Marine biosecurity: protecting indigenous marine species
Authors Cook E, Payne R, Macleod A, Brown S
Received 28 March 2015
Accepted for publication 18 September 2015
Published 13 January 2016 Volume 2016:5 Pages 1—14
Checked for plagiarism Yes
Review by Single-blind
Peer reviewer comments 2
Editor who approved publication: Dr David Lane
Elizabeth J Cook,1 Robin D Payne,2 Adrian K Macleod,3 Sarah F Brown4
1Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll, 2Alyth, Perthshire, 3Scottish Association for Marine Science Research Services Limited, Scottish Marine Institute, Oban, Argyll, 4Firth of Clyde Forum, Glasgow, UK
Abstract: Nonindigenous species (NIS) are those that have been intentionally or unintentionally introduced outside of their native range as a consequence of human activity. If these species then threaten indigenous species and biodiversity, and/or cause economic damage, they are referred to as “invasive.” Biological invasions are not only one of the greatest threats to indigenous marine biodiversity, but they can also cause massive economic and ecological damage. Their presence could also lead to a water body failing to achieve good environmental status under the forthcoming EU Marine Strategy Framework Directive. As the rate of invasion to Great Britain and European waters continues to increase, particularly in light of climate change, the emphasis by member states is on prevention rather than on control or eradication an NIS once an invasive NIS has become established. This paper reviews NIS biosecurity planning for the marine environment, including the most current legislative background, pathway identification and highlights the main issues with the current risk assessment processes. The potential impacts of marine NIS, practical biosecurity measures from Great Britain and internationally are also reviewed. The aim of this paper is to draw attention to the challenges associated with preventing the introduction of marine NIS and to highlight the urgent need for concerted action across the EU member states and marine industries to produce robust biosecurity plans to protect indigenous species.
Keywords: biosecurity, marine, non-indigenous invasive species, planning, indigenous, protection
Nonindigenous species (NIS) are those that have been intentionally or unintentionally introduced outside their native range, as a consequence either directly or indirectly of human activity.1 Once established, if these species then threaten biodiversity and/or cause economic damage, they are referred to as “invasive”.1,2 Biological invasions are not only one of the greatest threats to marine indigenous biodiversity,3 second only to habitat destruction,2 but they can also cause massive economic and ecological damage.4,5 Increased international trade has caused an exponential increase in the spread of NIS around the world over the last few decades,6,7 and this trend has been observed in Great Britain (GB).8,9
The estimated cost of NIS to the economy in GB is £1.7 billion a year.10 The annual cost of “marine-based” industries (eg, shipping and aquaculture in GB) is estimated to be £39.9 million, although this is probably an underestimate, as there is little distinction made between native and NIS during pest control operations.10
More than 90 NIS have been identified from British and Irish (including Republic of Ireland and Northern Ireland) marine and brackish environments.8,11 Their arrival has been principally due to shipping, including ballast waters and sediments, fouling of hulls and other associated hard structures, and imported consignments of cultured species.8 The majority of marine NIS in GB originate from the North Pacific, followed by the Northwest Atlantic.8 Many are initially reported from the sites of anthropogenic activity, such as ports, marinas, and aquaculture facilities, particularly in the English Channel, with a number subsequently spreading north to the North or Celtic Seas.8 In addition, many marine species have naturally extended their native range with increasing sea water temperature,11 however, this review is primarily aimed at NIS introduced through human activity.
Biosecurity plans are critical in providing a framework to reduce the risk of the introduction of marine NIS. The International Maritime Organization (IMO) recognized this importance and produced in 2011, a biofouling management plan and record book for the shipping industry.12 At a national level, for example, the GB Non-Native Species Framework Strategy,13 the new Invasive Alien Species Strategy for Northern Ireland14 and the Scottish Government Code of Practice on Non-Native Species,15 typically follow a three-stage approach including i) prevention, ii) rapid response, iii) control and containment. At a regional level, this approach has been adopted in Scotland, for example, in the production of biosecurity plans by the Firth of Clyde Forum16 and the Solway Firth Partnership.17 Biosecurity plans for NIS are also under development in Orkney for ballast water management18 and the Shetland Isles.19 However, a few examples of how biosecurity planning can be practically implemented by maritime industries at the site or operation level in Europe. The biosecurity planning guidance for preventing the introduction of disease for finfish farmers/traders and shellfish producers is being a notable example.20,21 By contrast, in New Zealand and Australia, their biosecurity measures for marine NIS are better developed and have been far more integrated with plant and animal health, placing a strong emphasis on border control (ie, prevention) and rapid response. These and other international examples of practical guidelines of how to minimize the introduction and spread of NIS, however, need to be understood for a wider variety of maritime activities before the biosecurity of indigenous species can be achieved.
This review provides an overview of biosecurity planning for the marine environment, including the most current legislative background, pathway identification, and risk assessment processes. The potential impacts of marine NIS are reviewed, together with the examples of practical biosecurity measures that have been used to control or eradicate these species. UK and international experience, including the successes and failures of biosecurity planning has also been explored in some detail, including plans developed for freshwater and terrestrial environments.
Why do we need biosecurity plans to protect our marine indigenous species?
The unintentional introduction of species to a region outside their normal range is widely recognized as a major threat to indigenous species diversity,22 arising from habitat modification, changes in ecosystem functioning, additional disease and parasitic introductions, and genetic impacts, such as hybridization with native species.23
The accidental or intentional introduction of NIS can cause significant changes to ecosystems.24 For example, the Pacific oyster, Crassostrea gigas, was intentionally introduced for aquaculture purposes in the US and Europe in 1928 and 1950s, respectively. This oyster naturally recruits to uncultivated regions in certain areas and can form dense intertidal hummocks of shell and live oysters.25 This species has been found to substantially reengineer a habitat to provide additional structures for other species, however, it can also cause significant changes to sediment porosity, bioturbation activity, and biogeochemical cycling.24 The Mediterranean mussel, Mytilus galloprovincialis, was also accidentally introduced to South Africa in the late 1970s. This species is now the dominant intertidal mussel on the west coast, where it has considerably modified the natural community composition.26 The carpet sea squirt, Didemnum vexillum, has been shown to have a negative impact on species diversity and abundance on the Georges Bank, northeast US27 and in the Netherlands.28 Lengyel et al27 found that the number of benthic macrofauna significantly declined with an increase in the abundance of D. vexillum and that benthic species composition was significantly altered after the appearance of this species on the Georges Bank. In the Netherlands, species diversity also decreased significantly, following the rapid increase in D. vexillum colonies, which can locally cover >95% of the hard bottom in the regions of Oosterschelde and Grevelingen.28
Ecosystem services are a set of ecosystem functions, many of which are critical to human survival (eg, climate regulation, air purification, and nutrient recycling).29 Ecosystem functioning is intrinsically linked to biodiversity and thus, changes in biodiversity can cause significant changes to the functioning of a particular environment or system. For example, Levin et al30 showed that an invasion by the NIS Spartina hybrid in the US, caused a shift in the system from an algae based to a predominantly detritus-based system. Furthermore, it changed the hydrodynamic regime in the estuary, which led to reduced survivorship of key species that supported higher trophic levels, such as migratory shorebirds.30 In addition, the lionfish, Pterois volitans, and Pterois miles were most likely introduced to Florida coastal waters in the mid 1980s by either releases or escapes from marine aquaria.31 Pterois volitans has dramatically expanded its range in the last 30 years, throughout the Caribbean, Gulf of Mexico, and as far south as Brazil.32 These species are highly efficient predators and their rapid increase in abundance in the Bahamas coincided with a 65% decline in the biomass of native prey species over 2 years, raising concern that this will have a serious deleterious impact on the structure and function of reef communities.33 Consequently, P. volitans has been recognized as one of the main species for conservation concern.34
Disease and parasite introduction
There are many cases of intentional movements of stock introducing NIS, including parasites and disease. For example, the trematode, Gyrodactylus salaris, was transported with Atlantic salmon, Salmo salar, from Swedish hatcheries to Norway and resulted in serious salmon mortalities in the recipient region.35 The importation of the Japanese eel, Anguilla japonica, for cultivation trials in Europe also released a nematode, which has gone on to spread and to cause significant damage to other eel species, such as the native eel Anguilla anguilla.36 In addition, the copepods Mytilicola orientalis, a gut parasite of bivalves; and Myicola ostreae, a parasite that lives on the gills of the Pacific oyster, C. gigas, have both been found in Ireland,37 France,38 and the Netherlands.39
Genetic impacts can occur either through the selection or modification of specific genetic traits linked to performance between native and NIS species or through the inter-breeding of NIS escapees from aquaculture facilities with natural populations. In the case of the former, the Japanese Yesso scallop Patinopecten (Mizuhopecten) yessoensis was intentionally hybridized with the smaller native species Chlamys farreri in People’s Republic of China to improve growth performance.40,41 This can result in a significant fraction of genetic variation residing at a higher organizational level (among populations) in aquaculture species compared with natural populations, where all variation resides below the family level.42 Genetic complexes will develop with a population often relating to the environment in which the population resides. Aquaculture practices of both inbreeding and selection of individuals for specific traits, however, can magnify the development of these genetic complexes in a population.
