Abstract

Exotic species are a growing global ecological threat; however, their overall effects are insufficiently understood. While some exotic species are implicated in many species extinctions, others can provide benefits to the recipient communities. Here, we performed a meta-analysis to quantify and synthesize the ecological effects of 76 exotic marine species (about 6% of the listed exotics) on ten variables in marine communities. These species caused an overall significant, but modest in magnitude (as indicated by a mean effect size of g < 0.2), decrease in ecological variables. Marine primary producers and predators were the most disruptive trophic groups of the exotic species. Approximately 10% (that is, 2 out of 19) of the exotic species assessed in at least three independent studies had significant impacts on native species. Separating the innocuous from the disruptive exotic species provides a basis for triage efforts to control the marine exotic species that have the most impact, thereby helping to meet Aichi Biodiversity Target 9 of the Convention on Biological Diversity.

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Data availability

All data underlying the study have been deposited in PANGAEA at https://doi.pangaea.de/10.1594/PANGAEA.895681.

Code availability

The R script used in this manuscript will be deposited in the Github community repository upon publication (https://github.com/ngeraldi/marine-exotics-global-analysis).

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Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.

    Simberloff, D. et al. Impacts of biological invasions: what’s what and the way forward. Trends Ecol. Evol. 28, 58–66 (2013).

  2. 2.

    Hulme, P. E., Pyšek, P., Nentwig, W. & Vilà, M. Will threat of biological invasions unite the European Union? Science 324, 40–41 (2009).

  3. 3.

    Catford, J. A., Bode, M. & Tilman, D. Introduced species that overcome life history tradeoffs can cause native extinctions. Nat. Commun. 9, 2131 (2018).

  4. 4.

    Seebens, H. et al. No saturation in the accumulation of alien species worldwide. Nat. Commun. 8, 14435 (2017).

  5. 5.

    Medina, F. M. et al. A global review of the impacts of invasive cats on island endangered vertebrates. Glob. Change Biol. 17, 3503–3510 (2011).

  6. 6.

    Doherty, T. S., Glen, A. S., Nimmo, D. G., Ritchie, E. G. & Dickman, C. R. Invasive predators and global biodiversity loss. Proc. Natl Acad. Sci. USA 113, 11261–11265 (2016).

  7. 7.

    Witte, F. et al. The destruction of an endemic species flock—quantitative data on the decline of the haplochromine cichlids of Lake Victoria. Environ. Biol. Fishes 34, 1–28 (1992).

  8. 8.

    Ramus, A. P., Silliman, B. R., Thomsen, M. S. & Long, Z. T. An invasive foundation species enhances multifunctionality in a coastal ecosystem. Proc. Natl Acad. Sci. USA 114, 8580–8585 (2017).

  9. 9.

    Geraldi, N. R., Smyth, A. R., Piehler, M. F. & Peterson, C. H. Artificial substrates enhance non-native macroalga and N-2 production. Biol. Invasions 16, 1819–1831 (2014).

  10. 10.

    Russell, J. C. & Blackburn, T. M. The rise of invasive species denialism. Trends Ecol. Evol. 32, 3–6 (2017).

  11. 11.

    Davis, M. et al. Don’t judge species on their origins. Nature 474, 153–154 (2011).

  12. 12.

    Clergeau, P. & Nuñez, M. A. The language of fighting invasive species. Science 311, 951–951 (2006).

  13. 13.

    Richardson, D. M. & Ricciardi, A. Misleading criticisms of invasion science: a field guide. Divers. Distrib. 19, 1461–1467 (2013).

  14. 14.

    Valéry, L., Fritz, H. & Lefeuvre, J.-C. Another call for the end of invasion biology. Oikos 122, 1143–1146 (2013).

  15. 15.

    Ricciardi, A. & Ryan, R. The exponential growth of invasive species denialism. Biol. Invasions 20, 549–553 (2018).

  16. 16.

    Gurevitch, J. & Padilla, D. K. Are invasive species a major cause of extinctions? Trends Ecol. Evol. 19, 470–474 (2004).

  17. 17.

    Clavero, M. & Garcia-Berthou, E. Invasive species are a leading cause of animal extinctions. Trends Ecol. Evol. 20, 110–110 (2005).

  18. 18.

    Pyšek, P., Blackburn, T. M., García-Berthou, E., Perglová, I. & Rabitsch, W. in Impact of Biological Invasions on Ecosystem Services (eds Vilà, M. & Hulme, P. E.) 157–175 (Springer, 2017).

  19. 19.

    Bellard, C., Cassey, P. & Blackburn, T. M. Alien species as a driver of recent extinctions. Biol. Lett. 12, 20150623 (2016).

  20. 20.

    Green, S. J., Akins, J. L., Maljković, A. & Côté, I. M. Invasive lionfish drive Atlantic coral reef fish declines. PLoS ONE 7, e32596 (2012).

  21. 21.

    Vilà, M. et al. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol. Lett. 14, 702–708 (2011).

  22. 22.

    Maggi, E. et al. Ecological impacts of invading seaweeds: a meta-analysis of their effects at different trophic levels. Divers. Distrib. 21, 1–12 (2015).

  23. 23.

    Gallardo, B., Clavero, M., Sánchez, M. I. & Vilà, M. Global ecological impacts of invasive species in aquatic ecosystems. Glob. Change Biol. 22, 151–163 (2016).

  24. 24.

    Guy-Haim, T. et al. Diverse effects of invasive ecosystem engineers on marine biodiversity and ecosystem functions—a global review and meta-analysis. Glob. Change Biol. 24, 906–924 (2018).

  25. 25.

    Mollot, G., Pantel, J. H. & Romanuk, T. N. in Advances in Ecological Research Vol. 56 (eds Bohan, D. A., Dumbrell, A. J. & Massol, F.) Ch. 2 (Academic, 2017).

  26. 26.

    Thomsen, M. S. et al. Impacts of marine invaders on biodiversity depend on trophic position and functional similarity. Mar. Ecol. Prog. Ser. 495, 39–47 (2014).

  27. 27.

    Cameron, E. K., Vilà, M. & Cabeza, M. Global meta-analysis of the impacts of terrestrial invertebrate invaders on species, communities and ecosystems. Glob. Ecol. Biogeogr. 25, 596–606 (2016).

  28. 28.

    Thompson, R. M., Hemberg, M., Starzomski, B. M. & Shurin, J. B. Trophic levels and trophic tangles: the prevalence of omnivory in real food webs. Ecology 88, 612–617 (2007).

  29. 29.

    Vergés, A. et al. Tropical rabbitfish and the deforestation of a warming temperate sea. J. Ecol. 102, 1518–1527 (2014).

  30. 30.

    Sala, E., Kizilkaya, Z., Yildirim, D. & Ballesteros, E. Alien marine fishes deplete algal biomass in the Eastern Mediterranean. PLoS ONE 6, e17356 (2011).

  31. 31.

