Skip to main content

Advertisement

Log in

A hazardous place to live: spatial and temporal patterns of species introduction in a hot spot of biological invasions

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

Abstract

Globally, the spread of non-indigenous species in marine ecosystems is a major ecological and socio-economical concern. The need for long-term assessment on a large scale is a pre-requisite for understanding the drivers associated with their establishment and expansion. Here, the patterns of invasions of subtidal soft-bottom assemblages of shelled molluscs have been quantified based on a unique dataset collected between 2005 and 2012 along the coast of Israel (SE Mediterranean Sea), a hotspot of bioinvasion. Overall, the number of non-indigenous species doubled between 2005 and 2012. Significant differences in terms of species richness and relative abundance were observed in space and time in both native and non-indigenous species. A combination of enduring disturbance regimes related to human activities and site-specific environmental conditions seem to have a critical role in promoting the observed patterns. Our results emphasize the value of long term broad-scale systematic surveys to the development of effective environmental policies for the control of bioinvasions.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson MJ (2001) Permutation tests for univariate or multivariate analysis of variance and regression. Can J Fish Aquat Sci 58:626–639

    Article  Google Scholar 

  • Anderson MJ, Robinson J (2003) Generalized discriminant analysis based on distances. Aust N Z J Stat 45:301–318

    Article  Google Scholar 

  • Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525

    Article  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA + for primer: guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • Bogi C, Galil BS (2007) First record of Theora (Endopleura) lubrica Gould, 1861 (Mollusca: Bivalvia: Semelidae) from a Levantine port. Aquat Invasions 2(1):77–79

    Article  Google Scholar 

  • Boudouresque CF, Meinesz A, Ribera MA, Ballesteros E (1995) Spread of the green alga Caulerpa taxifolia (Caulerpales, Chlorophyta) in the Mediterranean: possible consequences of a major ecological event. Sci Mar 59:21–29

    Google Scholar 

  • Brigden K, Stringer R (2002) A critical assessment of the Kishon River Masterplan Report published by the State of Israel Ministry of Environment, July 2001. http://www.greenpeace.to/publications/Kishon%20Haifa%202002.pdf

  • Carlton J (1996) Biological invasions and cryptogenic species. Ecology 77:1653–1655

    Article  Google Scholar 

  • Catford JA, Vesk PA, Richardson DM, Pyšek P (2012) Quantifying levels of biological invasion: towards the objective classification of invaded and invasible ecosystems. Glob Change Biol 18:44–62

    Article  Google Scholar 

  • Clarke KR, Ainsworth M (1993) A method of linking multivariate community structure to environmental variables. Mar Ecol Prog Ser 92:205–219

    Article  Google Scholar 

  • Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279(5350):555–558

    Article  CAS  PubMed  Google Scholar 

  • Convention on Biological Diversity (2015) Aichi biodiversity targets. https://www.cbd.int/sp/targets/. Accessed 6 November 2015

  • Crooks JA, Chang AL, Ruiz GM (2011) Aquatic pollution increase the relative success of invasive species. Biol Invasions 13:165–176

    Article  Google Scholar 

  • Dafforn KA, Glasby TM, Johnston EL (2009) Links between estuarine condition and spatial distributions of marine invaders. Divers Distrib 15:807–821

    Article  Google Scholar 

  • Dafforn KA, Kelaher BP, Simpson SL, Coleman MA, Hutchings PA, Clark GF, Knott NA, Doblin MA, Johnston EL (2013) Polychaete richness and abundance enhanced in anthropogenically modified estuaries despite high concentrations of toxic contaminants. PLoS ONE 8(9):e77018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emery KO, Neev D (1960) Mediterranean beaches of Israel. Israel Geol Surv Bull 26:1–23

    Google Scholar 

  • Essl F, Bacher S, Blackburn TM, Booy O, Brundu G, Brunel S, Cardoso AC, Eschen R, Gallardo B, Galil B, García-Berthou E, Genovesi P, Groom Q, Harrower C, Hulme PE, Katsanevakis S, Kenis M, Kühn I, Kumschick S, Martinou AF, Nentwig W, O’Flynn C, Pagad S, Pergl J, Pyšek P, Rabitsch W, Richardson DM, Roques A, Roy HE, Scalera R, Schindler S, Seebens H, Vanderhoeven S, Vilà M, Wilson JRU, Zenetos A, Jeschke JM (2015) Crossing frontiers in tackling pathways of biological invasions. Bioscience 65:769–782

