Pathways of introduction of marine non-indigenous species

Indicator definition

This indicator shows trends of marine non-indigenous species per pathway of introduction recorded in European seas since 1950. Analysis is shown at both European and regional sea level.

Units

Number of non-indigenous species 

Policy context and targets

Context description

The EU Biodiversity Strategy (EU, 2011) specifically stresses the need to assess pathways of biological invasions through its Target 5: "By 2020, invasive alien species and their pathways are identified and prioritised, priority species are controlled or eradicated, and pathways are managed to prevent the introduction and establishment of new invasive alien species".

The recently adopted European Commission Regulation on the prevention and management of the introduction and spread of invasive alien species determines that Member States carry out a comprehensive analysis of the pathways of unintentional introduction and spread of invasive alien species of EU concern. This should be carried out, at least, in their territory as well as in their marine waters as defined in Article 3(1) of Directive 2008/56/EC. Member States should also identify the pathways that require priority action ('priority pathways'), because of the volume of species or of the potential damage caused by the species entering the EU through them. They will also need to establish and implement action plans to address the priority pathways identified within three years of the initial assessment.

Other international agreements cover different groups of marine alien species or their pathways of introduction and start to address them as a threat to biodiversity:

1. It has been recognised that aquaculture and related activities (e.g. sport fishing, fishery stock enhancement, ornamental trade) have been important drivers of alien species in Europe in the past and that the trade in alien species needs specific rules in order to prevent the introduction of target and non-target species into the wild. In 2007, the first EC regulation on alien species was approved: No. 708 on 11 June 2007 (implemented by rules: No. 535 on 13 June 2008) concerning the use of alien and locally absent species in aquaculture.

2. The International Maritime Organisation (IMO) adopted the "International Convention for the Control and Management of Ships' Ballast Water and Sediments". The aim of the Convention is to prevent, minimise and ultimately eliminate the transfer of harmful aquatic organisms and pathogens through the control and management of ships' ballast water and sediments.

3. The Convention for the Control and Management of Ship’s Ballast Water and Sediments under the International Maritime Organisation addresses ballast water as the main pathway for MAS.

4. The Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES) adopted a resolution on IAS during COP13 (and reviewed at COP14) (resolution 13.10, trade in alien invasive species).

Targets

The EU Biodiversity Strategy (EU, 2011) specifically stresses the need to assess pathways of biological invasions through its Target 5: “By 2020, invasive alien species and their pathways are identified and prioritised, priority species are controlled or eradicated, and pathways are managed to prevent the introduction and establishment of new invasive alien species”.

The MSFD aims to reach Good Environmental Status (GES) of the marine environment by 2020. Descriptor 2 addresses marine alien species and is defined as “Non-indigenous species introduced by human activities are at levels that do not adversely alter the ecosystem".

Related policy documents

• AFS, 2001. International Convention on the Control of Harmful Anti-Fouling Systems on Ships.
  International Maritime Organization, London. 2001.
• COM(2008) 789 Final
  Communication from the Commission to the Council, the European Parliament, the European Economic and Social Committee and the Committee of the Regions Towards an EU Strategy on Invasive Species [SEC(2008) 2887 Et SEC(2008) 2886
• Council of Europe (2003). European strategy on invasive alien species. Convention on the Conservation of European Wildlife and Natural Habitats (Bern Convention).
  Council of Europe, T-PVS (2003) 7 revised: 60 pp.
• Decision VI/23 on Alien Species that threaten ecosystems, habitats and species.
  (COPVI, The Hague, April 2002) to which are annexed the Guiding Principles for the Prevention, Introduction and Mitigation of Impacts of Alien Species that threaten Ecosystems, Habitats or Species.
• EC (2013). Proposal for a regulation of the European Parliament and of the Council on the prevention and management of the introduction and spread of invasive alien species
  COM(2013) 620 final 9.9.13, 46pp
• European Commission (2006). Proposal for a Council Regulation concerning use of alien and locally absent species in aquaculture.
  COM(2006) 154 final: 32 pp.
• IMO (1997). International Maritime Organisation, Guidelines for the Control and Management of Ships’ Ballast Water to Minimise the Transfer of Harmful Aquatic Organisms and Pathogens.
  IMO Resolution A.868 (29). IMO, London.
• IMO (2004). International Convention for the Control and Management of Ships’ Ballast Water and Sediments.
  IMO, London.