Aquaculture (and potentially marine aquaria) escapees can also breed with natural populations. This hybridization and subsequent introgression can then lead to a breakdown of the genetic complexes, and forcing a reduced fitness in the hybrid individuals.43 For example, evidence has been found in the introgression of the Mediterranean mussel, M. galloprovincialis, genes into native Australian population.44
Legal drivers and legislative context
This section is not intended to be a comprehensive review of the complex set of acts, directives, and regulations covering NIS in the marine environment. Instead, it provides an example of the main UK legal and regulatory drivers, which although there is no explicit legal or regulatory requirement for maritime operators and developers to produce biosecurity plans for NIS, do consist of several existing laws and regulations that set a strong context for preparing and implementing these plans. These include; section 14 of the Wildlife and Countryside Act (2011) and the accompanying Code of Practice On NonNative Species,15 which have significantly strengthened the law, particularly in Scotland, where NIS legislation is now viewed as the most progressive in Europe.45 Specifically, the strengthening of the existing offense of releasing a nonnative animal from captivity and including two further offenses; allowing an animal to escape from captivity outwith its native range; and causing an animal to be in a place outwith its native range.
The Scottish offences in relation to NIS plants and animals are “strict liability offenses” so intention, recklessness, or negligence do not have to be proved. A legal defense that all reasonable steps were taken to prevent the offense and that all due diligence was exercised to avoid committing the offense that can be made. The Code of Practice on Non-native Species sets out in broad terms what “reasonable steps” mean in this context and the advice includes; adopting a precautionary approach and not carrying out operations that might lead to the spread of NIS until there is a clear understanding of the situation; carrying out risk assessments to understand the risk of spreading NIS, setting out how to avoid it happening; seeking advice and following good practice; and reporting the presence of NIS. Although the code stops short of specifying the need for a biosecurity plan, many of the main elements of this type of plan are set out as good practice.
The amended Scottish legislation also provides powers to relevant public bodies to enter into voluntary Species Control Agreements and, if an Species Control Agreement is refused, statutory Species Control Orders (SCOs).15 SCOs are intended for situations where a species has already been introduced and must specify which operations should be carried out, who is to carry them out and when they must be carried out. SCOs can, therefore, form a legal compulsion for two major elements of a biosecurity plan – rapid response and containment. SCOs and Emergency SCOs can operate on the “polluter pays” principle. If government agency staff or their contractors have to carry out the control and containment work, then the cost of this work can be recovered from the site operator.
The EU Marine Strategy Framework Directive46 and the Water Framework Directive47 set a wider strategic and operational context for preventing the spread of NIS and their control, which feeds down to the national and regional legislation, but do not act as direct drivers for the preparation of biosecurity plans. Unfortunately, the EU Regulation on Invasive Alien Species48 does not explicitly use the term “biosecurity” at any point. However, the components of the marine biosecurity planning (risk assessment, pathway recognition, pathway management, prevention, containment, early detection) are all mentioned and discussed. Member States are currently in the process of compiling an initial list of Species of Union Concern (SUC). Growing, breeding, selling, or intentionally releasing these species will be banned. Member States will also be able to list Invasive Alien Species of Member State Concern for similar bans.
Member states must also analyze the pathways of unintentional introduction and spread; identify “priority pathways” based on the volume or the impact of the species moved by that pathway and provide a pathway action plan with a timetable and measures to prevent the spread into or within the EU of the SUC. This plan will include awareness-raising measures, regulatory measures to minimize contamination and transport, border checks, and the existing ballast water conventions. At this stage, with no transposition to domestic law drafted, it is not easy to predict what impact this regulation will have in driving the need for biosecurity at the regional, site or operation level in the Member States.
In the UK, however, there are The Aquatic Animal Health (Scotland) Regulations 200949 and the equivalent Regulation for England and Wales, which implement the Council Directive 2006/88/EC50 on animal health requirements for aquaculture animals and products. These regulations require Aquaculture Production Businesses including shellfish and finfish farmers, as a condition of their authorization, to produce and implement a Biosecurity Measures Plan to restrict the spread of disease to their site(s) of operation. Although not intended to cover NIS, the plan preparation process, as well as, the actions and precautions specified by the plan for diseases, could potentially be expanded and used by other maritime industries, the aquarium trade and government agencies to prevent the introduction and spread of SUC.
Biosecurity – a survey of existing NIS plans
Biosecurity, as a term applied to NIS to describe measures to prevent their introduction and stop their spread, is still relatively new. Consequently, plans which have a range of titles including Invasive Species Action Plans, Non-Native Species Plans, Invasive Species Management Plans or Species Response Plans may well be, at least in part, biosecurity plans for NIS. These plans have been prepared in a variety of formats ranging from the more numerous countrywide strategic documents to the less frequent plans for small sites and individual operations (Table 1).20,21,51 National and catchment plan preparation has predominantly been driven by central government, environment agencies, and non-governmental organizations, hence the greater number of these plans compared with the site and operation level plans, where there is no regulatory requirement (apart from the aquaculture industry for disease) for their production. A range of biosecurity guidance and Codes of Practice do exist, however, but they typically lack a plan structure, sign-off, and accountability at an operational level, so there are no clear means to ensure that the guidance and codes are followed.
