Skip to main content

Advertisement

SpringerLink
Log in

Identifying key processes and drivers affecting the presence of non-indigenous marine species in coastal waters

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Non-indigenous species (NIS) pose a major threat to biodiversity and the functioning and services of ecosystems. Despite their rapid spread in coastal waters worldwide, biotic invasions are widely disregarded in marine conservation planning. To guide conservation actions, a better understanding of the underlying mechanisms determining the success of NIS are therefore needed. Here we develop a combined modelling approach to identify the key drivers and community assembly processes determining the occurrence of invasive benthic invertebrates, using Danish coastal waters as a case study. To reflect factors affecting the introduction, establishment and spread of NIS throughout the area, we compiled long-term monitoring data on NIS, as well as information on commercial shipping, environmental conditions and estimates of larvae settling densities derived from drift model simulations informed by species traits. We then applied a set of species distribution models to identify the key drivers determining the occurrence of NIS. Our results demonstrate a significant positive effect of vessel activity, a negative effect of depth and bottom salinity, as well as a positive effect of the simulated settling densities on the probability of presence. Taken together, our results highlight the role of commercial shipping, habitat characteristics and passive advection of early-life stages on the presence of NIS. Our combined modelling approach provide improved process understanding on the key community assembly processes determining the presence of NIS and may serve to guide monitoring, management and conservation planning in order to limit future invasions and their negative consequences on coastal ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Albins MA (2013) Effects of invasive pacific red lionfish pterois volitans versus a native predator on bahamian coral-reef fish communities. Biol Invasions 15:29–43

    Article  Google Scholar 

  • Bailey SA (2015) An overview of thirty years of research on ballast water as a vector for aquatic invasive species to freshwater and marine environments. Aquat Ecosyst Health Manage 18:261–268

    Article  CAS  Google Scholar 

  • Barr LM, Possingham HP (2013) Are outcomes matching policy commitments in Australian marine conservation planning? Mar Policy 42:39–48

    Article  Google Scholar 

  • Beletsky D, Beletsky R, Rutherford ES, Sieracki JL, Bossenbroek JM, Lindsay Chadderton W, Wittmann ME et al (2017) Predicting spread of aquatic invasive species by lake currents. J Great Lakes Res 43:14–32

    Article  Google Scholar 

  • Berg P, Poulsen J W, (2012), Implementation details for HBM. DMI technical report, No. 12–11, ISSN: 1399 – 1388, Copenhagen

  • Beukhof E, Spaanheden Dencker T, Pecuchet L, Lindegren M (2019a) Spatio-temporal variation in marine fish traits reveals community-wide responses to environmental change. Mar Ecol-Prog Ser 610:205–222

    Article  Google Scholar 

  • Beukhof E, Frelat R, Pecuchet L, Maureaud A, Dencker TS, Sólmundsson J, Punzón A et al (2019b) Marine fish traits follow fast-slow continuum across oceans. Sci Rep 9:17878. https://doi.org/10.1038/s41598-019-53998-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breiman L (2001) Random forests. Mach Learn 45:5–32

  • Carlton JT, Ruiz GM (2005) Vector science and integrated vec tor management in bioinvasion ecology: conceptual frame works. In: Mooney HA, Mack RN, McNeely JA, et al. (Eds).Invasive alien species: a new synthesis. Washington, DC: Island Press

  • Chen D, Xue Y, Fink D, Chen S, Gome, CP (2017) Deep multi-species embedding. IJCAI International joint conference on artificial intelligence, 0: 3639–3646

  • Christensen A, Mariani P, Payne MR (2018) A generic framework for individual-based modelling and physical-biological interaction. PLoS ONE 13(1):e0189956. https://doi.org/10.1371/journal.pone.0189956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christensen A. (2008), Bank resolved prognoses of sandeel fishing potential in the North Sea”. final report for the project "Fiskeriudsigt for tobis i Nordsøen på bankeniveau. (FIUF, 2005–2007)