Methodology

Methodology for indicator calculation

The list of species used is the same as that considered for the trends in introduction analysis (MAR002) and stored in the HCMR/EEA data base. It includes both alien and cryptogenic species. Information on the country, year of first introduction of each species and pathway(s) is publicly available through the species search widgets of EASIN updated as of October 2013 (http://easin.jrc.ec.europa.eu/use-easin/species-search) and is also provided in the supplementary file of Nunes et al. (2014) http://www.aquaticinvasions.net/2014/Supplements/AI_2014_Nunes_etal_Supplement.xls. The HCMR/EEA data base is in full agreement with the classification given in EASIN, yet updated to June 2014.

Trends in introduction per pathway were calculated on a decadal basis, considering the very first sighting/collection of the species in European Waters. In the absence of an exact collection date, the date of publication was used as the best available information. All species, both established and casual, were taken into account.

The primary pathway/vector was filled in to the degree possible. Marine and estuarine species are those aquatic species that do not complete their entire life cycle in freshwater (modified after ICES, 2005). Vagrant species, mostly fish and crustaceans of tropical Atlantic origin, whose mode of introduction is unknown, were not considered in the calculations. Thus, the pathway was calculated for 1 416 species.

To categorise pathways of primary introduction of alien species into a new region, we have followed the framework proposed by Katsanevakis et al (2013).

Five pathways are associated with human activity either as commodities (release and escape), contaminants of commodities, stowaways on modes of transport and opportunists exploiting corridors resulting from transport infrastructures. The sixth category highlights alien species that may arrive unaided in a region as a result of natural spread (rather than human transport), following a primary human-mediated introduction in a neighbouring region.

Aquaculture: Historically, aquaculture and stock transfers of aquatic species resulted in a significant amount of taxa being transported worldwide. Of the species imported for mariculture, it is not known how many have been intentionally released for stocking. This is a practice for introduced species in inland waters not considered in this analysis. So, this category is not analysed here. However, we have included those imported species that have escaped from aquaculture and spread in the wild under the category ‘aquaculture escape’, even if they are released freshwater species if found in estuarine areas of the Baltic Sea. The so called aquaculture contaminants are hereby assigned as ‘aquaculture accidentally introduced’ species.

Shipping: With regard to NIS, stowaways include organisms that foul the hulls of ships, are transported as seeds or resting stages in ballast water, as well as in shipping containers and cargo. Estimates reveal that more than 480 000 annual ship movements occur worldwide with the potential for transporting organisms. Various calculations have been made on the amount of ballast water carried with the world’s fleet of merchant ships – it has been estimated that 2–12 billion tonnes of ballast water are transported annually. In ballast tanks and other ship vectors including hulls, anchor chains and sea chests, ships may carry 4 000 to 7 000 taxa each day (Gollasch, 1996). Under shipping we have also included species transferred by recreational boats, mostly encountered in marinas, and species transferred by fishing boats.

Given the IMO Policies on Ballasts after 2004 (BWC), it was deemed important to examine the trends in the two different modes of introduction (ballasts and fouling) separately.

Under Corridors, we have separated those species progressively introduced via the Suez Canal (mostly Indo-Pacific species occurring in the eastern Mediterranean, also called Lessepsian immigrants) and those Ponto-Caspian species spreading in the Baltic via inland canals.

A final category is aquarium trade. The recent focus on the aquarium trade as a possible mechanism for environmentally sustainable development poses an especially dangerous threat (Papavlassopoulou et al, 2014), although this has so far escaped the attention of most environmentalists, conservationists, ecologists, and policy makers.

When investigating gateways of introduction in European Seas, the country and year of initial introduction of marine alien species in Europe were identified (for 1 380 species in Nunes et al 2014). The country through which a species was first introduced in Europe will hereafter be called ‘recipient country’. For 31 species, more than one recipient country was associated with their introduction into European Seas. This may happen when a species has been collected independently in the same year from different countries, such as, for example Desdemona ornata (Banse, 1957) from Italy (Lardicci and Castelli 1986) and Greece (Panagopoulos and Nicolaidou 1989-90), Fibrocapsa japonica (Toriumi and Takano, 1973) from France (Billard 1992) and Germany (Elbrächter 1994) or Hemigrapsus sanguineus (De Haan, 1835) from France and the Netherlands (Breton et al. 2002). 