    The Strategic Plan for Biodiversity 2011-2020 and the Aichi Biodiversity Targets UNEP/CBD/COP/DEC/X/2 2010 (UNEP, CBP, 2010).

  32. 32.

    Jeschke, J. M. et al. Defining the impact of non-native species. Conserv. Biol. 28, 1188–1194 (2014).

  33. 33.

    Lockwood, J. L., Hoopes, M. F. & Marchetti, M. P. Invasion Ecology (Wiley-Blackwell, 2013).

  34. 34.

    Blackburn, T. M. et al. A proposed unified framework for biological invasions. Trends Ecol. Evol. 26, 333–339 (2011).

  35. 35.

    Young, A. M. & Larson, B. M. H. Clarifying debates in invasion biology: a survey of invasion biologists. Environ. Res. 111, 893–898 (2011).

  36. 36.

    Richardson, D. M. et al. Naturalization and invasion of alien plants: concepts and definitions. Divers. Distrib. 6, 93–107 (2000).

  37. 37.

    Jackson, M. C., Loewen, C. J. G., Vinebrooke, R. D. & Chimimba, C. T. Net effects of multiple stressors in freshwater ecosystems: a meta-analysis. Glob. Change Biol. 22, 180–189 (2016).

  38. 38.

    Nunes, J. A. C. C. et al. Global trends on reef fishes’ ecology of fear: flight initiation distance for conservation. Mar. Environ. Res. 136, 153–157 (2018).

  39. 39.

    Bellard, C., Genovesi, P. & Jeschke, J. M. Global patterns in threats to vertebrates by biological invasions. Proc. R. Soc. B 283, 20152454 (2016).

  40. 40.

    Blackburn, T. M., Cassey, P., Duncan, R. P., Evans, K. L. & Gaston, K. J. Avian extinction and mammalian introductions on oceanic islands. Science 305, 1955–1958 (2004).

  41. 41.

    Graham, N. A. J. et al. Seabirds enhance coral reef productivity and functioning in the absence of invasive rats. Nature 559, 250–253 (2018).

  42. 42.

    Delibes, M., Clavero, M., Prenda, J., Blazquez, M. D. & Ferreras, P. Potential impact of an exotic mammal on rocky intertidal communities of northwestern Spain. Biol. Invasions 6, 213–219 (2004).

  43. 43.

    Kurle, C. M., Croll, D. A. & Tershy, B. R. Introduced rats indirectly change marine rocky intertidal communities from algae- to invertebrate-dominated. Proc. Natl Acad. Sci. USA 105, 3800–3804 (2008).

  44. 44.

    Tilman, D., May, R. M., Lehman, C. L. & Nowak, M. A. Habitat destruction and the extinction debt. Nature 371, 65–66 (1994).

  45. 45.

    Anton, A. et al. Decoupled effects (positive to negative) of nutrient enrichment on ecosystem services. Ecol. Appl. 21, 991–1009 (2011).

  46. 46.

    Garcia, D., Martinez, D., Stouffer, D. B. & Tylianakis, J. M. Exotic birds increase generalization and compensate for native bird decline in plant–frugivore assemblages. J. Anim. Ecol. 83, 1441–1450 (2014).

  47. 47.

    Strauss, S. Y., Lau, J. A. & Carroll, S. P. Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol. Lett. 9, 354–371 (2006).

  48. 48.

    Strayer, D. L. Eight questions about invasions and ecosystem functioning. Ecol. Lett. 15, 1199–1210 (2012).

  49. 49.

    Freestone, A. L., Ruiz, G. M. & Torchin, M. E. Stronger biotic resistance in tropics relative to temperate zone: effects of predation on marine invasion dynamics. Ecology 94, 1370–1377 (2013).

  50. 50.

    Hillebrand, H. On the generality of the latitudinal diversity gradient. Am. Nat. 163, 192–211 (2004).

  51. 51.

    Saintilan, N. Biogeography of Australian saltmarsh plants. Austral. Ecol. 34, 929–937 (2009).

  52. 52.

    Kerswell, A. P. Global biodiversity patterns of benthic marine algae. Ecology 87, 2479–2488 (2006).

  53. 53.

    Vilà, M. et al. How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Front. Ecol. Environ. 8, 135–144 (2010).

  54. 54.

    Ricciardi, A. & Kipp, R. Predicting the number of ecologically harmful exotic species in an aquatic system. Divers. Distrib. 14, 374–380 (2008).

  55. 55.

    Kumschick, S. et al. Comparing impacts of alien plants and animals in Europe using a standard scoring system. J. Appl. Ecol. 52, 552–561 (2015).

  56. 56.

    Lowe, S., Browne, M. & Boudjelas, S. 100 of the World’s Worst Invasive Alien Species (IUCN/SSC Invasive Species Specialist Group (ISSG), 2000).

  57. 57.

    Pauchard, A. et al. Biodiversity assessments: origin matters. PLoS Biol. 16, e2006686 (2018).

  58. 58.

    South, J., Dick, J. T. A., McCard, M., Barrios-O’Neill, D. & Anton, A. Predicting predatory impact of juvenile invasive lionfish (Pterois volitans) on a crustacean prey using functional response analysis: effects of temperature, habitat complexity and light regimes. Environ. Biol. Fishes 100, 1155–1165 (2017).

  59. 59.

    Green, D. S. & Crowe, T. P. Context- and density-dependent effects of introduced oysters on biodiversity. Biol. Invasions 16, 1145–1163 (2014).

  60. 60.

    Thomsen, M. et al. Forty years of experiments on aquatic invasive species: are study biases limiting our understanding of impacts? NeoBiota 22, 1–22 (2014).

  61. 61.

    Ricciardi, A. Are modern biological invasions an unprecedented form of global change? Conserv. Biol. 21, 329–336 (2007).

  62. 62.

    Seebens, H. et al. Global rise in emerging alien species results from increased accessibility of new source pools. Proc. Natl Acad. Sci. USA 115, E2264–E2273 (2018).

  63. 63.

    Davis, M. A. & Chew, M. K. ‘The denialists are coming!’ Well, not exactly: a response to Russell and Blackburn. Trends Ecol. Evol. 32, 229–230 (2017).

  64. 64.

    Koricheva, J., Gurevitch, J., Mengersen, K. (eds) Handbook of Meta-analysis in Ecology and Evolution (Princeton Univ. Press, 2013).

  65. 65.

    Nosek, B. A. et al. Promoting an open research culture. Science 348, 1422–1425 (2015).

  66. 66.

    Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G. & PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 6, e1000097 (2009).

  67. 67.

    Borenstein, M., Hedges, L. V., Higgins, J. P. T. & Rothstein, H. R. Introduction to Meta-Analysis (Wiley-Blackwell, 2009).

  68. 68.

    Hannam, M. P. & Wyllie-Echeverria, S. Microtopography promotes coexistence of an invasive seagrass and its native congener. Biol. Invasions 17, 381–395 (2015).

  69. 69.

    Viechbauer, W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 36, 1–48 (2010).