  • Clarke Murray C, Gartner H, Gregr EJ, Chan K, Pakhomov E, Therriault TW (2014) Spatial distribution of marine invasive species: environmental, demographic and vector drivers. Divers Distrib 20:824–836

    Article  Google Scholar 

  • Conley DJ, Carstensen J, Aertebjerg G, Christensen PB, Dalsgaard T, Hansen JLS, Josefson AB (2007) Long-term changes and impacts of hypoxia in Danish coastal waters RID B-5428-2008. Ecol Appl 17:S165–S184

    Article  Google Scholar 

  • Conley DJ, Carstensen J, Aigars J, Axe P, Bonsdorff E, Eremina T, Haahti BM et al (2011) Hypoxia is increasing in the coastal zone of the baltic sea. Environ Sci Technol 45:6777–6783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • David P, Thébault E, Anneville O, Duyck PF, Chapuis E, Loeuille N (2017) Impacts of invasive species on food webs: a review of empirical data. Adv Ecol Res 56:1–60

    Article  Google Scholar 

  • Drake JM, Lodge DM (2007) Hull fouling is a risk factor for intercontinental species exchange in aquatic ecosystems. Aquat Invasions 2:121–131

    Article  Google Scholar 

  • Dudley N, Parrish JD, Redford KH, Stolton S (2010) The revised IUCN protected area management categories: the debate and ways forward. Oryx 44:485–490

    Article  Google Scholar 

  • Edgar GJ, Stuart-Smith RD, Willis TJ, Kininmonth S, Baker SC, Banks S, Barrett NS et al (2014) Global conservation outcomes depend on marine protected areas with five key features. Nature 506:216–220

    Article  CAS  PubMed  Google Scholar 

  • Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80

    Article  Google Scholar 

  • Elith J, Leathwick JR (2009) Species distribution models: Ecological explanation and prediction across space and time. Annu Rev Ecol Evol Syst 40:677–697

    Article  Google Scholar 

  • Fitzsimons JA (2011) Mislabeling marine protected areas and why it matters-a case study of Australia. Conserv Lett 4:340–345

    Article  Google Scholar 

  • Galil BS (2009) Taking stock: inventory of alien species in the Mediterranean Sea. Biol Invasions 11:359–372

    Article  Google Scholar 

  • Galil BS, Marchini A, Occhipinti-Ambrogi A, Minchin D, Narščius A, Ojaveer H, Olenin S (2014) International arrivals: widespread bioinvasions in European Seas. Ethol Ecol Evol 26:152–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallien L, Carboni M (2017) The community ecology of invasive species: where are we and what’s next? Ecography 40:335–352

    Article  Google Scholar 

  • Gallien L, Carboni M, Münkemüller T (2014) Identifying the signal of environmental filtering and competition in invasion patterns - a contest of approaches from community ecology. Methods Ecol Evol 5:1002–1011

    Article  Google Scholar 

  • Gallien L, Mazel F, Lavergne S, Renaud J, Douzet R, Thuiller W (2015) Contrasting the effects of environment, dispersal and biotic interactions to explain the distribution of invasive plants in alpine communities. Biol Invasions 17:1407–1423

    Article  PubMed  PubMed Central  Google Scholar 

  • Giakoumi S, Guilhaumon F, Kark S, Terlizzi A, Claudet J, Felline S, Cerrano C et al (2016) Space invaders; biological invasions in marine conservation planning. Divers Distrib 22:1220–1231

    Article  Google Scholar 

  • Goldsmit J, Archambault P, Chust G, Villarino E, Liu G, Lukovich JV, Barber DG et al (2018) Projecting present and future habitat suitability of ship-mediated aquatic invasive species in the Canadian Arctic. Biol Invasions 20:501–517