    Article  Google Scholar 

  • European Commission (EC) (2008) Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Off J Europ Un L164:19–40

    Google Scholar 

  • European Commission (EC) (2010) Commission decision of 1 September 2010 on criteria and methodological standards on good environmental status of marine waters. 2010/477/EU. Off J Europ Un 232:14–24

    Google Scholar 

  • European Commission (EC) (2011) Communication from the Commission to the European Parliament, the Council, the Economic and Social Committee and the Committee of the Regions—Our Life Insurance, Our Natural Capital: an EU Biodiversity Strategy to 2020. COM 2011:244

    Google Scholar 

  • European Commission (EC) (2014) Regulation (EU) No 1143/2014 of the European Parliament and of the Council of 22 October 2014 on the prevention and management of the introduction and spread of invasive alien species. Off J Europ Un 317:35–55

    Google Scholar 

  • Fischer P (1865) Note sur les faunes conchyliologiques des deux rivages de l’isthme de Suez. J Conchyl 13:241–248

    Google Scholar 

  • Fischer P (1870) Sur la faune conchyliologique marine des baies de Suez et de l’Akabah. J Conchyl 18:161–179

    Google Scholar 

  • Fischer P (1871) Sur la faune conchyliologique marine de la baie de Suez. J Conchyl 19:209–226

    Google Scholar 

  • Forrest BM, Gardner JPA, Taylor MD (2009) Internal borders for managing invasive marine species. J Appl Ecol 46:46–54

    Article  Google Scholar 

  • Francour P, Harmelin-Vivien M, Harmelin JG, Duclerc J (1995) Impact of Caulerpa taxifolia colonization on the littoral icthyofauna of North-Western Mediterranean Sea—Preliminary results. Hydrobiologia 300:345–353

    Article  Google Scholar 

  • Galil BS (2007) Seeing red–marine alien species along the Mediterranean coast of Israel. Aquat Invasions 2:281–312

    Article  Google Scholar 

  • Galil BS (2008) Alien species in the Mediterranean Sea—which, when, where, why? Hydrobiologia 606:105–116

    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(2–3):152–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galil BS, Marchini A, Occhipinti-Ambrogi A (2016) East is East and west is west? Management of marine bioinvasions in the Mediterranean Sea. Estuar Coast Shelf Sci. Available online 5 January, 2016

  • Gravili C, Bevilacqua S, Terlizzi A, Boero F (2015) Missing species among Mediterranean non-Siphonophoran Hydrozoa. Biodivers Conserv 24:1329–1357

    Article  PubMed  PubMed Central  Google Scholar 

  • Haas G (1948) Sue l’immigration de mollusques indo-pacifiques dans les eaux cotières de la Palestine. J Conchyl 88:141–144

    Google Scholar 

  • Harmelin-Vivien M, Francour P, Harmelin JG (1999) Impact of Caulerpa taxifolia on Mediterranean fish assemblages: a six year study. In: Proceedings of the workshop on invasive Caulerpa in the Mediterranean. MAP technical Reports Series. UNEP, Athens, pp 127–138

  • Herut B, Cohen Y, Shefer E, Gordon N, Galil B, Tibor G, Tom M (2006) Environmental quality of Israel’s Mediterranean coastal waters in 2005, IOLR Report H25/2006. [in Hebrew]

  • Herut B, Shefer E, Gordon N, Galil B, Lubinevsky H, Tibor G, Tom M, Rilov G, Silverman J, Rinkevich B (2014) The national monitoring program of Israel’s Mediterranean coastal waters—scientific report for 2012, IOLR Report H62/2013 [in Hebrew]

  • Hornung H (1989) Metal levels in some benthic organisms of Haifa Bay, Mediterranean (Israel). Toxicol Environ Chem 20(1):255–260

    Article  Google Scholar 

  • Hornung H, Krumgalz BS, Cohen Y (1984a) Mercury pollution in sediments, benthic organisms and inshore fishes of Haifa Bay, Israel. Mar Environ Res 12(3):191–208