  70. 70.

    Egger, M., Smith, G. D., Schneider, M. & Minder, C. Bias in meta-analysis detected by a simple, graphical test. BMJ 315, 629–634 (1997).

  71. 71.

    Habeck, C. W. & Schultz, A. K. Community-level impacts of white-tailed deer on understory plants in North American forests: a meta-analysis. Aob Plants 7, plv119 (2015).

  72. 72.

    Viechtbauer, W. & Cheung, M. W.-L. Outlier and influence diagnostics for meta-analysis. Res. Synth. Methods 1, 112–125 (2010).

  73. 73.

    Zarnetske, P. L., Seabloom, E. W. & Hacker, S. D. Non-target effects of invasive species management: beachgrass, birds, and bulldozers in coastal dunes. Ecosphere 1, art13 (2010).

  74. 74.

    Moseman, S. M., Zhang, R., Qian, P. Y. & Levin, L. A. Diversity and functional responses of nitrogen-fixing microbes to three wetland invasions. Biol. Invasions 11, 225–239 (2009).

  75. 75.

    Castorani, M. C. N. & Hovel, K. A. Invasive prey indirectly increase predation on their native competitors. Ecology 96, 1911–1922 (2015).

  76. 76.

    Crooks, J. A. Assessing invader roles within changing ecosystems: historical and experimental perspectives on an exotic mussel in an urbanized lagoon. Biol. Invasions 3, 23–36 (2001).

  77. 77.

    Munari, C. Effects of the exotic invader Musculista senhousia on benthic communities of two Mediterranean lagoons. Hydrobiologia 611, 29–43 (2008).

  78. 78.

    Magalhaes, W. F. & Bailey-Brock, J. H. Polychaete assemblages associated with the invasive green alga Avrainvillea amadelpha and surrounding bare sediment patches in Hawaii. Memoirs Mus. Vic. 71, 161–168 (2014).

  79. 79.

    Caño, L., Campos, J. A., García-Magro, D. & Herrera, M. Invasiveness and impact of the non-native shrub Baccharis halimifolia in sea rush marshes: fine-scale stress heterogeneity matters. Biol. Invasions 16, 2063–2077 (2014).

  80. 80.

    Mendez, M. M., Schwindt, E. & Bortolus, A. Differential benthic community response to increased habitat complexity mediated by an invasive barnacle. Aquat. Ecol. 49, 441–452 (2015).

  81. 81.

    Wonham, M. J., O’Connor, M. & Harley, C. D. G. Positive effects of a dominant invader on introduced and native mudflat species. Mar. Ecol. Prog. Ser. 289, 109–116 (2005).

  82. 82.

    Elías, R. et al. Effect of the invader Boccardia proboscidea (Polychaeta: Spionidae) on richness, diversity and structure of SW Atlantic epilithic intertidal community. Mar. Pollut. Bull. 91, 530–536 (2015).

  83. 83.

    Cordell, J. R., Levy, C. & Toft, J. D. Ecological implications of invasive tunicates associated with artificial structures in Puget Sound, Washington, USA. Biol. Invasions 15, 1303–1318 (2013).

  84. 84.

    Bonnici, L., Evans, J., Borg, J. A. & Schembri, P. J. J. Biological aspects and ecological effects of a bed of the invasive non-indigenous mussel Brachidontes pharaonis (Fischer P., 1870) in Malta. Mediterr. Mar. Sci. 13, 153–161 (2012).

  85. 85.

    Malyshev, A. & Quijón, P. A. Disruption of essential habitat by a coastal invader: new evidence of the effects of green crabs on eelgrass beds. ICES J. Mar. Sci. 68, 1852–1856 (2011).

  86. 86.

    Gregory, G. J. & Quijón, P. A. The impact of a coastal invasive predator on infaunal communities: assessing the roles of density and a native counterpart. J. Sea Res. 66, 181–186 (2011).

  87. 87.

    Whitlow, W. L. Changes in survivorship, behavior, and morphology in native soft-shell clams induced by invasive green crab predators. Mar. Ecol. 31, 418–430 (2010).

  88. 88.

    Whitlow, W. L., Rice, N. A. & Sweeney, C. Native species vulnerability to introduced predators: testing an inducible defense and a refuge from predation. Biol. Invasions 5, 23–31 (2003).

  89. 89.

    Large, S. I. & Smee, D. L. Biogeographic variation in behavioral and morphological responses to predation risk. Oecologia 171, 961–969 (2013).

  90. 90.

    Griffen, B. D. & Byers, J. E. Community impacts of two invasive crabs: the interactive roles of density, prey recruitment, and indirect effects. Biol. Invasions 11, 927–940 (2009).

  91. 91.

    Estelle, V. & Grosholz, E. D. Experimental test of the effects of a non-native invasive species on a wintering shorebird. Conserv. Biol. 26, 472–481 (2012).

  92. 92.

    Wootton, L. First report of Carex macrocephala in Eastern North America with notes on its co-occurrence with Carex kobomugi in New Jersey. J. Torrey Bot. Soc. 134, 126–134 (2007).

  93. 93.

    Wootton, L. S. et al. When invasive species have benefits as well as costs: managing Carex kobomugi (Asiatic sand sedge) in New Jersey’s coastal dunes. Biol. Invasions 7, 1017–1027 (2005).

  94. 94.

    Novoa, A. & González, L. Impacts of Carpobrotus edulis (L.) N.E.Br. on the germination, establishment and survival of native plants: a clue for assessing its competitive strength. PLoS ONE 9, e107557 (2014).

  95. 95.

    Magnoli, S. M., Kleinhesselink, A. R. & Cushman, J. H. Responses to invasion and invader removal differ between native and exotic plant groups in a coastal dune. Oecologia 173, 1521–1530 (2013).

  96. 96.

    Novoa, A., González, L., Moravcová, L. & Pyšek, P. Constraints to native plant species establishment in coastal dune communities invaded by Carpobrotus edulis: implications for restoration. Biol. Conserv. 164, 1–9 (2013).

  97. 97.

    Hata, K., Kato, H. & Kachi, N. Seedlings of a native shrub can establish under forests dominated by an alien tree, Casuarina equisetifolia, on subtropical oceanic islands. J. For. Res. 17, 208–212 (2012).

  98. 98.

    Smith, J. R., Vogt, S. C., Creedon, F., Lucas, B. J. & Eernisse, D. J. The non-native turf-forming alga Caulacanthus ustulatus displaces space-occupants but increases diversity. Biol. Invasions 16, 2195–2208 (2014).

  99. 99.

    Bulleri, F. & Piazzi, L. Variations in importance and intensity of competition underpin context dependency in the effects of an invasive seaweed on resident assemblages. Mar. Biol. 162, 485–489 (2015).

  100. 100.

    Tomas, F., Box, A. & Terrados, J. Effects of invasive seaweeds on feeding preference and performance of a keystone Mediterranean herbivore. Biol. Invasions 13, 1559–1570 (2011).