    Article  Google Scholar 

  • Gosselin LA, Qian PY (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282

    Article  Google Scholar 

  • Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391

    Article  Google Scholar 

  • Gray JS, Wu RSS, Or YY (2002) Effects of hypoxia and organic enrichment on the coastal marine environment RID B-4203-2010. Mar Ecol-Prog Ser 238:249–279

    Article  Google Scholar 

  • Hansen FT, Christensen A, Gabellini AP (2020). Ranking of Danish ports according to shipping activities and to the potential of natural dispersal of nonindigenous species. DTU Aqua. DTU Aqua-rapport No. 369–2020

  • IPBES (2019) Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services

  • Katsanevakis S, Wallentinus I, Zenetos A, Leppäkoski E, Çinar ME, Oztürk B, Grabowski M et al (2014) Impacts of invasive alien marine species on ecosystem services and biodiversity: a pan-European review. Aquat Invasions 9:391–423

    Article  Google Scholar 

  • Keddy PA (1992) Assembly and response rules: two goals for predictive community ecology. J Veg Sci 3:157–164

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Leppäkoski E, Gollasch S, Gruszka P, Ojaveer H, Olenin S, Panov V (2002) The Baltic - A sea of invaders. Can J Fish Aquat Sci 59:1175–1188

    Article  Google Scholar 

  • Li Y, Shen Z (2020) Roles of dispersal limit and environmental filtering in shaping the spatiotemporal patterns of invasive alien plant diversity in China. Front Ecol Evol 8:1–14

    Article  Google Scholar 

  • Lindegren M, Diekmann R, Möllmann C (2010) Regime shifts, resilience and recovery of a cod stock. Mar Ecol Prog Ser 402:239–253

    Article  Google Scholar 

  • Lindegren M, Vigliano P, Nilsson PA (2012a) Alien Invasions and the Game of Hide and Seek in Patagonia. PLoS ONE 7:e44350–e44350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindegren M, Blenckner T, Stenseth NC (2012b) Nutrient reduction and climate change cause a potential shift from pelagic to benthic pathways in a eutrophic marine ecosystem. Glob Change Biol 18:3491–3503

    Article  Google Scholar 

  • Lindegren M, Thomas MK, Jónasdóttir SH, Nielsen TG, Munk P (2020) Environmental niche separation promotes coexistence among ecologically similar zooplankton species—North Sea copepods as a case study. Limnol Oceanogr 65:545–556

    Article  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Norberg A, Abrego N, Blanchet FG, Adler FR, Anderson BJ, Anttila J, Araújo MB et al (2019) A comprehensive evaluation of predictive performance of 33 species distribution models at species and community levels. Ecol Monogr 89:1–24

    Article  Google Scholar 

  • Ojaveer H, Jaanus A, Mackenzie BR, Martin G, Olenin S, Radziejewska T, Telesh I et al (2010) Status of biodiversity in the Baltic sea. PLoS ONE 5:1–19

    Article  CAS  Google Scholar 

  • Ovaskainen O, Tikhonov G, Norberg A, Guillaume Blanchet F, Duan L, Dunson D, Roslin T et al (2017) How to make more out of community data? a conceptual framework and its implementation as models and software. Ecol Lett 20:561–576

    Article  PubMed  Google Scholar 

  • Paavola M, Olenin S, Leppäkoski E (2005) Are invasive species most successful in habitats of low native species richness across European brackish water seas? Estuarine Coastal Shelf Sciences 64:738–750

    Article  Google Scholar 

  • Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser 177:269–297

    Article  Google Scholar 

  • Pecuchet L, Törnroos A, Lindegren M (2016) Patterns and drivers of fish community assembly in a large marine ecosystem. Mar Ecol Prog Ser 546:239–248

    Article  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Radinger J, Alcaraz-Hernández JD, García-Berthou E (2019) Environmental filtering governs the spatial distribution of alien fishes in a large, human-impacted Mediterranean river. Divers Distrib 25:701–714