Table 1 Biosecurity plans for invasive nonindigenous species by category
There are some NIS plans that include “biosecurity” in their title. These plans generally include actions on the long-term, strategic control, and eradication of a well-established NIS rather than on preventative measures, which would usually be included in a biosecurity plan. As long-term strategic control and eradication are almost always technically impossible or not viable economically in the marine environment,52 it is critical to be aware though that preventative measures are a key component of any biosecurity planning process.
Pathway and vector identification
The need to understand the pathways (ie, route between the source region and the region of release) of invasion by NIS and the vectors (ie, specific means by which an invasive species moves within a particular pathway, for example, shipping (commercial and recreational), intentional stock, or aquarium trade movements) to prevent the introduction of NIS from one region to another is paramount in preparing a marine biosecurity plan. In the UK, a study found that the majority of NIS species introduced to British waters since 1850s originated from the North Pacific, particularly the north-west (eg, Asia and Japan) followed by the Northwest Atlantic (eg, east coast of the US).8 This result is consistent with the findings of previous studies,61,62 suggesting that NIS from regions with similar temperature regimes to the recipient region are more likely to become established and widespread, as species would be physiologically adapted to the environmental conditions experienced in these waters. Of course, there are always species that are able to tolerate a wide range of environmental conditions (eg, Zebra mussel Dreissena polymorpha and tubeworm Ficopomatus enigmaticus), enabling them to survive in conditions outside the conditions typically experienced in their native range.8
There are also a number of species where their introduction into British waters was likely to be a result of secondary spread, where a species is transferred from the initial point of introduction by various more localized vectors (eg, coastal or local shipping, fisheries, stock movements, or by natural mechanisms). For example, the Japanese skeleton shrimp Caprella mutica (Figure 1)63,64 and the non-indigenous bryozoan, Tricellaria inopinata,65 were first recorded in mainland Europe prior to their appearance in the UK and secondary spread via hull fouling and aquaculture activities is likely to have contributed to the rapid expansion of their distribution throughout the region.
Figure 1 The Japanese Skeleton Shrimp, Caprella mutica.
Major vectors currently identified for marine NIS include vessels (ballast water and hull fouling – particularly slow-moving vessels, such as barges, semi-submersible oil rigs, or vessels berthed in one place over long periods); aquaculture activities, including intentional stock transfer and unintentional introductions via escapes and hitchhikers;66–68 the aquarium trade69 and canals, such as the Suez Canal, which are a major conduit for the spread of alien species between separate biogeographical regions.70,71 In British waters, where only a single vector was identified, vessels and aquaculture activities were considered responsible for at least 47% and 30% of NIS introductions, respectively.8 Where the mode of arrival could have been via more than one vector, then vessels and aquaculture activities were still cited as major vectors along with other modes of transmission. The natural spread of NIS, can also be an important vector for the dispersal of certain species (eg, Japanese wireweed, Sargassum muticum) (Figure 2) 72,73 and nonindigenous plankton species, although this vector has received significantly less attention to date than ballast water and hull fouling, with the exception of monitoring for the nonindigenous phytoplankton, Karenia mikimotoi.74
Figure 2 The Japanese wireweed, Sargassum muticum.
The majority of studies to date have identified the high-risk pathways for a particular geographical region, rather than on a site or operational level, based on literature reviews and expert knowledge. A study identifying the high-risk pathways for the introduction and establishment of marine NIS across the UK and Ireland demonstrated the application of pathway analysis at this wider scale.62 It is critical, however, that the pathways and vectors are identified and prioritized, based on their potential for transferring NIS, at a site and operation level, so that the high-risk pathways can be reduced or intercepted to remove any NIS.
Risk is the likelihood of a harmful event (or impact) occurring, multiplied by the magnitude of the consequences if the event occurs (eg, economic loss, ecosystem damage etc).75 Conventional risk analysis typically involves three stages, which culminate in risk calculation and evaluation. Each stage includes measures of uncertainty in its results;
- Likelihood of introduction – Based on the intensity of pathways/vectors previously identified and previous knowledge on major pathways/vectors of introduction for particular groups of NIS, if known.
- Likelihood of establishment and spread – Based on environmental parameters and the suitability of available substrate in the recipient environment and natural and anthropogenic means of dispersal.
- Potential impacts – Based on the potential harm that the NIS could cause in the recipient environment.
Risk can be estimated using a variety of methods, from inexpensive qualitative assessments, which can produce subjective results to more expensive semi- and qualitative methods, which focus on specific routes or taxa with known harmful characteristics and require detailed information that does not always exist.76 The following sections highlight some of the problems experienced in performing these assessments.
Likelihood of introduction
The greatest “likelihood of introduction” or highest risk is typically where the vector has arrived from another ocean basin in the same hemisphere8 or from another port/aquaculture site where NIS have been previously identified.77,78 For example, in the case of the later, the movement of mussel “seed” from an area known to contain the slipper limpet Crepidula fornicata in the UK, resulted in the transfer of this nonnative limpet in to an important seabed lay mussel producing region of North Wales.79 A major issue with this, however, is the lack of baseline data throughout Europe to provide reliable evidence of the presence and distribution of NIS for this analysis.75 At present, only ten European ports out of 1,200 from 22 coastal Member States have been surveyed and most of these have been comprised of a single survey, which provides an insufficient basis for pathway-risk analysis.75
It has also been suggested that regions with experience large volumes of shipping movements (eg, cross-channel ferries, commercial, and recreational vessels) and importation of stock for aquaculture purposes, over many years, are likely to be high-risk sites for NIS introductions.8 However, a study of 16 large bays in the US, found that there was no relationship between the quantity and frequency of ballast water discharges from foreign vessels and the number of NIS.80 The volume of ballast water discharges was, therefore, not considered in a process of risk assessment for ballast water management75 and although not proven for hull fouling or aquaculture activities, it should be considered that even small quantities of NIS could result in a successful introduction.