  101. 101.

    Tamburello, L. et al. Variation in the impact of non-native seaweeds along gradients of habitat degradation: a meta-analysis and an experimental test. Oikos 124, 1121–1131 (2015).

  102. 102.

    Klein, J. C. & Verlaque, M. Macrophyte assemblage associated with an invasive species exhibiting temporal variability in its development pattern. Hydrobiologia 636, 369–378 (2009).

  103. 103.

    Kersting, D. K., Ballesteros, E., De Caralt, S. & Linares, C. Invasive macrophytes in a marine reserve (Columbretes Islands, NW Mediterranean): spread dynamics and interactions with the endemic scleractinian coral Cladocora caespitosa. Biol. Invasions 16, 1599–1610 (2014).

  104. 104.

    Tejada, S., Deudero, S., Box, A. & Sureda, A. Physiological response of the sea urchin Paracentrotus lividus fed with the seagrass Posidonia oceanica and the alien algae Caulerpa racemosa and Lophocladia lallemandii. Mar. Environ. Res. 83, 48–53 (2013).

  105. 105.

    Klein, J. C. & Velarque, M. Temporal trends in invasion impacts in macrophyte assemblages of the Mediterranean Sea. Cah. Biol. Mar. 53, 403–407 (2012).

  106. 106.

    Vázquez-Luis, M., Sanchez-Jerez, P. & Bayle-Sempere, J. T. Effects of Caulerpa racemosa var. cylindracea on prey availability: an experimental approach to predation of amphipods by Thalassoma pavo (Labridae). Hydrobiologia 654, 147–154 (2010).

  107. 107.

    Vázquez-Luis, M., Sanchez-Jerez, P. & Bayle-Sempere, J. T. Changes in amphipod (Crustacea) assemblages associated with shallow-water algal habitats invaded by Caulerpa racemosa var. cylindracea in the western Mediterranean Sea. Mar. Environ. Res. 65, 416–426 (2008).

  108. 108.

    Cebrian, E., Linares, C., Marschal, C. & Garrabou, J. Exploring the effects of invasive algae on the persistence of gorgonian populations. Biol. Invasions 14, 2647–2656 (2012).

  109. 109.

    Gribben, P. E., Byers, J. E., Wright, J. T. & Glasby, T. M. Positive versus negative effects of an invasive ecosystem engineer on different components of a marine ecosystem. Oikos 122, 816–824 (2013).

  110. 110.

    Gallucci, F., Hutchings, P., Gribben, P. & Fonseca, G. Habitat alteration and community-level effects of an invasive ecosystem engineer: a case study along the coast of NSW, Australia. Mar. Ecol. Prog. Ser. 449, 95–108 (2012).

  111. 111.

    Gribben, P. E. et al. Reduced performance of native infauna following recruitment to a habitat-forming invasive marine alga. Oecologia 158, 733–745 (2009).

  112. 112.

    Wright, J. T. & Gribben, P. E. Predicting the impact of an invasive seaweed on the fitness of native fauna. J. Appl. Ecol. 45, 1540–1549 (2008).

  113. 113.

    Byers, J. E., Wright, J. T. & Gribben, P. E. Variable direct and indirect effects of a habitat-modifying invasive species on mortality of native fauna. Ecology 91, 1787–1798 (2010).

  114. 114.

    Taylor, S. L., Bishop, M. J., Kelaher, B. P. & Glasby, T. M. Impacts of detritus from the invasive alga Caulerpa taxifolia on a soft sediment community. Mar. Ecol. Prog. Ser. 420, 73–81 (2010).

  115. 115.

    Gribben, P. E., Wright, J. T., O’Connor, W. A. & Steinberg, P. Larval settlement preference of a native bivalve: the influence of an invasive alga versus native substrata. Aquat. Biol. 7, 217–227 (2009).

  116. 116.

    Strain, E. M. A. & Johnson, C. R. The effects of an invasive habitat modifier on the biotic interactions between two native herbivorous species and benthic habitat in a subtidal rocky reef ecosystem. Biol. Invasions 15, 1391–1405 (2013).

  117. 117.

    Strain, E. M. A. & Johnson, C. R. Competition between an invasive urchin and commercially fished abalone. Mar. Ecol. Prog. Ser. 377, 169–182 (2009).

  118. 118.

    Mason, T. J. & French, K. Management regimes for a plant invader differentially impact resident communities. Biol. Conserv. 136, 246–259 (2007).

  119. 119.

    Bugnot, A. B., Coleman, R. A., Figueira, W. F. & Marzinelli, E. M. Community-level impacts of the invasive isopod Cirolana harfordi. Biol. Invasions 17, 1149–1161 (2015).

  120. 120.

    Drouin, A., McKindsey, C. W. & Johnson, L. E. Higher abundance and diversity in faunal assemblages with the invasion of Codium fragile ssp. fragile in eelgrass meadows. Mar. Ecol. Prog. Ser. 424, 105–117 (2011).

  121. 121.

    Schmidt, A. L. & Scheibling, R. E. Effects of native and invasive macroalgal canopies on composition and abundance of mobile benthic macrofauna and turf-forming algae. J. Exp. Mar. Biol. Ecol. 341, 110–130 (2007).

  122. 122.

    Chavanich, S. & Harris, L. G. Impact of the non-native macroalga Codium fragile (Sur.) Hariot ssp tomentosoides (van Goor) Silva on the native snail Lacuna vincta (Montagu, 1803) in the Gulf of Maine. Veliger 47, 85–90 (2004).

  123. 123.

    Drouin, A., McKindsey, C. W. & Johnson, L. E. Detecting the impacts of notorious invaders: experiments versus observations in the invasion of eelgrass meadows by the green seaweed Codium fragile. Oecologia 168, 491–502 (2012).

  124. 124.

    Novais, A., Souza, A. T., Ilarri, M., Pascoal, C. & Sousa, R. Facilitation in the low intertidal: effects of an invasive species on the structure of an estuarine macrozoobenthic assemblage. Mar. Ecol. Prog. Ser. 522, 157–167 (2015).

  125. 125.

    Ilarri, M. I., Souza, A. T., Antunes, C., Guilhermino, L. & Sousa, R. Influence of the invasive Asian clam Corbicula fluminea (Bivalvia: Corbiculidae) on estuarine epibenthic assemblages. Estuar. Coast. Shelf Sci. 143, 12–19 (2014).

  126. 126.

    Talman, S. & Keough, M. Impact of an exotic clam, Corbula gibba, on the commercial scallop Pecten fumatus in Port Phillip Bay, south-east Australia: evidence of resource-restricted growth in a subtidal environment. Mar. Ecol. Prog. Ser. 221, 135–143 (2001).

  127. 127.

    Ragueneau, O. et al. Biodeposition by an invasive suspension feeder impacts the biogeochemical cycle of Si in a coastal ecosystem (Bay of Brest, France). Biogeochemistry 75, 19–41 (2005).

  128. 128.