Given these potential multiple pathway of introduction at Pan-European level, the percentages add to more than 100% (i.e. 116.3%) as some species are linked to more than one pathway. Temporal trends in the numbers of newly recorded marine alien species in Europe are given in relation to the pathways of introduction. Some species that were linked to more than one pathway were given a value of 1/k, for each of the k associated pathways, so that the overall contribution of each species to the total number of new aliens per decade was always one (Katsanevakis et al, 2013).

Methodology for gap filling

Unless species are found when deliberately moved, evidence of their actual transmission is seldom known.

Information on vectors is mostly derived from expert judgement on an extensive review of the referred databases, since specific research projects aimed at identifying vectors and occurrences are complicated and demand large resources. The only exception is published reports issued on maritime traffic worldwide (BWM, 2005). In a large number of cases, likely pathways are merely inferred, for example taking into account the most common activity occurring in a specific location (shipping, aquaculture), but no scientific evidence is provided.

Vertebrate pathways tend to be characterised as deliberate releases, exempting the Lessepsian immigrants that arrived unintentionally via the Suez Canal, invertebrates were introduced mostly as contaminants and plants as escapees. Pathogenic microorganisms and fungi are generally introduced as contaminants of their hosts.

Methodology references

• BWM (2005) International Convention on the control and management of ship’s ballast water and sediments. International Maritime Organization, London.
• Calado R., 2006. Marine ornamental species in European Waters: a valuable overlooked resource or a future threat for the conservation of marine ecosystems? Scientia Marina, 70,3: 389-398
• Hulme et al., 2008. Grasping at the routes of biological invasions: a framework for integrating pathways into policy Journal of Applied Ecology, 45: 403–414
• Gollasch S., Galil B.S. & Cohen A.N., 2006. Bridging Divides: Maritime Canals as Invasion Corridors. Springer, Dordrecht, the Netherlands.
• Galil B.S., Nehring S. & Panov V.E., 2007. Waterways as invasion highways: impact of climate change and globalization. Biological Invasions (ed. W. Nentwig), pp. 59–74. Ecological Studies No. 193. Springer, Berlin, Germany.
• Gollasch S., 2002. The importance of ship fouling as a vector of species introductions into the North Sea. Biofouling, 18: 105–121.
• Garcia-Berthou E., Alcaraz C., Pou-Rovira Q., Zamora L., Coenders G. & Feo C., 2005. Introduction pathways and establishment rates of invasive aquatic species in Europe. Canadian Journal of Fisheries and Aquatic Sciences, 62: 453–463.
• ICES (2005). Vector pathways and the spread of exotic species in the sea. D. Minchin, S. Gollasch and I. Wallentinus (Eds). ICES Cooperative Research Report, No. 271, pp. 25
• Katsanevakis S, Zenetos A,Belchior C,Cardoso AC., 2013. Invading European seas: assessing pathways of introduction of marine aliens. Ocean and Coastal Management, 76: 64–74.
• Minchin D., 2004. Aquatic transport and the spread of aquatic species: challenges for management. In: Davenport J and Davenport JL (eds) The effects of human transport on ecosystems: cars and planes, boats and trains, 244-265. Dublin: Royal Irish Academy
• Minchin D., 2006. The transport and spread of living aquatic species. In: Davenport J and Davenport JD (eds) The Ecology of Transportation: Managing Mobility for the Environment. pp 77-97. Springer, The Netherlands.
• Minchin D., 2007. Aquaculture and transport in a changing environment: Overlap and links in the spread of alien biota. Marine Pollution Bulletin, 55: 302–313
• Molnar JL, Gamboa RL, Revenga C, Spalding MD, 2008. Assessing the global threat of invasive species to marine biodiversity. Front. Ecol. Environ. 6(9): 458-492.
• Nunes AL., Katsanevakis S., Zenetos A. & Cardoso AC. (2014). Gateways to alien Invasions in the European Seas Aquatic Invasions, 9,2: 133–144
• Savini D., Occhipinti–Ambrogi A., Marchini A., Tricarico E, Gherardi F., Olenin S., Gollasch S., 2010. The top 27 animal alien species introduced into Europe for aquaculture and related activities. Journal of Applied Ichthyology. Special Issue: Alien Species in Aquaculture and Fisheries, 26(2): 1–7.
• Wolff W.J. & Reise K., 2002. Oyster imports as a vector for the introduction of alien species into northern and western European waters. -In : Leppäkoski, E., Gollasch, S. & Olenin, S. (eds): Invasive aquatic species of Europe. Distribution, impacts and management.Kluwer, Dordrecht, pp. 193-204.
• Papavlasopoulou I., Vardakas L., Perdikaris C., Kommatas D. Paschos I. (2014). Ornamental fish in pet stores in Greece: a threat to biodiversity? Mediterranean Marine Science, 15 (1)126-134. 