Likelihood of establishment and subsequent spread
The greatest “likelihood of establishment and subsequent spread” of a NIS in a recipient environment will be predominantly based on the environmental characteristics (eg, temperature, salinity, etc) and the availability of suitable substrate at a site, if required, based on the premise that the species will be able to survive the voyage. If environmental conditions are similar to the donor region and suitable substrate is provided, then there is a greater likelihood that NIS will survive and become established.11,75 In previous risk assessments, based on “environmental matching”, a variety of environmental variables have been used,81–83 however, due to the general lack of baseline data and life history knowledge for many NIS, it was suggested that salinity is the most “straight forward” parameter to use in the process of risk analysis.75 For example, the likelihood of a marine NIS becoming established in a freshwater environment (<0.5 PSU) is highly unlikely. The likelihood of NIS surviving does increase, however, as the salinity increases, and it has been suggested that as salinity reaches 18 PSU, the likelihood of establishment will increase.75 For example, the Japanese skeleton shrimp, C. mutica, is typically found in fully marine environments (>30 PSU), but a 100% mortality was found at salinities below 16 PSU.84 There are exceptions though, particularly for brackish water species, such as the Zebra mussel, D. polymorpha,85 and species, such as the Chinese mitten crab, Eriocheir sinensis, which migrates from freshwater to marine to spawn and complete their life-cycle.86
The potential impact from NIS is considered to be greater if the species has already been shown to have had a deleterious effect on the environment, economy, human health, property, or resources in another region in which it has been introduced. If the impact has also been considered “severe”, then this species could be classified as “high impact”.75 For example, the slipper limpet, C. fornicata was classified in a risk assessment commissioned by the GB Non-Native Species Secretariat, as likely to have a “massive impact” both economically and environmentally, effecting fisheries and aquaculture, as well as, significantly modifying habitat and out-competing native species.87 The main issue, however, is that for many NIS across Europe, there is a distinct lack of understanding of their life history strategies and impacts on native species, thus considerably increasing the “uncertainty” in the process of risk assessment.88
Methods for understanding the risks of NIS introduction and establishment are becoming more refined all the time,66 as critical data gaps are filled via research and documented evidence. Earlier work assessing the risk of NIS in aquaculture at a European scale is a good example of this.67 However, with so many “unknowns” and the difficultly in determining the potential “harmfulness” of a particular species, it has been suggested that a precautionary approach must be adopted, treating all known and suspected NIS as potentially harmful and equally unwanted.89
One particular method of assessment, Hazard Analysis and Critical Control Point (HACCP) planning, however, has been produced that enables the production of biosecurity plans for specific activities and has been applied to managing the risk of spreading NIS between water bodies.90 HACCP was originally created for the food standard industry.90 This procedure takes each activity on a site or within a wider operation, looks at it in detail and breaks it down into a series of tasks. At the heart of HACCP is the precautionary principle, so the method of risk calculation, which follows as the next stage in the process, does not attempt to ascribe a value or rating to the severity or the potential impacts. The likelihood of invasion is considered, but the emphasis is not on the overall risk, but on developing control measures for each activity to prevent the spread of NIS and defining the Critical Control Points when they are best applied.
These control measures are actions that can be used to reduce the probability that NIS may be introduced to a new area. To ensure that such control measures are functioning as intended, it is important to attach a set of measurable prescribed ranges, limits, and/or criteria for control measures and detail corrective actions to use to safeguard against any mishaps.
The development of effective control measures, however, does require the pooling of resources from a number of sources. Perhaps the most important of these are informed personnel with the practical knowledge of the process involved in the activity, along with any constraints imposed. Knowledge of existing preventive measures required by law is also essential to include in control measures listed. A degree of specialized knowledge of potential nontarget species is also required. Such knowledge might include the range of certain conditions that undesirable species can tolerate. Applying this type of information to the control measures included as part of the biosecurity plan greatly strengthens its effectiveness. HACCP has already been used as the basis for pathogen biosecurity and NIS in mariculture.58 It could be simplified and combined with pathway management to become the basis for marine biosecurity planning at a site and operation level.
Contingency and rapid response plans
The need to be prepared to act if biosecurity measures for NIS fail has been widely acknowledged and should be included in biosecurity plans. Rapid response and contingency plans have been produced, drawing partly on experience from the response to pathogen threats, such as foot and mouth disease and avian influenza, and environmental threats such as oil spill planning. In practice, most rapid responses to the discovery of NIS are actions which get under way immediately and planning the activity only follows at a later stage if the process starts to stretch into the longer term.91–93
Practical marine biosecurity measures
Various practical measures have been undertaken to reduce the likelihood of a NIS being introduced or spreading from a site of introduction. These measures have predominantly used freshwater as either a preventative measure or as a control (ie, through washing of structures). However, aerial exposure, chemicals, smothering, and mechanical-based measures have also been used, depending on the particular activity.
The proximity of the site/operation to a freshwater source can significantly influence the likelihood of the successful establishment of a marine NIS. Studies have shown that many marine NIS have a broad tolerance to temperature, but will only tolerate a much smaller salinity range.94 For example, the Japanese skeleton shrimp, C. mutica, has been found to tolerate temperatures ranging from 2°C to 20°C, whereas high mortalities are experienced when salinities fall to 16 PSU.95 It is, therefore, likely that a large proportion of marine NIS associated with shipping (ie, transported either in ballast water or as hull fouling), will be excluded from sites with high freshwater input.95 In a survey of 88 UK marinas which contained NIS, high freshwater input into the marina basin was highlighted as a significant feature in reducing the likelihood of NIS establishment. More specifically marinas located within 20 m of a freshwater source had significantly fewer NIS than those sited over 1 km away.96
Removal and prevention of biofouling
NIS are highly opportunistic and robust, surviving for extended periods of time in the hostile environment of a ballast tank97 or out-competing native species in highly disturbed environments on a wide variety of artificial structures, as native species are often poorly adapted to the altered physical and biological environment both on and around these man-made objects.98 Ballast water, vessel hulls, floating pontoons, navigation buoys, fin- and shell-fish cultivation infrastructure are particularly prone to inoculation by NIS,99 as they all provide a unique habitat for a variety of reasons, including isolation from surrounding waters or seabed, novel materials (eg, plastics), and shading.100 The Japanese skeleton shrimp, C. mutica, for instance, occurs in exceptionally high densities on artificial structures such as pontoons and aquaculture infrastructures, which are raised from the seabed where they are able to avoid benthic predation pressure.95 The likelihood of the successful establishment of a NIS, therefore, would be significantly increased by a reduction in the duration of the passage time or the presence of artificial structures. Therefore, any design features or maintenance practices that prevent the survival of NIS in ballast water and the accumulation of bio-fouling or can remove fouling from these artificial structures, without causing unintentional dispersal of the NIS, would reduce the risk of NIS establishment and spread.45,52,101
Aerial exposure is a practical measure that has been shown to successfully remove biofouling, including NIS from a wide variety of artificial structures for many years.102 Novel designs, such as rotating pontoon floats are currently being trialed in North Wales, which would allow surfaces exposed above the water line to be air dried in sections for prolonged periods, thus killing the any fouling organisms attached to the floats.52 Locking pontoons are also in the conceptual phase. These could be “locked” at the top of high tide, exposing the underside of the pontoon surface to the air when the tide drops.52 In addition, modular structures, which can easily be removed for air drying would also provide a practical solution for reducing the risk of NIS establishment.