    Le Pape, O., Guerault, D. & Desaunay, Y. Effect of an invasive mollusc, American slipper limpet Crepidula fornicata, on habitat suitability for juvenile common sole Solea solea in the Bay of Biscay. Mar. Ecol. Prog. Ser. 277, 107–115 (2004).

  129. 129.

    Martin, S. et al. Benthic community respiration in areas impacted by the invasive mollusk Crepidula fornicata. Mar. Ecol. Prog. Ser. 347, 51–60 (2007).

  130. 130.

    Smith, B. E., Collie, J. S. & Lengyel, N. L. Fish trophic engineering: ecological effects of the invasive ascidian Didemnum vexillum (Georges Bank, northwestern Atlantic). J. Exp. Mar. Biol. Ecol. 461, 489–498 (2014).

  131. 131.

    Long, H. A. & Grosholz, E. D. Overgrowth of eelgrass by the invasive colonial tunicate Didemnum vexillum: consequences for tunicate and eelgrass growth and epifauna abundance. J. Exp. Mar. Biol. Ecol. 473, 188–194 (2015).

  132. 132.

    Dijkstra, J. A., Lambert, W. J. & Harris, L. G. Introduced species provide a novel temporal resource that facilitates native predator population growth. Biol. Invasions 15, 911–919 (2013).

  133. 133.

    Petillon, J., Frederic, Y., Alain, C. & Lefeuvre, J.-C. Impact of an invasive plant (Elymus athericus) on the conservation value of tidal salt marshes in western France and implications for management: responses of spider populations. Biol. Conserv. 126, 103–117 (2005).

  134. 134.

    Bruschetti, M., Bazterrica, C., Luppi, T. & Iribarne, O. An invasive intertidal reef-forming polychaete affect habitat use and feeding behavior of migratory and locals birds in a SW Atlantic coastal lagoon. J. Exp. Mar. Biol. Ecol. 375, 76–83 (2009).

  135. 135.

    Bazterrica, M. C., Botto, F. & Iribarne, O. Effects of an invasive reef-building polychaete on the biomass and composition of estuarine macroalgal assemblages. Biol. Invasions 14, 765–777 (2012).

  136. 136.

    Bruschetti, M., Luppi, T., Fanjul, E., Rosenthal, A. & Iribarne, O. Grazing effect of the invasive reef-forming polychaete Ficopomatus enigmaticus (Fauvel) on phytoplankton biomass in a SW Atlantic coastal lagoon. J. Exp. Mar. Biol. Ecol. 354, 212–219 (2008).

  137. 137.

    Schwindt, E., Iribarne, O. O. & Isla, F. I. Physical effects of an invading reef-building polychaete on an Argentinean estuarine environment. Estuar. Coast. Shelf Sci. 59, 109–120 (2004).

  138. 138.

    Bazterrica, M. C. et al. Factors controlling macroalgae assemblages in a Southwest Atlantic coastal lagoon modified by an invading reef forming polychaete. J. Exp. Mar. Biol. Ecol. 443, 169–177 (2013).

  139. 139.

    Heiman, K. W. & Micheli, F. Non-native ecosystem engineer alters estuarine communities. Integr. Comp. Biol. 50, 226–236 (2010).

  140. 140.

    Bruschetti, M., Bazterrica, C., Fanjul, E., Luppi, T. & Iribarne, O. Effect of biodeposition of an invasive polychaete on organic matter content and productivity of the sediment in a coastal lagoon. J. Sea Res. 66, 20–28 (2011).

  141. 141.

    Fukunaga, A., Peyton, K. A. & Thomas, F. I. M. Epifaunal community structure and ammonium uptake compared for the invasive algae, Gracilaria salicornia and Acanthophora specifera, and the native alga, Padina thivyi. J. Exp. Mar. Biol. Ecol. 456, 78–86 (2014).

  142. 142.

    Thomsen, M., Stæhr, P. A., Nejrup, L. B. & Schiel, D. R. Effects of the invasive macroalgae Gracilaria vermiculophylla on two co-occurring foundation species and associated invertebrates. Aquat. Invasions 8, 133–145 (2013).

  143. 143.

    Höffle, H., Thomsen, M. S. & Holmer, M. High mortality of Zostera marina under high temperature regimes but minor effects of the invasive macroalgae Gracilaria vermiculophylla. Estuar. Coast. Shelf Sci. 92, 35–46 (2011).

  144. 144.

    Thomsen, M. S. Experimental evidence for positive effects of invasive seaweed on native invertebrates via habitat-formation in a seagrass bed. Aquat. Invasions 5, 341–346 (2010).

  145. 145.

    Martínez-Lüscher, J. & Holmer, M. Potential effects of the invasive species Gracilaria vermiculophylla on Zostera marina metabolism and survival. Mar. Environ. Res. 69, 345–349 (2010).

  146. 146.

    Janiak, D. S. & Whitlatch, R. B. 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 (2012).

  147. 147.

    Brousseau, D. & Goldberg, R. Effect of predation by the invasive crab Hemigrapsus sanguineus on recruiting barnacles Semibalanus balanoides in western Long Island Sound, USA. Mar. Ecol. Prog. Ser. 339, 221–228 (2007).

  148. 148.

    Brousseau, D. J., Goldberg, R. & Garza, C. Impact of predation by the invasive crab Hemigrapsus sanguineus on survival of juvenile blue mussels in Western Long Island Sound. Northeast. Nat. 21, 119–133 (2014).

  149. 149.

    Bennett, A. E., Thomsen, M. & Strauss, S. Y. Multiple mechanisms enable invasive species to suppress native species. Am. J. Bot. 98, 1086–1094 (2011).

  150. 150.

    Harvey, K. J., Britton, D. R. & Minchinton, T. E. Detecting impacts of non-native species on associated invertebrate assemblages depends on microhabitat. Austral. Ecol. 39, 511–521 (2014).

  151. 151.

    Kamalakannan, B., Jeevamani, J. J. J., Nagendran, N. A., Pandiaraja, D. & Chandrasekaran, S. Impact of removal of invasive species Kappaphycus alvarezii from coral reef ecosystem in Gulf of Mannar, India. Curr. Sci. 106, 1401–1408 (2014).

  152. 152.

    Sato, S., Chiba, T. & Hasegawa, H. Long-term fluctuations in mollusk populations before and after the appearance of the alien predator Euspira fortunei on the Tona coast, Miyagi Prefecture, northern Japan. Fish. Sci. 78, 589–595 (2012).

  153. 153.

    Rowles, A. D. & O’dowd, D. J. Impacts of the invasive Argentine ant on native ants and other invertebrates in coastal scrub in south-eastern Australia. Austral. Ecol. 34, 239–248 (2009).

  154. 154.

    Bedini, R., Bedini, M., Bonechi, L. & Piazzi, L. Effects of non-native turf-forming Rhodophyta on mobile macro-invertebrate assemblages in the north-western Mediterranean Sea. Mar. Biol. Res. 11, 430–437 (2015).