    Article  CAS  Google Scholar 

  • Hornung H, Barash A, Danin Z (1984b) Note on the ecology of Mollusca collected in Haifa Bay (Israel). Centro (Msida) 1(1):41–48

    Google Scholar 

  • Kennedy TA, Naemm S, Howe KM, Knops JMH, Tilman D, Reich P (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638

    Article  CAS  PubMed  Google Scholar 

  • Kress N, Herut B (1998) Hypernutrification in the oligotrophic eastern Mediterranean: a study in Haifa Bay (Israel). Estuar Coast Shelf Sci 46:645–656

    Article  CAS  Google Scholar 

  • Lenz M, da Gama BAP, Gerner NV, Gobin J, Gröner F, Harry A, Jenkins SR, Kraufvelin P, Mummelthei C, Sareyka J, Xavier EA, Wahl M (2011) Non-native marine invertebrates are more tolerant towards environmental stress than taxonomically related native species: results from a globally replicated study. Environ Res 111:943–952

    Article  CAS  PubMed  Google Scholar 

  • Levi F, Francour P (2004) Behavioural response of Mullus surmuletus to habitat modification by the invasive macroalga Caulerpa taxifolia. J Fish Biol 64:55–64

    Article  Google Scholar 

  • Lewin R (1983) Origin of species in stressed environments. Science 222:1112

    Article  CAS  PubMed  Google Scholar 

  • MacIsaac HJ, Tedla R, Ricciardi A (2010) Patterns and rate of growth of studies in invasion ecology. In: Richardson DM (ed.) 50 years of invasion ecology, pp 51–60

  • Mazor T, Possingham HP, Edelist D, Brokovich E, Kark S (2014) The crowded sea: incorporating multiple marine activities in conservation plans can significantly alter spatial priorities. PLoS ONE 9(8):e104489

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller AW, Ruiz GM (2009) Differentiating successful and failed invaders: species pools and the importance of defining vector, source and recipient regions. In: Rilov G, Crooks J (eds) Biological invasions in marine ecosystems: ecological, management, and geographic perspectives. Springer, Berlin, pp 153–170

    Chapter  Google Scholar 

  • Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ojaveer H, Galil BS, Campbell ML, Carlton JT, Canning-Clode J, Cook EJ, Davidson AD, Hewitt CL, Jelmert A, Marchini A, McKenzie CH, Minchin D, Occhipinti-Ambrogi A, Olenin S, Ruiz G (2015) Classification of non-indigenous species based on their impacts: considerations for application in marine management. PLoS Biol 13(4):e1002130

    Article  PubMed  PubMed Central  Google Scholar 

  • Perkins LB, Leger EA, Novak RS (2011) Invasion triangle: an organizational framework for species invasion. Ecol Evol 1:610–625

    Article  PubMed  PubMed Central  Google Scholar 

  • Piola RF, Johnston EL (2008) Pollution reduces native diversity and increases invader dominance in marine hard substrate communities. Divers Distrib 14:329–342

    Article  Google Scholar 

  • Portman ME, Shabtay-Yanai A, Zanzuri A (2016) Incorporation of socio-economic features’ ranking in multicriteria analysis based on ecosystem services for marine protected area planning. PLoS ONE 11(5):e0154473

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Ruiz GM, Fofonoff P, Hines AH (1999) Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnol Oceanogr 44:950–972

    Article  Google Scholar 

  • Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annu Rev Ecol Syst 31:481–531

    Article  Google Scholar 

  • Ruiz GM, Fofonoff PW, Steves B, Foss SF, Shiba SN (2011) Marine invasion history and vector analysis of California: a hotspot for western North America. Divers Distrib 17:362–373

    Article  Google Scholar 

  • Sala E, Kizilkaya Z, Yildirim D, Ballesteros E (2011) Alien marine fishes deplete algal biomass in the eastern Mediterranean. PLoS ONE 6(2):e17356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seebens H, Gastner MT, Blasius B (2013) The risk of marine bioinvasion caused by global shipping. Ecol Lett 16:782–790

    Article  CAS  PubMed  Google Scholar 

  • Shefer E, Silverman J, Herut B (2015) Trace metal bioaccumulation in Israeli Mediterranean coastal marine mollusks. Quatern Int 390:44–55