Artificial structures that can be removed from the water, such as vessels, pontoon floats, navigation buoys, and aquaculture infrastructure can be jet washed, preferably with fresh water to remove any biofouling. To minimize the likelihood of spreading NIS, any washing must be done in an appropriate enclosed area where there is no risk of runoff reaching the sea and that all debris is safely disposed of according to guidelines for biological waste. It is paramount that any washing is done on land and that the “in-water” cleaning of anything beyond a light algal coating on the structures is discouraged, as certain NIS damaged by physical abrasion may be induced to spawn, while others can survive being dislodged or broken into fragments.72,103,104
Chemical treatments, such as biocides, chlorine, ozone, hydrogen peroxide, chlorine dioxide, acetic acid, etc, have been used to directly and indirectly treat for NIS. For example, a “BioBullet” in which the biocide is encapsulated within a particle that is ingested by the NIS has been successful at eradicating the Zebra mussel D. polymorpha and the sea squirt D. vexillum105,106 from enclosed environments. Chemical treatments have also been used to indirectly eradicate NIS, either via addition to ballast water or by the spraying or dipping of aquaculture infrastructure and stock.107,108 Dipping seed mussels, coated with a nonnative sea squirt Didemnum spp., in a 0.5% solution of bleach for 2 minutes was a 100% effective method of treatment for the invasive sea squirt and it left the mussels relatively unaffected.107 Trials in New Zealand, also found that acetic acid sprayed over a colonial sea squirt, Eudistoma elongatum, was particularly effective at removing the sea squirt from oyster racks exposed at low tide. Spraying or immersion of infested structures with a saturated solution of hydrated lime (calcium hydroxide) or 5% acetic acid was also effective against the invasive solitary tunicate, Styela clava in Prince Edward Island, Canada, which grows in dense aggregations on mussel lines and oyster racks.108 The dipping of dredged oysters, and associated species, in saturated or strong salt solutions is also a cheap, safe, and effective treatment for nonnative sea squirts and the macroalga, Sargassum muticum without harming the oysters.109 The main drawback of using certain biocides, however, is their potential effect on nontarget organisms within the wider environment and, therefore, careful regulation of their use is required.108
Enclosure of artificial structures
For structures that are fixed to the seabed, or are unable to be removed from the water for logistical or other reasons, then enclosure with plastic film/bags has been shown to be effective at removing biofouling, including NIS.52,110 The enclosure technique prevents a supply of clean water to the biofouling and smothers it through lack of oxygen. A chemical accelerant has been found to be effective at reducing the application time, such as sodium hypochlorite, acetic acid, chlorine, or freshwater for the invasive carpet sea squirt D. vexillum.106,107,111 The freshwater method is considered particularly effective though, since it reduces any risk of spillage and effect on the environment.106 On a much larger scale, this enclosure technique is currently in the developmental phase for the pontoon floats of semi-submersible oil rigs and associated supply vessels in New Zealand.112
For sites, such as harbors, marinas, and canal systems, which have their own lock gates, then there have been examples where the gates have been closed to allow for the rapid isolation and eradication of NIS. For example, when a nonnative bivalve Mytilopsis sp. was identified in three Australian marinas, all the sites were quarantined by closing their lock gates and treated rapidly using chemicals, allowing the invasive species to be eradicated before it became established in a more open environment.92 This follows a similar procedure used to successfully eradicate fresh and brackish water NIS from enclosed bodies of water, such as flooded quarries, reservoirs, and cooling pipes.105,113 As illustrated by the £4.2 million project at Bury Marina, Wales, although it is a costly process, it is also possible to adapt existing enclosed harbors and marinas to have lock gates.114
Filtration is the most commonly used treatment for the removal of NIS from ballast water, and it can be accomplished during ballasting operations using a shipboard filtration system. The physical separation and removal of organisms can be undertaken either whilst loading ballast water or during the voyage. Cyclonic separation can also be used. Depending on the design and application, the hydrocyclones require less pump pressure than screen filters and allow separation of sediments and other suspended solids to approximately 20 μm.115 A combination of filtration and cyclonic separation have been shown to be over 90% effective at removing micro- and macro-zooplankton from the ballast water. However, phytoplankton removal was only 30% effective.116
Following the unintentional introduction of the slipper limpet, C. fornicata, to the Menai Strait, North Wales with seed mussels from a site in the English Channel in 2006, a successful eradication of this species was undertaken. This procedure involved; the removal of the mussel lay and as much of the associated material as practicable by dredgers, followed by the smothering of any remaining C. fornicata in the affected area, with a dense layer of mussels sourced from an unaffected area. As this species is unable to either burrow or reposition themselves once covered, it was highly unlikely that they would survive the smothering. Subsequent monitoring surveys have since found no sign of live limpets.91
The mussel industry in New Zealand has also found that the mechanical stripping, grading, and restocking process that occurs between 6 and 12 months in the growth cycle is sufficient to control the growth of fouling organisms, including invasive tunicates. Occasionally, this process has had to be repeated later on in the cycle if a NIS is particularly abundant, but farms are generally reluctant to do this due to cost and difficulties in getting the larger mussels to reattach securely to the lines (B Forrest, personal communication, 2013). In Ireland, the rope-grown mussel industry has also successfully conducted a removal program during the grading and harvesting process, when small quantities of the invasive sea squirt D. vexillum was found on the mussel ropes.106
Once the surfaces have been cleaned of fouling, paints are generally applied to vessel hulls and finfish aquaculture cage netting which contain antifouling biocides.117 These paints prevent the settlement and growth of fouling organisms through the continual leaching of biocides, predominantly heavy metals such as copper and zinc into the surrounding water.118 Although such antifouling paints have proven to be effective, factors such as paint age, damage, or areas left unpainted can significantly decrease their efficiency. Studies have shown that paint age can have a significant influence on biofouling communities, with older paint allowing the establishment of greater quantities of fouling.119 Unpainted surfaces, such as those that evade actual paint coverage, eg, regions covered by support frames whilst the vessel is in dry dock and niche areas such as the propeller shaft, may allow sufficient area to facilitate biofouling.120 In addition, minor failures (<0.5 cm wide) in the anti-fouling system, as a result of accidental damage during daily operations (eg, anchor damage, vessel groundings or minor collisions) can also lead to the rapid establishment of fouling species, including NIS on the unprotected areas.120 The application of anti-fouling paints to structures that are likely to remain in the water for extended periods of time, following manufacturers’, guidelines should be promoted by government agencies to reduce the likelihood of NIS establishment.
Continuous surveillance and monitoring
Continuous surveillance and monitoring for NIS will allow for the early identification of an introduction event at a particular location and to provide reliable baseline data on the presence and distribution of a particular species.75 This is vital, as the management options to eradicate or mitigate the impacts of NIS decreases over time as populations become established and spread.98 It has been found that within as little as 6 months between surveys, a new NIS can establish and rapidly colonize a site. 92
The standardization of sampling protocols, however, still needs to be improved between countries to enable the generation of reliable and comparable results.75 In Australia and New Zealand, extensive surveys have been completed since the early 2000s in both international and domestic ports, including plankton, sedentary encrusting and benthic species and mobile species following the protocols developed by the Australian Centre for Research on Introduced Marine Pest for baseline surveys of NIS in ports.121 These protocols have since been adopted by the IMO’s Global Ballast Water Management Programme and variations of this protocol have been applied to port surveys in many other countries.122 These surveys, however, are expensive and require expert taxonomic knowledge to complete. A cheaper, more targeted rapid assessment approach, in combination with a pre-survey literature review, has been used successfully for fouling NIS in marina surveys in the US,123 UK,124 and Ireland.125 This approach, however, still requires expertise in taxonomic identification.
In addition to monitoring the site itself, closely monitoring the pathways of introduction (ie, vessel and stock movements) is also crucial in preventing the introduction of NIS. The aquaculture industry, already has a requirement to log any stock movements to restrict the spread of disease,20,21 however this needs to be expanded to include NIS. The IMO voluntary guidelines for the control and management of ships’ biofouling also include the requirement for each commercial126 and recreational127 vessel and associated industries (ie, shipbuilders, ship repair yards etc) to complete a biofouling management plan and record book, detailing anti-fouling systems used, their maintenance and inspection history, plus any periods when the vessel has been laid up or inactive for extended periods of time. However, as these IMO guidelines are only voluntary, there is little evidence yet of their update by vessel owners.