  155. 155.

    Eash-Loucks, W. E., Kimball, M. E. & Petrinec, K. M. Long-term changes in an estuarine mud crab community: evaluating the impact of non-native species. J. Crustac. Biol. 34, 731–738 (2014).

  156. 156.

    O’Shaughnessy, K. A. & Harding, J. M. & Burge, E. J. Ecological effects of the invasive parasite Loxothylacus panopaei on the flatback mud crab Eurypanopeus depressus with implications for estuarine communities. Bull. Mar. Sci. 90, 611–621 (2014).

  157. 157.

    Wilkie, E. M., Bishop, M. J. & O’Connor, W. A. The density and spatial arrangement of the invasive oyster Crassostrea gigas determines its impact on settlement of native oyster larvae. Ecol. Evol. 3, 4851–4860 (2013).

  158. 158.

    Krassoi, F. R., Brown, K. R., Bishop, M. J., Kelaher, B. P. & Summerhayes, S. Condition-specific competition allows coexistence of competitively superior exotic oysters with native oysters. J. Anim. Ecol. 77, 5–15 (2008).

  159. 159.

    Bray, D. J., Green, I., Golicher, D. & Herbert, R. J. H. Spatial variation of trace metals within intertidal beds of native mussels (Mytilus edulis) and non-native Pacific oysters (Crassostrea gigas): implications for the food web? Hydrobiologia 757, 235–249 (2015).

  160. 160.

    Green, D. S., Boots, B. & Crowe, T. P. Effects of non-indigenous oysters on microbial diversity and ecosystem functioning. PLoS ONE 7, e48410 (2012).

  161. 161.

    Green, D. S. & Crowe, T. P. Physical and biological effects of introduced oysters on biodiversity in an intertidal boulder field. Mar. Ecol. Prog. Ser. 482, 119–132 (2013).

  162. 162.

    Wegener, A. R. & Buschbaum, C. Alien epibiont (Crassostrea gigas) impacts on native periwinkles (Littorina littorea). Aquat. Invasions 6, 281–290 (2011).

  163. 163.

    Kochmann, J., Buschbaum, C., Volkenborn, N. & Reise, K. Shift from native mussels to alien oysters: differential effects of ecosystem engineers. J. Exp. Mar. Biol. Ecol. 364, 1–10 (2008).

  164. 164.

    Green, D. S., Rocha, C. & Crowe, T. P. Effects of non-indigenous oysters on ecosystem processes vary with abundance and context. Ecosystems 16, 881–893 (2013).

  165. 165.

    Nicastro, A., Bishop, M. J., Kelaher, B. P. & Benedetti-Cecchi, L. Export of non-native gastropod shells to a coastal lagoon: alteration of habitat structure has negligible effects on infauna. J. Exp. Mar. Biol. Ecol. 374, 31–36 (2009).

  166. 166.

    Hietanen, S., Laine, A. O. & Lukkari, K. The complex effects of the invasive polychaetes Marenzelleria spp. on benthic nutrient dynamics. J. Exp. Mar. Biol. Ecol. 352, 89–102 (2007).

  167. 167.

    Urban-Malinga, B., Warzocha, J. & Zalewski, M. Effects of the invasive polychaete Marenzelleria spp. on benthic processes and meiobenthos of a species-poor brackish system. J. Sea Res. 80, 25–34 (2013).

  168. 168.

    Quintana, C. O., Kristensen, E. & Valdemarsen, T. Impact of the invasive polychaete Marenzelleria viridis on the biogeochemistry of sandy marine sediments. Biogeochemistry 115, 95–109 (2013).

  169. 169.

    Kristensen, E., Hansen, T., Delefosse, M., Banta, G. T. & Quintana, C. O. Contrasting effects of the polychaetes Marenzelleria viridis and Nereis diversicolor on benthic metabolism and solute transport in sandy coastal sediment. Mar. Ecol. Prog. Ser. 425, 125–139 (2011).

  170. 170.

    Yuan, W. S., Hoffman, E. A. & Walters, L. J. Effects of nonnative invertebrates on two life stages of the native eastern oyster Crassostrea virginica. Biol. Invasions 18, 689–701 (2016).

  171. 171.

    Krumhansl, K. A., Lee, J. M. & Scheibling, R. E. Grazing damage and encrustation by an invasive bryozoan reduce the ability of kelps to withstand breakage by waves. J. Exp. Mar. Biol. Ecol. 407, 12–18 (2011).

  172. 172.

    Roohi, A. et al. Impact of a new invasive ctenophore (Mnemiopsis leidyi) on the zooplankton community of the Southern Caspian sea. Mar. Ecol. 29, 421–434 (2008).

  173. 173.

    Aldridge, D. C., Salazar, M., Serna, A. & Cock, J. Density-dependent effects of a new invasive false mussel, Mytilopsis trautwineana (Tryon 1866), on shrimp, Litopenaeus vannamei (Boone 1931), aquaculture in Colombia. Aquaculture 281, 34–42 (2008).

  174. 174.

    Branch, G. M., Odendaal, F. & Robinson, T. B. Competition and facilitation between the alien mussel Mytilus galloprovincialis and indigenous species: moderation by wave action. J. Exp. Mar. Biol. Ecol. 383, 65–78 (2010).

  175. 175.

    Sellheim, K., Stachowicz, J. J. & Coates, R. C. Effects of a nonnative habitat-forming species on mobile and sessile epifaunal communities. Mar. Ecol. Prog. Ser. 398, 69–80 (2010).

  176. 176.

    Hanekom, N. Invasion of an indigenous Perna perna mussel bed on the south coast of South Africa by an alien mussel Mytilus galloprovincialis and its effect on the associated fauna. Biol. Invasions 10, 233–244 (2008).

  177. 177.

    Chapman, M. G., People, J. & Blockley, D. Intertidal assemblages associated with naturalcorallina turf and invasive mussel beds. Biodivers. Conserv. 14, 1761–1776 (2005).

  178. 178.

    Hollebone, A. L. & Hay, M. E. An invasive crab alters interaction webs in a marine community. Biol. Invasions 10, 347–358 (2008).

  179. 179.

    Kimball, M. E. & Able, K. W. Nekton utilization of intertidal salt marsh creeks: tidal influences in natural Spartina, invasive Phragmites, and marshes treated for Phragmites removal. J. Exp. Mar. Biol. Ecol. 346, 87–101 (2007).

  180. 180.

    Torchin, M. E. Native fish grows faster in the presence of a potential introduced competitor. Aquat. Invasions 5, 163–167 (2010).

  181. 181.

    Richman, S. E. & Lovvorn, J. R. Relative foraging value to lesser scaup ducks of native and exotic clams from San Francisco Bay. Ecol. Appl. 14, 1217–1231 (2004).

  182. 182.

    Brenneis, V. E. F., Sih, A. & de Rivera, C. E. Integration of an invasive consumer into an estuarine food web: direct and indirect effects of the New Zealand mud snail. Oecologia 167, 169–179 (2011).

