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Community composition influences the population growth and ecological impact of invasive species in response to climate change

  • Global change ecology – original research
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Abstract

Predicting long-term impacts of introduced species is challenging, since stressors related to global change can influence species–community interactions by affecting both demographic rates of invasive species and the structure of the invaded ecosystems. Invasive species can alter ecosystem structure over time, further complicating interactions between invasive species and invaded communities in response to additional stressors. Few studies have considered how cumulative impacts of species invasion and global change on the structure of invaded ecosystems may influence persistence and population growth of introduced species. Here, we present an empirically based population model for an invasive epiphytic bryozoan that can dramatically alter the structure of its invaded kelp bed ecosystems. We use this model to predict the response of invasive species to climate change and associated changes in the invaded community. Population growth of the bryozoan increased under near-future projections of increasing ocean temperature; however, the magnitude of population growth depended on the community composition of invaded kelp beds. Our results suggest that, in some cases, indirect effects of climate change mediated through changes to the structure of the invaded habitat can modulate direct effects of climate change on invasive species, with consequences for their long-term ecological impact. Our findings have important implications for management of invasive species, as modifying invaded habitats at local to regional scales may be more logistically feasible than addressing stressors related to global climate change.

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References

  • Barlow ND, Kean JM (2004) Resource abundance and invasiveness: a simple model. Biol Invasions 6:261–268

    Article  Google Scholar 

  • Blackburn TM, Cassey P, Lockwood KL (2009) The role of species traits in the establishment success of exotic birds. Glob Change Biol 15:2852–2860

    Article  Google Scholar 

  • Bohn K, Richardson CA, Jenkins SR (2015) The distribution of the invasive non-native gastropod Crepidula fornicata in the Milford Haven Waterway, its northernmost population along the west coast of Britain. Helgol Mar Res 69:313–325

    Article  Google Scholar 

  • Byers JE, Noonburg EG (2003) Scale dependent effects of biotic resistance to biological invasion. Ecology 84:1428–1433

    Article  Google Scholar 

  • Carlton JT (1996) Pattern, process, and prediction in marine invasion ecology. Biol Conserv 78:97–106

    Article  Google Scholar 

  • Carlton JT (2000) Global change and biological invasions in the ocean. In: Mooney HA, Richard JH (eds) invasive species in a changing world. Island Press, Washington, DC, pp 31–54

    Google Scholar 

  • Caswell H (2001) Matrix population models. Sinauer Associates, Sunderland

    Google Scholar 

  • Cockrell ML, Sorte CJB (2013) Predicting climate-induced changes in population dynamics of invasive species in a marine epibenthic community. J Exp Mar Biol Ecol 440:42–48

    Article  Google Scholar 

  • Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166

    Article  Google Scholar 

  • Dafforn KA, Johnson EL, Glasby TM (2009) Shallow moving structures promote marine invader dominance. Biofouling 25:277–287

    Article  PubMed  CAS  Google Scholar 

  • Denley D, Metaxas A (2016) Quantifying mortality of modular organisms: a comparison of partial and whole colony mortality in a colonial bryozoan. Ecosphere 7(10):e01483. https://doi.org/10.1002/ecs2.1483

    Article  Google Scholar 

  • Denley D, Metaxas A (2017a) Effects of intrinsic and extrinsic factors on reproduction of an ecologically significant invasive bryozoan: implications for invasion success. Mar Biol 164:145. https://doi.org/10.1007/s00227-017-3172-3

    Article  Google Scholar 

  • Denley D, Metaxas A (2017b) Lack of substrate specificity contributes to invasion success and persistence of Membranipora membranacea in the northwest Atlantic. Mar Ecol Prog Ser 580:117–129. https://doi.org/10.3354/meps12287

    Article  Google Scholar 

  • Dick JTA, Alexander ME, Ricciardi A, Laverty C, Downey PO, Xu M, Jeschke JM, Saul W-C, Hill MP, Wasserman R, Barrios-O’Neil D, Weyl OLF, Shaw RH (2017) Functional responses can unify invasion ecology. Biol Invasions 19:1667–1672