In the meantime, one approach that has been developed for quarantine personnel in New Zealand was a ranking scale used to quantify hull fouling on recreational vessels entering from international waters.103 This enables staff with minimal taxonomic expertise and training in the approach, to distinguish from a brief visual inspection of the hull from the surface, between vessels that carry, no, sparse or extensive fouling on their hulls. The staff member can then allocate each vessel a rank of 0–5 on arrival and those with a fouling rank of >2 (ie, small patches of macrofouling), can then be subject to further biosecurity measures.103
Conclusion and future directions
Biosecurity is critical if the exponential increase in the spread of NIS around the world over the last few decades is to be tackled. National biosecurity plans have been produced by the UK and New Zealand, however, site-specific NIS plans are rare. With the introduction of new regulations and guidance in Scotland, a regulatory driver has been introduced for the first time to encourage maritime operators to produce their own biosecurity plans. It is crucial to encourage other countries to adopt a similar regulatory framework as Scotland to address the issue of NIS biosecurity.
The need to understand the pathways of invasion and the vectors which transport NIS from region to region, to be prepared to act rapidly if planned biosecurity measures fail and to undertake continuously monitoring, is also paramount in preparing a biosecurity plan and successfully preventing the introduction of NIS. The EU Regulation on Alien Invasive Species will enable Member States to critically evaluate pathways and vectors for a SUC, however, the impacts of many marine NIS are still either unknown or poorly understood leading to a high degree of uncertainty in the process of risk assessment. This can only, therefore, be addressed with further research on the environmental, as well as the socio-economic impacts that marine NIS may have on an introduced region.
Maritime operators can also undertake preventative measures to reduce the risk of NIS introduction, either through effective ballast water treatment and/or the prevention of biofouling accumulation on submerged structures. Increasing the efficacy of ballast water treatment to reduce filtration times, the development of novel in-water cleaning techniques, prolonging the effectiveness of anti-fouling systems on static and mobile structures and improving taxonomic expertise are all key challenges for the future.
The review team would like to express their thanks to the members of the Firth of Clyde Forum Steering Group, all the stakeholders who provided advice, information, case history materials and reports and the anonymous reviewer for their comments on the manuscript.
The authors report no conflicts of interest in this work.
Convention on Biological Diversity [database on the Internet]. Secretariat of the Convention on Biological Diversity. Rio de Janeiro, Brazil; 1992. Available from: http://www.biodiv.org. Accessed March 14, 2015.
Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E. Quantifying threats to imperiled species in the United States. Bioscience. 1998;48(8):607–615.
Molnar JL, Gamboa RL, Revenga C, Spalding MD. Assessing the global threat of invasive species to marine biodiversity. Front Ecol Env. 2008;6:485–492.
Vitousek PM, D’Antonio CM, Loope LL, Rejmanek M, Westbrooks R. Introduced species: a significant component of human-caused global change. N Z J Ecol. 1997;21(1):1–16.
Pimentel D, Zuniga R, Morrison D. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ. 2005;52(3):273–288.
Carlton JT. Global change and biological invasions in the oceans. In: Mooney HI, Hobbs R, editors. Impact of Global Change on Invasive Species, Covelo CA: Island Press; 2000:31–53.
Hulme PE. Trade, transport and trouble: managing invasive species pathways in an era of globalisation. J Appl Ecol. 2009;46:10–18.
Minchin D, Cook EJ, Clark PF. A list of alien brackish and marine British species. Aquat Invasions. 2013;8(1):3–19.
Roy HE, Bacon J, Beckmann B, et al. Non-Native Species in Great Britain: Establishment, Detection and Reporting to Inform Effective Decision Making. A Report to the UK Department of Environment, Fisheries and Rural Affairs, UK; 2012:110.
Williams F, Eschen R, Harris A, et al. The Economic Cost of Invasive Non-Native Species on Great Britain. Wallingford: Centre for Biosciences and Agriculture International; 2010.
Cook EJ, Jenkins S, Maggs C, et al. Impacts of Climate Change on Non-Native Species. UK: Marine Climate Change Impacts Partnership; Plymouth, UK:2013.
Marine Environment Protection Committee. Guidelines for the Control and Management of Ships’ Biofouling to Minimise the Transfer of Invasive Aquatic Species; International Maritime Organisation, London, UK:2011. Available from: http://www.imo.org/en/OurWork/Environment/Biofouling/Documents/RESOLUTION%20MEPC.207.pdf. Accessed April 22, 2015.
DEFRA. The Invasive Non-Native Species Framework Strategy for Great Britain. London: Department for Environment, Food and Rural Affairs; London, UK:2008. Available from: http://www.nonnativespecies.org/index.cfm?sectionid=55. Accessed January 15, 2015.
Department of the Environment Northern Ireland. An Invasive Alien Species Strategy for Northern Ireland. UK: Department of the Environment Northern Ireland; 2013. Available from: http://invasivespeciesireland.com/news/an-invasive-alien-species-strategy-for-northern-ireland/. Accessed January 15, 2015.
Scottish Government. Code of Practice on Non-Native Species – Made by the Scottish Ministers under section 14C of the Wildlife and Countryside Act 1981. Edinburgh, UK: Scottish Government; 2012. Available from: http://www.gov.scot/Publications/2012/08/7367. Accessed February 10, 2015.
Mills F. Firth of Clyde Biosecurity Plan 2012 – 2016. UK: Firth of Clyde Forum; Glasgow, UK:2012. Available from: http://clydeforum.com/attachments/biosecplan.pdf. Accessed January 12, 2015.
Solway Firth Partnership. Draft Biosecurity Plan – Marine Invasive Non-Native Species in the Solway. Dunfries, UK: Solway Firth Partnership; 2013. Available from: http://www.solwayfirthpartnership.co.uk/uploads/Marine%20Invasive%20Non-native%20Species/Marine%20INNS%20in%20Solway%202013.pdf. Accessed January 12, 2015.
Orkney Islands Council. Ballast Water Management Policy for Scapa Flow. Orkney, UK: Orkney Islands Council; 2014. Available from: http://www.orkneyharbours.com/pdfs/bwm/Ballast%20Water%20Management%20Policy%20for%20Scapa%20Flow%20April%202014.pdf. Accessed February 10, 2015.
Collin SB, MacIver K, Shucksmith R. A Biosecurity Plan for the Shetland Islands. Scalloway, Shetland Isles: NAFC Marine Centre; 2015. Available from: http://www.nafc.uhi.ac.uk/departments/marine-science-and-technology/BiosecurityPlan.pdf. Accessed May 23, 2015.
Cefas. Finfish Biosecurity Measures Plan – Guidance and Templates for Finfish Farmers and Traders. Weymouth, UK: Cefas; 2009. Available from: https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/278581/Finfish_biosecurity_measures_plan.pdf. Accessed February 15, 2015.
Cefas. Shellfish Biosecurity Measures Plan – Guidance and Templates for Shellfish Farmers. Weymouth, UK: Cefas; 2009. https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/278580/Shellfish_biosecurity_measures_plan.pdf. Accessed February 15, 2015.