  183. 183.

    Elise, S., Urbina-Barreto, I., Boadas-Gil, H., Galindo-Vivas, M. & Kulbicki, M. No detectable effect of lionfish (Pterois volitans and P. miles) invasion on a healthy reef fish assemblage in Archipelago Los Roques National Park, Venezuela. Mar. Biol. 162, 319–330 (2015).

  184. 184.

    Black, A. N., Weimann, S. R., Imhoff, V. E., Richter, M. L. & Itzkowitz, M. A differential prey response to invasive lionfish, Pterois volitans: prey naivete and risk-sensitive courtship. J. Exp. Mar. Biol. Ecol. 460, 1–7 (2014).

  185. 185.

    Albins, M. A. Effects of invasive Pacific red lionfish Pterois volitans versus a native predator on Bahamian coral-reef fish communities. Biol. Invasions 15, 29–43 (2013).

  186. 186.

    Anton, A. et al. Prey naiveté to invasive lionfish (Pterois volitans) on Caribbean coral reefs. Mar. Ecol. Prog. Ser. 544, 257–269 (2016).

  187. 187.

    Green, S. J. et al. Linking removal targets to the ecological effects of invaders: a predictive model and field test. Ecol. Appl. 24, 1311–1322 (2014).

  188. 188.

    Ingeman, K. E. & Webster, M. S. Native prey mortality increases but remains density-dependent following lionfish invasion. Mar. Ecol. Prog. Ser. 531, 241–252 (2015).

  189. 189.

    Sweetman, A. K. et al. Impacts of exotic mangrove forests and mangrove deforestation on carbon remineralization and ecosystem functioning in marine sediments. Biogeosciences 7, 2129–2145 (2010).

  190. 190.

    Bidegain, G. & Juanes, J. A. Does expansion of the introduced Manila clam Ruditapes philippinarum cause competitive displacement of the European native clam Ruditapes decussatus? J. Exp. Mar. Biol. Ecol. 445, 44–52 (2013).

  191. 191.

    Holloway, M. G. & Keough, M. J. An introduced polychaete affects recruitment and larval abundance of sessile invertebrates. Ecol. Appl. 12, 1803–1823 (2002).

  192. 192.

    Holloway, M. G. & Keough, M. J. Effects of an introduced polychaete, Sabella spallanzanii, on the development of epifaunal assemblages. Mar. Ecol. Prog. Ser. 236, 137–154 (2002).

  193. 193.

    Robinson, T. B. & Swart, C. Distribution and impact of the alien anemone Sagartia ornata in the West Coast National Park. Koedoe 57, a1246 (2015).

  194. 194.

    Salvaterra, T., Green, D. S., Crowe, T. P. & O’Gorman, E. J. Impacts of the invasive alga Sargassum muticum on ecosystem functioning and food web structure. Biol. Invasions 15, 2563–2576 (2013).

  195. 195.

    Lang, A. C. & Buschbaum, C. Facilitative effects of introduced Pacific oysters on native macroalgae are limited by a secondary invader, the seaweed Sargassum muticum. J. Sea Res. 63, 119–128 (2010).

  196. 196.

    Sánchez, Í. & Fernández, C. Impact of the invasive seaweed Sargassum Muticum (phaeophyta) on an intertidal macroalgal assemblage1. J. Phycol. 41, 923–930 (2005).

  197. 197.

    Rossi, F., Incera, M., Callier, M. & Olabarria, C. Effects of detrital non-native and native macroalgae on the nitrogen and carbon cycling in intertidal sediments. Mar. Biol. 158, 2705–2715 (2011).

  198. 198.

    Britton-Simmons, K. H., Pister, B., Sánchez, I. & Okamoto, D. Response of a native, herbivorous snail to the introduced seaweed Sargassum muticum. Hydrobiologia 661, 187–196 (2011).

  199. 199.

    Vye, S. R., Emmerson, M. C., Arenas, F., Dick, J. T. A. & O’Connor, N. E. Stressor intensity determines antagonistic interactions between species invasion and multiple stressor effects on ecosystem functioning. Oikos 124, 1005–1012 (2015).

  200. 200.

    Rodil, I. F., Olabarria, C., Lastra, M. & López, J. Differential effects of native and invasive algal wrack on macrofaunal assemblages inhabiting exposed sandy beaches. J. Exp. Mar. Biol. Ecol. 358, 1–13 (2008).

  201. 201.

    Vaz‐Pinto, F., Olabarria, C. & Arenas, F. Ecosystem functioning impacts of the invasive seaweed Sargassum muticum (Fucales, Phaeophyceae). J. Phycol. 50, 108–116 (2014).

  202. 202.

    Buschbaum, C., Chapman, A. S. & Saier, B. How an introduced seaweed can affect epibiota diversity in different coastal systems. Mar. Biol. 148, 743–754 (2006).

  203. 203.

    White, L. F. & Shurin, J. B. Density dependent effects of an exotic marine macroalga on native community diversity. J. Exp. Mar. Biol. Ecol. 405, 111–119 (2011).

  204. 204.

    Viejo, R. M. Mobile epifauna inhabiting the invasive Sargassum muticum and two local seaweeds in northern Spain. Aquat. Bot. 64, 131–149 (1999).

  205. 205.

    Tang, Y. et al. Ecological influence of exotic plants of Sonneratia apetala on understory macrofauna. Acta Oceanol. Sin. 31, 115–125 (2012).

  206. 206.

    Ma, Z., Gan, X., Cai, Y., Chen, J. & Li, B. Effects of exotic Spartina alterniflora on the habitat patch associations of breeding saltmarsh birds at Chongming Dongtan in the Yangtze River estuary, China. Biol. Invasions 13, 1673–1686 (2011).

  207. 207.

    Gan, X. et al. Potential impacts of invasive Spartina alterniflora on spring bird communities at Chongming Dongtan, a Chinese wetland of international importance. Estuar. Coast. Shelf Sci. 83, 211–218 (2009).

  208. 208.

    Zhou, H.-X., Liu, J.-E., Zhou, J. & Qin, P. Effect of an alien species Spartina alterniflora Loisel on biogeochemical processes of intertidal ecosystem in the Jiangsu coastal region, China. Pedosphere 18, 77–85 (2008).

  209. 209.

    Neira, C., Levin, L. A., Grosholz, E. D. & Mendoza, G. Influence of invasive Spartina growth stages on associated macrofaunal communities. Biol. Invasions 9, 975–993 (2007).

  210. 210.

    Chen, H., Zhang, P., Li, B. & Wu, J. Invasive cordgrass facilitates epifaunal communities in a Chinese marsh. Biol. Invasions 17, 205–217 (2015).

  211. 211.

    Ma, Z., Gan, X., Choi, C.-Y. & Li, B. Effects of invasive cordgrass on presence of Marsh Grassbird in an area where it is not native. Conserv. Biol. J. Soc. Conserv. Biol. 28, 150–158 (2014).