    Article  Google Scholar 

  • Didham RK, Tylianakis JM, Gemmell NJ, Rand TA, Ewers RM (2007) Interactive effects of habitat modification and species invasion on native species decline. Trends Ecol Evol 22:489–496

    Article  PubMed  Google Scholar 

  • Drake JM, Baggenstos P, Lodge DM (2005) Propagule pressure and persistence in experimental populations. Biol Lett 1:480–483

    Article  PubMed  PubMed Central  Google Scholar 

  • Drayton B, Primack RB (1999) Experimental extinction of garlic mustard (Alliaria petiolata) populations: implications for weed science and conservation biology. Biol Invasions 1:159–167

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Filbee-Dexter K, Feehan CJ, Scheibling RE (2016) Large-scale degradation of a kelp ecosystem in an ocean warming hotspot. Mar Ecol Prog Ser 543:141–152

    Article  CAS  Google Scholar 

  • Forrest BM, Fletcher LM, Atalah J, Piola RF, Hopkins GA (2013) Predation limits spread of Didemnum vexillum into natural habitats from refuges on anthropogenic structures. PLoS One 8(12):e82229. https://doi.org/10.1371/journal.pone.0082229

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fridley JD, Stachowicz JJ, Naeem S, Sax DF, Seabloom EW, Smith MD, Stohlgren TJ, Tilman D, Von Holle B (2007) The invasion paradox: reconciling pattern and process is species invasions. Ecology 88:3–17

    Article  PubMed  CAS  Google Scholar 

  • Gehman A-LM, Hall RJ, Byers JE (2018) Host and parasite thermal ecology jointly determine the effect of climate warming on epidemic dynamics. PNAS 21:12. https://doi.org/10.1073/pnas.1705067115

    Article  CAS  Google Scholar 

  • Gonzalez A, Lambert A, Ricciardi A (2008) When does ecosystem engineering cause invasion and species replacement? Oikos 117:1247–1257

    Article  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

    Article  PubMed  Google Scholar 

  • Harris LG, Tyrrell MC (2001) Changing community states in the Gulf of Maine: synergism between invaders, overfishing and climate change. Biol Invasions 3:9–21

    Article  Google Scholar 

  • Hellmann JJ, Byers JE, Bierwagen BG, Dukes JS (2008) Five potential consequences of climate change for invasive species. Conserv Biol 22:534–543

    Article  PubMed  Google Scholar 

  • Hulme PE, Pysek P, Jarosík V, Pergl J, Schaffner U, Vilà M (2013) Bias and error in understanding plan invasion impacts. Trends Ecol Evol 28:212–218

    Article  PubMed  Google Scholar 

  • Iacarella JC, Dick JTA, Alexander ME, Ricciardi A (2015) Ecological impacts of invasive alien species along temperature gradients: testing the role of environmental matching. Ecol Appl 25:706–716

    Article  PubMed  Google Scholar 

  • Kean JM, Barlow ND (2000) A spatial model for successful biological control of Sitona discoideus by Microctonus aethiopoides. J Appl Ecol 10:689–710

    Article  Google Scholar 

  • Kirtman B, Power SB, Adedoyin JA, Boer GJ, Bojariu R, Camilloni I, Doblas-Reyes FJ, Fiore AM, Kimoto M, Meehl GA, Prather M, Sarr A, Schär C, Sutton R, van Oldenborgh GJ, Vecchi G, Wang HJ (2013) Near-term climate change: projections and predictability. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PH (eds) Climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    Article  PubMed  Google Scholar 

  • Krumhansl KA, Scheibling RE (2011) Detrital production in Nova Scotia kelp beds: patterns and processes. Mar Ecol Prog Ser 421:67–82

    Article  Google Scholar 

  • Krumhansl KA, Lee JM, Scheibling RE (2011) 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

    Article  Google Scholar 

  • Krumhansl KA, Lauzon-Guay J-S, Scheibling RE (2014) Modeling effects of climate change and phase shifts on detrital production of a kelp bed. Ecology 95:763–774

    Article  PubMed  Google Scholar 

  • Lambert G (2003) Marine biodiversity of Guam: the Ascidiacea. Micronesica 35–36:588–597