    Article  Google Scholar 

  • Richardson DM, Pyšek P (2012) Naturalization of introduced plants: ecological drivers of biogeographical patterns. New Phytol 196:383–396

    Article  PubMed  Google Scholar 

  • Rosenberg R, Hellman B, Johansson B (1991) Hypoxic Tolerance of Marine Benthic Fauna. Marine Ecol-Progress Series 79:127–131

    Article  Google Scholar 

  • Rosenberg R, Agrenius S, Hellman B, Nilsson HC, Norling K (2002) Recovery of marine benthic habitats and fauna in a Swedish fjord following improved oxygen conditions. Mar Ecol Prog Ser 234:43–53

    Article  Google Scholar 

  • Shinen JS, Morgan SG (2009) Mechanisms of invasion resistance: competition among intertidal mussels promotes establishment of invasive species and displacement of native species. Mar Ecol Prog Ser 383:187–197

    Article  Google Scholar 

  • Stubbs WJ, Wilson JB (2004) Evidence for limiting similarity in a sand dune community. J Ecol 92:557–567

    Article  Google Scholar 

  • Svendsen LM, van der Bijl L, Boutrup S, Norup B (eds) NOVANA. Nationwide Monitoring and Assessment Programme for the Aquatic and Terrestrial: NERI Technical Report No. 532. Prog Descrip, National Environmental Research Institute, Denmark

  • Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273

    Article  PubMed  Google Scholar 

  • Tikhonov G, Opedal ØH, Abrego N, Lehikoinen A, de Jonge MMJ, Oksanen J, Ovaskainen O (2020) Joint species distribution modelling with the r-package Hmsc. Methods Ecol Evol 11:442–447

    Article  PubMed  PubMed Central  Google Scholar 

  • Tittensor DP, Walpole M, Hill SLL et al (2014) A mid-term analysis of progress toward international biodiversity targets. Science 346:241–244

  • Vitusek PM, DAntonio CM, Loope LL, Westbrooks R (1996) Biological Invasions as Global Environmental Change. Am Sci 84:468–478

  • Wood, S. N. 2017. Generalized additive models: an introduction with R, 2nd ed. Chapman and Hall/CRC.

Download references

Acknowledgements

This project was funded by the Danish Maritime Fund by request of the Danish Environmental Protection Agency (DEPA). We wish to thank all people involved in the NOVANA program for ensuring availability and accessibility to high-quality monitoring data. We also wish to thank three anonymous reviewers for constructive criticism and feedback received during peer review.

Funding

This project was funded by the Danish Maritime Fund by request of the Danish Environmental Protection Agency (DEPA). The authors declare they have no financial interests.

Author information

Authors and Affiliations

  1. Centre for Ocean Life, National Institute of Aquatic Resources, Technical University of Denmark, Kemitorvet, Building 202, 2800 Kgs, Lyngby, Denmark

    Martin Lindegren

  2. National Institute of Aquatic Resources, Technical University of Denmark, Kemitorvet, Building 202, 2800 Kgs, Lyngby, Denmark

    Martin Lindegren, Aurelia Pereira Gabellini, Peter Munk, Karen Edelvang & Flemming Thorbjørn Hansen

Authors
  1. Martin Lindegren
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aurelia Pereira Gabellini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter Munk
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karen Edelvang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Flemming Thorbjørn Hansen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

FH and ML designed the study. FH and APG performed drift model simulations. APG performed data extraction. ML performed data processing and statistical analysis. ML drafted a first version of the ms. All authors took part in assessing and discussing results, as well as editing and revising the ms.

Corresponding author

Correspondence to Martin Lindegren.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2909 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lindegren, M., Gabellini, A.P., Munk, P. et al. Identifying key processes and drivers affecting the presence of non-indigenous marine species in coastal waters. Biol Invasions 24, 2835–2850 (2022). https://doi.org/10.1007/s10530-022-02802-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-022-02802-w

Keywords

Search

Navigation