    Article  Google Scholar 

  • Simberloff D (2005) Non-native species do threaten the natural environment! J Agric Environ Ethics 18:595–607

    Article  Google Scholar 

  • Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P, Sousa R, Tabacchi E, Vila M (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66

    Article  PubMed  Google Scholar 

  • Stachowicz JJ, Byrnes JE (2006) Species diversity, invasion success, and ecosystem functioning: disentangling the influence of resource competition, facilitation, and extrinsic factors. Mar Ecol Progr Ser 311:251–262

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamburello L, Maggi E, Benedetti-Cecchi L, Bellistri G, Rattray AJ, Ravaglioli C, Rindi L, Roberts J, Bulleri F (2015) Variation in the impact of non-native seaweeds along gradients of habitat degradation: a meta-analysis and an experimental test. Oikos 124:1–11

    Article  Google Scholar 

  • Thomas Y, Pouvreau S, Alunno-Bruscia M, Barillé L, Gohin F, Bryère P, Gernez P (2016) Global change and climate-driven invasion of the pacific oyster (Crassostrea gigas) along European coasts: a bioenergetics modelling approach. J Biogeogr 43:568–579

    Article  Google Scholar 

  • UNEP (United Nations Enviornment Programme) (2016a) Integrated monitoring and assessment programme of the Mediterranean Sea and coast and related assessment criteria. UNEP(DEPI)/MED IG.22/28 (Decision IG.22/7). http://www.unepmap.org/index.php?module=library&mode=doc&action=results&s_final=1

  • UNEP (United Nations Enviornment Programme) (2016b) Updated Action Plans Concerning “Cetaceans, Coralligenous and Other Calcareous Bio-concretions, and Species Introductions and Invasive Species; Mandate for update of the “Action Plan on Marine and Coastal Birds” and revision of the “Reference List of Marine and Coastal Habitat Types in the Mediterranean. UNEP(DEPI)/MED IG.22/28 (Decision IG.22/12). http://www.unepmap.org/index.php?module=library&mode=doc&action=results&s_final=1

  • Vaillant L (1865) Recherches sur la faune malacologique de la baie de Suez. J Conchyl 13:97–127

    Google Scholar 

  • Vergés A, Tomas F, Cebrian E, Ballesteros E, Kizilkaya Z, Dendrinos P, Karamanlidis AA, Spiegel D, Sala E (2014) Tropical rabbitfish and the deforestation of a warming temperate sea. J Ecol 102:1518–1527

    Article  Google Scholar 

  • Verlaque M, Fritayre P (1994) Mediterranean algal communities are changing in the face of the invasive alga Caulerpa taxifolia (Vahl) C Agardh. Oceanol Acta 17:659–672

    Google Scholar 

  • Von Holle B, Simberloff D (2005) Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology 86:3212–3218

    Article  Google Scholar 

  • Winer BJ, Brown DR, Michels KM (1991) Statistical principles in experimental design. McGraw-Hill, New York

    Google Scholar 

Download references

Acknowledgements

We are grateful to the anonymous reviewers for their perceptive and helpful comments on an earlier version of the manuscript. The authors thank Dr. Isaac Gertman and Mr. Yaron Gretner, Israel Oceanographic and Limnological Research, and Mr. Rami Klinger, Israel Ports Development & Assets, for sharing with us valuable information. Funding for the monitoring the environmental quality of Israel’s Mediterranean coastal waters was provided by the Ministry of Environment. RITMARE Flagship Project funded by the Italian Ministry of University and Research, the European Community’s 7th Framework Programmes (FP7/2007–2013) for the project COCONET (Grant Agreement No. 287844, http://www.coconet-fp7.eu/), the European Union’s Horizon 2020 for the project MERCES (Grant Agreement No. 689518, http://www.merces-project.eu) are also acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Giuseppe Guarnieri.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1149 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guarnieri, G., Fraschetti, S., Bogi, C. et al. A hazardous place to live: spatial and temporal patterns of species introduction in a hot spot of biological invasions. Biol Invasions 19, 2277–2290 (2017). https://doi.org/10.1007/s10530-017-1441-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-017-1441-1

Keywords

Navigation