    Google Scholar 

  • Lefkovitch LP (1965) The study of population growth in organisms grouped by stages. Biometrics 21:1–18

    Article  Google Scholar 

  • Levin PS, Coyer JA, Petrik K, Good TP (2002) Community-wide effects of nonindigenous species on temperate rocky reefs. Ecology 83:3182–3193

    Article  Google Scholar 

  • Loder WL, van der Baaren A, Yashayaev I (2015) Climate comparisons and change projections for the northwest Atlantic from six CMIP5 models. Atmos Ocean 53:529–555

    Article  Google Scholar 

  • Lodge DM (1993a) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133–137

    Article  PubMed  CAS  Google Scholar 

  • Lodge DM (1993b) Species invasions and deletions: community effects and responses to climate and habitat change. In: Kareiva PM, Kingsolver JG, Huey RB (eds) Biotic interactions and global change. Sinauer Associates Inc., Sunderland, pp 367–387

    Google Scholar 

  • MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86:42–55

    Article  Google Scholar 

  • Mech AM, Tobin PC, Teskey RO, Rhea JR, Gandhi KJK (2018) Increases in summer temperatures decrease the survival of an invasive forest insect. Biol Invasions 20:365–374

    Article  Google Scholar 

  • O’Brien J (2018) Processes reinforcing regime shift to turf-forming algae in a kelp bed ecosystem. PhD dissertation, Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada

  • Occhipinti-Ambrogi A (2007) Global change and marine communities: alien species and climate change. Mar Pollut Bull 55:342–352

    Article  PubMed  CAS  Google Scholar 

  • Pimm SL (1989) Theories of predicting success and impact of introduced species. In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmànek M, Williamson M (eds) Biological invasions: a global perspective. Wiley, Chichester, pp 351–367

    Google Scholar 

  • Rahel FJ, Olden JD (2008) Assessing the effects of climate change on aquatic invasive species. Conserv Biol 22:521–533

    Article  PubMed  Google Scholar 

  • Rejmánek M (1995) What makes a species invasive? In: Pysek P, Prach K, Rejmánek M, Wade PM (eds) Plant invasions. SPB Academic Publishing, The Hague, pp 3–13

    Google Scholar 

  • Ricciardi A, Jones LA, Kestrup AM, Ward JM (2011) Impacts of biological invasions on freshwater ecosystems. In: Richardson DM (ed) Fifty years of invasion ecology: the legacy of Charles Elton. Blackwell Publishing Ltd, Chichester, pp 225–235

    Google Scholar 

  • Ricciardi A, Hoopes MF, Marchetti MP, Lockwood JL (2013) Progress toward understanding the ecological impacts of nonnative species. Ecol Monogr 83:263–282

    Article  Google Scholar 

  • Rius M, Clusella-Trullas S, McQuaid CD, Navarro RA, Griffiths CL, Matthee CA, von der Heyden S, Turon X (2014) Range expansions across ecoregions: interactions of climate change, physiology and genetic diversity. Glob Ecol Biogeogr 23:76–88

    Article  Google Scholar 

  • Rosecchi E, Thomas F, Crivelli AJ (2001) Can life-history traits predict the fate of introduced species? A case study of two cyprinid fish in southern France. Freshw Biol 46:845–863

    Article  Google Scholar 

  • Saunders M, Metaxas A (2007) Temperature explains settlement patterns of the introduced bryozoan Membranipora membranacea in Nova Scotia, Canada. Mar Ecol Prog Ser 344:95–106

    Article  Google Scholar 

  • Saunders M, Metaxas A (2008) High recruitment of the introduced bryozoan Membranipora membranacea is associated with kelp bed defoliation in Nova Scotia, Canada. Mar Ecol Prog Ser 369:139–151

    Article  Google Scholar 

  • Saunders M, Metaxas A (2009a) Effects of temperature, size, and food on the growth of Membranipora membranacea in laboratory and field studies. Mar Biol 156:2267–2276

    Article  Google Scholar 

  • Saunders M, Metaxas A (2009b) Population dynamics of a nonindigenous epiphytic bryozoan Membranipora membranacea in the western North Atlantic: effects of kelp substrate. Aquat Biol 8:83–94