Worm B, Barbier EB, Beaumont N, et al. Impacts of biodiversity loss on ocean ecosystem services. Science. 2006;314(5800):787–790.
Lovei GL. Biodiversity – global change through invasion. Nature. 1997;388(6643):627–628.
Ruesink JL, Feist BE, Harvey CJ, et al. Changes in productivity associated with four introduced species: ecosystem transformation of a ‘pristine’ estuary. Mar Ecol Prog Ser. 2006;311:203–215.
Herbert RJH, Roberts C, Humpreys J, Fletcher S. The Pacific Oyster (Crassostrea gigas) in the UK: Economic, Legal and Environmental Issues Associated with its Cultivation, Wild Establishment and Exploitation. London: Shellfish Association of Great Britain; 2012.
Robinson TB, Griffiths CL, McQuaid C, Rius M. Marine alien species of South Africa – status and impacts. Afr J Mar Sci. 2005;27(1):297–306.
Lengyel NL, Collie JS, Valentine PC. The invasive colonial ascidian Didemnum vexillum on Georges Bank – ecological effects and genetic identification. Aquat Invasions. 2009;4:143–152.
Gittenberger A. Recent population expeansion of non-native ascidians in The Netherlands. J Exp Mar Biol Ecol. 2007;342:122–126.
Kremen C. Managing ecosystem services: what do we need to know about their ecology? Ecol Lett. 2005;8(5):468–479.
Levin AL, Neira C, Grosholz ED. Invasive cordgrass modifies wetland trophic function. Ecology. 2006;87:419–432.
Semmens BX, Buhle ER, Salomon AK, Pattengill-Semmens CV. A hotspot of non-native marine fishes: evidence for the aquarium trade as an invasion pathway. Mar Ecol Prog Ser. 2004;266:239–244.
Ferreira CEL, Luiz OJ, Floeter SR, et al. First record of invasive Lionfish (Pterois volitans) for the Brazilian coast. PLoS One. 2015;10(4).
Green SJ, Akins JL, Maljkovic A, Cote IM. Invasive lionfish drive atlantic coral reef fish declines. PLoS One. 2012;7(3).
Sutherland WJ, Clout M, Côté IM, et al. A horizon scan of global conservation issues for 2010. Trends Ecol Evol. 2010;25:1–7.
Johnsen BO, Jensen AJ. The Gyrodactylus story in Norway. Aquaculture. 1991;98:289–302.
Kennedy CR, Fitch DJ. Colonisation, larval survival and epidemiology of the nematode Anguillicola crassus, parasite in the eel Anguilla anguilla in Britain. J Fish Biol. 1990;36:117–131.
Holmes JMC, Minchin D. Two exotic copepods imported into Ireland with the Pacific oyster Crassostrea gigas (Thunberg). Ir Nat J. 1995;25:17–20.
Goulletquer P, Bachelet G, Sauriau PG, Noel P. Open Atlantic coast of Europe – a century of introduced species into French waters. In: Leppäkoski E, Gollasch S, Olenin S, editors. Invasive Aquatic Species of Europe Distribution, Impacts and Management. Dordrecht, Boston and London: Kluwer Academic Publishers; 2002:276–290.
Wolff WJ. Non-indigenous marine and estuarine species in The Netherlands. Zool Med Leiden. 2005;79:1–116.
Yang AG, Wang QY, Liu ZH, Zhou LQ. The hybrid between the scallops Chlamys farreri and Patinopecten yessoensis and the inheritance characteristics of its first filial generation. Mar Fish Res. 2004; 25(5):1–5.
Yu RH, Bao ZM, Wang ZP, et al. Hybridization of Clamys farreri and Patinopecten yessoensis. J Ocean Univ Chin. 2006;36(1):85–88.
Youngson AF, Dosdatz A, Saroglia M, Jorda WC. Genetic interactions between marine finfish species in European aquaculture and wild conspecifics. J Appl Ichthyol. 2001;17:153–162.
Skaala O, Wennevik V, Glover KA. Evidence of temporal genetic change in wild Atlantic salmon, Salmo salar L., populations affected by farm escapees. ICES J Mar Sci. 2006;63(7):1224–1233.
Sanjuan A, Zapata C, Alvarez G. Genetic differentiation in Mytilus galloprovincialis Lmk throughout the world. Ophelia. 1997;47:13–31.
Payne RD, Cook EJ, Macleod A. Marine Biosecurity Planning – Guidance for Producing Site and Operation-Based Plans for Preventing the Introduction of Non-Native Species. Scottish Natural Heritage, Perth, UK: 2014. Available from: http://www.snh.gov.uk/docs/A1294630.pdf. Accessed March 3, 2015.
Marine Strategy Framework Directive. European Union; Secretariat to the Council of the European Union, Brussels, Belgium:2008. Available from: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2008:164:0019:0040:EN:PDF. Accessed March 5, 2015.
Water Framework Directive. European Union; Secretariat to the Council of the European Union, Brussels, Belgium:2000. Available from: http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32000L0060&from=EN. Accessed March 5, 2015.
Regulation on the prevention and management of the introduction and spread of invasive alien species. EU: 2014. Available from: http://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32014R1143&from=EN. Accessed March 5, 2015.
Aquatic Animal Health (Scotland) Regulations. UK: 2009. Available from: http://www.legislation.gov.uk/ssi/2009/85/contents/made. Accessed March 10, 2015.
Council Directive on animal heath requirements for aquaculture animals and products 2006/88/EC. EU: 2006. Available from: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2006:328:0014:0056:en:PDF. Accessed March 10, 2015.
Ciria. Invasive Species Management for Infrastructure Managers and the Construction Industry. London, UK: Ciria; 2008.
Holt RHF, Cordingley AP. Eradication of the Non-Native Carpet Ascidian (Sea Squirt) Didemnum Vexillum in Holyhead Harbour: Progress, Methods and Results to Spring 2011. A Report to the Countryside Council for Wales, UK; 2011:104.
GB Non-Native Species Secretariat. The Invasive Non-Native Species Framework Strategy for Great Britain. GB Non-Native Species Secretariat; York, UK:2008. Available from: http://www.nonnativespecies.org/index.cfm?sectionid=55. Accessed January 15, 2015.
Ministry for Primary Industries. Management Action Plan – Biosecurity Response Preparedness Implementation Plan for Recommendations Following Exercise Taurus. Wellington: Ministry for Primary Industries; Wellington, NZ:2012. Available from: http://www.biosecurity.govt.nz/files/pests/foot-n-mouth/mpi-ex-taurus-2012-preparedness-management-action-plan.pdf. Accessed March 27, 2015.
Shine CA. Toolkit for Developing Legal and Institutional Frameworks for Invasive Alien Species. Nairobi: Global Invasive Species Programme; 2008.
Ward AI, Stebbing P, Jeffery K. Bio-Security in the Marine and Freshwater Environment. A Report to FERA and CEFAS, UK; 2013:135.
OGP/IPIECA. Alien invasive Species and the Oil and Gas Industry – Guidance for Prevention and Management. London, UK: OGP/IPIECA; 2010. Available from: http://www.ogp.org.uk/pubs/436.pdf. Accessed April 22, 2015.