  212. 212.

    Tong, C. et al. Contrasting nutrient stocks and litter decomposition in stands of native and invasive species in a sub-tropical estuarine marsh. Environ. Res. 111, 909–916 (2011).

  213. 213.

    Qin, H. et al. Effects of invasive cordgrass on crab distributions and diets in a Chinese salt marsh. Mar. Ecol. Prog. Ser. 415, 177–187 (2010).

  214. 214.

    Wu, Y.-T. et al. Effects of saltmarsh invasion by Spartina alterniflora on arthropod community structure and diets. Biol. Invasions 11, 635–649 (2009).

  215. 215.

    Yuan, J. et al. Shifts in methanogen community structure and function across a coastal marsh transect: effects of exotic Spartina alterniflora invasion. Sci. Rep. 6, 18777 (2016).

  216. 216.

    Zhou, H.-X., Liu, J. & Qin, P. Impacts of an alien species (Spartina alterniflora) on the macrobenthos community of Jiangsu coastal inter-tidal ecosystem. Ecol. Eng. 35, 521–528 (2009).

  217. 217.

    Cutajar, J., Shimeta, J. & Nugegoda, D. Impacts of the invasive grass Spartina anglica on benthic macrofaunal assemblages in a temperate Australian saltmarsh. Mar. Ecol. Prog. Ser. 464, 107–120 (2012).

  218. 218.

    Hacker, S. D. & Dethier, M. N. Community modification by a grass invader has differing impacts for marine habitats. Oikos 113, 279–286 (2006).

  219. 219.

    Gooden, B. & French, K. Impacts of alien plant invasion on native plant communities are mediated by functional identity of resident species, not resource availability. Oikos 124, 298–306 (2015).

  220. 220.

    Gooden, B. & French, K. Non-interactive effects of plant invasion and landscape modification on native communities. Divers. Distrib. 20, 626–639 (2014).

  221. 221.

    Pettay, D. T., Wham, D. C., Smith, R. T., Iglesias-Prieto, R. & LaJeunesse, T. C. Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proc. Natl Acad. Sci. USA 112, 7513–7518 (2015).

  222. 222.

    Miranda, R. J., Cruz, I. C. S. & Barros, F. Effects of the alien coral Tubastraea tagusensis on native coral assemblages in a southwestern Atlantic coral reef. Mar. Biol. 163, 45 (2016).

  223. 223.

    Irigoyen, A. J., Trobbiani, G., Sgarlatta, M. P. & Raffo, M. P. Effects of the alien algae Undaria pinnatifida (Phaeophyceae, Laminariales) on the diversity and abundance of benthic macrofauna in Golfo Nuevo (Patagonia, Argentina): potential implications for local food webs. Biol. Invasions 13, 1521–1532 (2011).

  224. 224.

    Forrest, B. M. & Taylor, M. D. Assessing invasion impact: survey design considerations and implications for management of an invasive marine plant. Biol. Invasions 4, 375–386 (2002).

  225. 225.

    South, P. M. et al. Transient effects of an invasive kelp on the community structure and primary productivity of an intertidal assemblage. Mar. Freshw. Res. 67, 103–112 (2016).

  226. 226.

    Gestoso, I., Arenas, F. & Olabarria, C. Biotic resistance and facilitation of a non-indigenous mussel vary with environmental context. Mar. Ecol. Prog. Ser. 506, 163–173 (2014).

  227. 227.

    Hendrickx, J. P., Creese, R. G. & Gribben, P. E. Impacts of a non-native gastropod with a limited distribution; less conspicuous invaders matter too. Mar. Ecol. Prog. Ser. 537, 151–162 (2015).

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Acknowledgements

The authors are thankful to the following individuals: S. Ghani for conducting the network diagrams for Fig. 2, using resources and services at the Visualization Core Lab at KAUST; I. Ferri for advice on the design of Fig. 5; and C. Nelson for her assistance organizing the Invasive Species Workshop at KAUST. This research was supported by King Abdullah University of Science and Technology (KAUST) through baseline funding to C.M.D., by Horizon 2020 Framework Programme (EU Framework Programme for Research and Innovation H2020) (grant no. 659246) to S.B., by the Ministry of Economy and Competitiveness, Agencia Estatal de Investigación (Spanish Agencia Estatal de Investigación) (grant no. FJCI – 2016 – 30728) to S.B., by the Ministry of Economy and Competitiveness, Agencia Estatal de Investigación (Spanish Agencia Estatal de Investigación) (grant no. CGL 2015 – 71809 – P) to N.M., J.S.-G. and S.B., and by the ARC Centre of Excellence for Coral Reef Studies (grant no. CE 140100020) to J.M.P.

Author information

Affiliations

  1. Red Sea Research Centre, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia

    • Andrea Anton
    • , Nathan R. Geraldi
    •  & Carlos M. Duarte
  2. School of Biological Sciences, The University of Queensland, Brisbane, Queensland, Australia

    • Catherine E. Lovelock
  3. Institute of Oceanography, Hellenic Center for Marine Research, Heraklion, Greece

    • Eugenia T. Apostolaki
  4. Global Change Research Group, Institut Mediterrani d’Estudis Avançats (IMEDEA), CSIC-UIB, Esporles, Spain

    • Scott Bennett
    • , Nuria Marbà
    •  & Julia Santana-Garcon
  5. Dauphin Island Sea Laboratory, Marine Environmental Sciences Consortium, Dauphin Island, AL, USA

    • Just Cebrian
  6. Department of Marine Sciences, University of South Alabama, Mobile, AL, USA

    • Just Cebrian
  7. Northern Gulf Institute, Mississippi State University, Stennis Space Center, MS, USA

    • Just Cebrian
  8. Arctic Research Centre, Department of Bioscience, Aarhus University, Aarhus, Denmark

    • Dorte Krause-Jensen
  9. Department of Bioscience, Aarhus University, Silkeborg, Denmark

    • Dorte Krause-Jensen
  10. Laboratorio de Ecologia, Instituto de Investigaciones Marinas y Costeras (IIMyC) CONICET-UNMdP, Mar de Plata, Argentina

    • Paulina Martinetto
  11. Australian Research Council Centre of Excellence for Coral Reef Studies, School of Biological Sciences, The University of Queensland, Brisbane, Queensland, Australia

    • John M. Pandolfi
  12. Computational Bioscience Research Center, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia

    • Carlos M. Duarte

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Contributions

C.M.D., A.A., C.E.L. and N.R.G. conceived and designed the study. A.A., N.R.G., C.E.L., E.T.A., S.B., J.C., D.K.-J., N.M., P.M., J.M.P. and J.S.-G. constructed the dataset. A.A. and N.R.G. performed the data analyses with contributions from all co-authors. All authors contributed to writing and improving the manuscript and approved the submission.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Andrea Anton.

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    Supplementary Figures 1–4 and Supplementary Tables 1–5

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DOI

https://doi.org/10.1038/s41559-019-0851-0