    Article  Google Scholar 

  • Saunders MI, Metaxas A, Filgueira R (2010) Implication of warming temperatures for population outbreaks of nonindigenous species (Membranipora membranacea, Bryozoa) in rocky subtidal ecosystems. Limnol Oceanogr 55:1627–1642

    Article  Google Scholar 

  • Scheibling RE, Gagnon P (2009) Temperature-mediated outbreak dynamics of the invasive bryozoan Membranipora membranacea in Nova Scotian kelp beds. Mar Ecol Prog Ser 309:1–13

    Article  Google Scholar 

  • Simberloff D (2011) How common are invasion-induced ecosystem impacts? Biol Invasions 13:1255–1268

    Article  Google Scholar 

  • Simons RD, Page HM, Zaleski S, Miller R, Dugan JE, Schroeder DM, Doheny B (2016) The effects of anthropogenic structures on habitat connectivity and the potential spread of non-native invertebrate species in the offshore environment. PLoS One 11(3):e0152261. https://doi.org/10.1371/journal.pone.0152261

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simonson EJ, Scheibling RE, Metaxas A (2015) Kelp in hot water: I. Warming seawater temperature induces weakening and loss of kelp tissue. Mar Ecol Prog Ser 537:89–104

    Article  CAS  Google Scholar 

  • Sorte CJB, Stachowicz JJ (2011) Patterns and processes of compositional change in a California epibenthic community. Mar Ecol Prog Ser 435:63–74

    Article  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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Strayer DL (2012) Eight questions about invasions and ecosystem functioning. Ecol Lett 15:1199–1210

    Article  PubMed  Google Scholar 

  • Vitousek PM (1990) Biological invasions and ecosystem processes: towards an integration of population biology and ecosystem studies. Oikos 57:7–13

    Article  Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL, Rejmánek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16

    Google Scholar 

  • Williamson M (1996) Biological invasions. Chapman and Hall, London

    Google Scholar 

  • Yorke AF, Metaxas A (2012) Relative importance of kelps and fucoids as substrata of the invasive epiphytic bryozoan Membranipora membranacea in Nova Scotia, Canada. Aquat Biol 16:17–30

    Article  Google Scholar 

  • Yoshioka PM (1973) The population dynamics and ecology of the encrusting ectoproct Membranipora serrilamella. PhD dissertation, University of California, San Diego, California, USA

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Acknowledgements

We thank J. Lindley, R. E. Scheibling, J. O’Brien, C. Feehan, K. Sorochan, K. Filbee-Dexter, E. Simonson, and K. Desilets for assistance with field work. R. E. Scheibling and two anonymous reviewers provided comments on an earlier version of the manuscript. This research was funded by a Natural Sciences and Engineering Research Council (NSERC) Discovery grant to A.M, and a Dalhousie Faculty of Graduate Studies scholarship, Nova Scotia Scholarship, NSERC Canada Graduate Scholarship, and Dalhousie Killam Scholarship to D.D.

Funding

This study was funded by a Natural Sciences and Engineering Research Council Discover grant (NSERC RGPIN-2016-04,878) to AM.

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  1. Department of Oceanography, Dalhousie University, Halifax, NS, B3H 4R2, Canada

    Danielle Denley, Anna Metaxas & Katja Fennel

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  1. Danielle Denley
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  2. Anna Metaxas
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  3. Katja Fennel
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Contributions

DD collected and analysed field data, developed the study design and matrix population model, analysed model output, and wrote the manuscript. AM supervised the study design and analysis and edited the manuscript, KF supervised the development of the matrix population model and analysis of model output and edited the manuscript.

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Correspondence to Danielle Denley.

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All applicable national and institutional guidelines for the care and use of animals were followed in accordance with the recommendations of the Canadian Council on Animal Care and the policies of Dalhousie University.

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Communicated by Daniel C. Reed.

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Denley, D., Metaxas, A. & Fennel, K. Community composition influences the population growth and ecological impact of invasive species in response to climate change. Oecologia 189, 537–548 (2019). https://doi.org/10.1007/s00442-018-04334-4

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