Uncertainties

Methodology uncertainty

In many cases, it is impossible to identify the introduction vector. Thus the pathway of 100 species is assigned as ‘unknown’. In bivalves, for example, introductions may be attributed to larval transport in ballast water releases, adults in hull fouling of ships or imports of stock for aquaculture purposes, or for direct human consumption but released into the environment

For species that are most frequently associated with hull fouling, this form of transport was assumed to be the responsible vector. For planktonic taxa and microscopic resting stages ballast water has been deemed to be the most likely vector since such species that are associated with hull fouling might be expected to become flushed away during ship journeys at sea. Human activities near to the site of the first records are generally assumed to be responsible for an introduction event. However, such deductions are not always secure and, for this reason, more than one vector has been calculated where the likely vector remains unclear. Forty species of tropical Atlantic origin have recently entered the Mediterranean via Gibraltar. These are classified as ‘vagrant’ and ‘range expansion’ and are not included in the pathway analysis.

Where more than one pathway of introduction is suspected/documented, the analysis has considered both modes of introduction. Thus, the resulting percentage of contribution per pathway amounts to more than 100%. 

Data sets uncertainty

See rationale uncertainty

Rationale uncertainty

Different levels of certainty are associated with alien species that become introduced. A scheme proposed by Dan Minchin (2007), provides a basis for an improved quality of information for pathways and vectors.

(1) There is direct information of a pathway/vector: The species was clearly associated to a specific vector(s) of a pathway at the time of introduction to a particular locality. This is the case in intentional introductions (i.e. aquaculture/commodity) and in many cases of Lessepsian immigrants (when there was direct evidence of a gradual expansion along the Suez Canal and then in the localities around the exit of the Canal in the Mediterranean).

(2) Almost likely pathway/vector can be inferred: The species appears for the first time in a locality where a single pathway/vector(s) is known to operate and there is no other rational explanation for its presence except by this pathway/vector(s). This applies to many species introduced by shipping or aquarium trade or as aquaculture contaminants. In some cases a specific vector could not be inferred, e.g. some species probably introduced by shipping could not be further linked to ballasts or hull fouling and were classified as ‘shipping/unknown’. In many cases, inference is based on known examples of introductions elsewhere for the same or similar species, the biology and ecology of the species, the habitats and locales it occupies in both the native and introduced range, and its pattern of dispersal (if known), e.g. for a fouling species frequently recorded in ports, shipping has been assumed to be the most probable vector.

(3) One or more possible pathways/vectors can be inferred: The species cannot be convincingly ascribed to a single pathway/vector. Inference is based on the activities in the locality where the species was found and may include evidence on similarly behaving species reported elsewhere.

(4) Unknown: Where there is doubt as to any specific pathway explaining an arrival. Herein, the pathway of 100 species has been assigned as ´unknown´.

References

Gruet, Y., Heral, M., Robert, J.-M., 1976. Premie`res observations sur l’introduction de la faune associe΄e au naissain d’huı tres Japonaises Crassostrea gigas (Thunberg), importe΄ sur la coˆ te Atlantique FrancΈaise. Cahiers de Biologie Marine 17, 173–184.

Hare, J.A., Whitfield, P.E., 2003. An integrated assessment of the introduction of lionfish (Pterois volitans/miles complex) to the Western Atlantic Ocean. NOAA Technical memorandum NOS NCCOS 2, 21

McMahon, R.F., 1983. Ecology of an invasive pest bivalve, Corbicula. In: The Mollusca, Vol. 6. Academic Press, pp. 505–553.

Minchin D., 2007. Aquaculture and transport in a changing environment: Overlap and links in the spread of alien biota. Marine Pollution Bulletin 55 (2007) 302–313

Lilly, E.L., Kulis, D.M., Gentien, P. & Anderson, D.M. (2002) Paralytic shellfish poisoning toxins in France linked to human-induced strain of Alexandrium catanella from the western Pacific: evidence from DNA and toxin analysis. Journal of Plankton Research, 24, 443–452.

Ruiz, G.M. & Carlton, J.T. (2003) Invasive Species: Vectors and Management Strategies. Island Press, Washington, DC.