad Sci USA 100:7650–7654

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zimmerman JK, Comita LS, Thompson J, Uriarte M, Brokaw N (2010) Patch dynamics and community metastability of a subtropical forest: compound effects of natural disturbance and human land use. Landsc Ecol 25:1099–1111

    Google Scholar 

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Acknowledgments

This study was funded by the European Regional Development Fund (ERDF) through the programme POFC-COMPETE, ‘Quadro de Referência Estratégico Nacional (QREN), and the Portuguese Fundação para a Ciência e a Tecnologia (FCT) through the project “RAP—Responses to Anthropogenic Perturbations: climatic and nutrient effects on rock pool assemblages” (PTDC/MAR/111223/2009) and national funds (PEst-C/MAR/LA0015/2011). I. Bertocci was supported by FCT within Programa Ciência 2008—Fundo Social Europeu. E. Cacabelos, G. Carvalho, J. Franco and A. Plicanti assisted with field work. The manuscript benefited from valuable comments by José L. Espinar and an anonymous reviewer.

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Correspondence to Iacopo Bertocci.

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Bertocci, I., Domínguez Godino, J., Freitas, C. et al. The regime of climate-related disturbance and nutrient enrichment modulate macroalgal invasions in rockpools. Biol Invasions 17, 133–147 (2015). https://doi.org/10.1007/s10530-014-0711-4

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  • DOI: https://doi.org/10.1007/s10530-014-0711-4

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