Kelly J, Maguire CM. Marine Aquaculture Code of Practice. Invasive Species Ireland; Belfast, Northern Ireland:2009. Available from: http://invasivespeciesireland.com/wp-content/uploads/2010/07/Marina_Operators_CoP-.pdf. Accessed February 25, 2015.
Cumbria Freshwater Invasive Non-Native Species Initiative. Event Biosecurity Support Pack. Ulverston, Cumbria, UK:2013. Available from: https://www.facebook.com/cfinns. Accessed January 12, 2015.
Anon. Asian Hornet Response Plan. Fera, York, UK: Anon; 2012. Available from: www.nationalbeeunit.com/downloadDocument.cfm?id=675. Accessed February 27, 2015.
Eno NC, Clark RA, Sanderson WG. Non-Native Marine Species in British Waters: a Review and Directory. Peterborough: Joint Nature Conservation Committee; 1997.
Minchin D, Eno C. Exotics of coastal and inland waters of Ireland and Britain. In: Leppäkoski E, Gollasch S, Olenin S, editors. Invasive Aquatic Species of Europe: Distribution, Impact and Management. Dordrecht: Kluwer; 2002:267–275.
Ashton GV, Stevens MI, Hart MC, et al. Mitochondrial DNA reveals multiple Northern Hemisphere introductions of Caprella mutica (Crustacea, Amphipoda). Mol Ecol. 2008;17(5):1293–1303.
Cook EJ, Jahnke M, Kerckhof F, et al. European expansion of the introduced amphipod Caprella mutica Schurin 1935. Aquat Invasions. 2007;2(4):411–421.
Cook EJ, Stehlikova J, Beveridge CM, et al. Distribution of the invasive bryozoan Tricellaria inopinata in Scotland and a review of its European expansion. Aquat Invasions. 2013;8(3):281–288.
Carlton JT, Geller JB. Ecological roulette: the global transport of nonindigenous marine organisms. Science. 1993;261:78–82.
Mooney HA, Cleland EE. The evolutionary impact of invasive species. Proc Natl Acad Sci U S A. 2001;98:5446–5451.
Streftaris N, Zenetos A, Papathanassiou E. Globalisation in marine ecosystems: the story of non-indigenous marine species across European seas. Oceanogr Mar Biol Annu Rev. 2005;43:419–453.
Padilla DK, Williams SL. Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Front Ecol Env. 2004;2:131–138.
Galil BS. A sea under siege- alien species in the Mediterranean. Biol Invasions. 2000;2:177–786.
Galil BS, Boero F, Campbell ML, et al. Double trouble’: the expansion of the Suez Canal and marine bioinvasions in the Mediterranean Sea. Biol Invasions. 2015;17:973–976.
Harries DB, Cook EJ, Harrow S, et al. The establishment of the invasive alga Sargassum muticum on the west coast of Scotland: Rapid northwards spread and identification of potential new areas for colonisation. Aquat Invasions. 2007;2(4):367–377.
Giesler RJ. The Establishment and Spread of the Invasive Wireweed, Sargassum Muticum in the Isle of Man. A Report to the Isle of Man Government, UK; 2013;29.
Davidson K, Miller P, Wilding T, et al. A large and prolonged bloom of Karenia mikimotoi in Scottish waters in 2006. Harmful Algae. 2009;8(2):349–361.
David M, Gollasch S, Leppakoski E. Risk assessment for exemptions from ballast water management – The Baltic Sea case study. Mar Pollut Bull. 2013;75:205–217.
Hilliard R. Best Practice for the Management of Introduced Marine Pests – A Review. Australia: 2005. Available from: http://www.issg.org/pdf/publications/GISP/Guidelines_Toolkits_BestPractice/Hilliard_2005.pdf. Accessed January 23, 2015.
ICES. Report of the Working Group on Introductions and Transfers of Marine Organisms. Copenhagen, Denmark: International Council for the Exploration of the Sea; 2005. Available from: http://www.ices.dk/reports/ACME/2005/WGITMO05.pdf. Accessed January 18, 2015.
Minchin D, Gollasch S, Wallentinus I, editors. Vector Pathways and the Spread of Exotic Species in the Sea. Copenhagen: International Council for the Exploration of the Sea; 2005.
Sewell J, Pearce S, Bishop J, Evans JL. Investigations to Determine the Potential Risk for Certain Non-Native Species to be Introduced to North Wales with Mussel Seed Dredged from Wild Seed Beds. A Report to the Countryside Council for Wales, UK; 2008:82.
Ruiz GM, Fofonnoff PW, Ashton G, Minton MS, Miller AW. Geographic variation in marine invasions among large esturaries: effects of ships and time. Ecol Appl. 2013;23(2):311–320.
Chan FT, Bailey SA, Wiley CJ, MasIssac HJ. Predictive relative risk assessment for ballast-mediated invasions at Canadian Arctic Ports. Biol Invasions. 2013;15(2):295–308.
Gollasch S, Leppakoski E. Initial risk assessment of alien species in Nordic Coastal Waters. A Report to the Nordic Council of Ministers, Copenhagen, Denmark; 1999:244.
Keller RP, Drake JM, Drew MB, Lodge DM. Linking environmental conditions and ship movements to estimate invasive species transport across the global shipping network. Divers Distrib. 2011;17:93–102.
Ashton GV, Willis KJ, Burrows MT, Cook EJ. Environmental tolerance of Caprella mutica: implications for its distribution as a marine non-native species. Mar Environ Res. 2007;64(3):305–312.
Carlton JT. Dispersal mechanisms of the Zebra Mussel (Dreissena polymorpha). In: Nalepa TF, Schloesser DW, editors. Zebra Mussels: Biology, Impacts and Control. Michigan: Lewis Publishers; 1993:677–697.
Clark PF, Rainbow PS, Robbins RS, et al. The alien Chinese mitten crab Eriocheir sinensis (Crustacea: Decapoda: Brachyura), in the Thames catchment. J Mar Biol Assoc UK. 1998;78:1215–1221.
Sewell J, Sweet N. GB Non-native Organism Risk Assessment for Crepidula fornicata. GB Non-native species secretariat, York, UK; 2011. Available from: http://www.nonnativespecies.org. Accessed February 27, 2015.
Ojaveer H, Galil BS, Campbell ML, et al. Classification of non-indigenous species based on their impacts: the marine perspective. PLoS Biol. 2015;13(4).
Hewitt CL, Hayes KM. Risk assessment of marine biological invasions. In: Leppäkoski E, Gollasch S, Olenin S, editors. Invasive Aquatic Species of Europe: Distribution, Impacts and Management. Dordrecht: Kluwer Academic; 2002:456–466.
Britton D, Heimowitz P, Pasko S, Patterson M, Thompson J. HACCP Hazard Analysis and Critical Control Point Planning to Prevent the Spread of Invasive Species. US Fish and Wildlife Service, Albuquerque, US; 2011. Available from: http://www.haccp-nrm.org/haccp_manual_2 011_final_press_ready.pdf. Accessed March 5, 2015.
Wilson J, Smith K. Code of Good Practice for Mussel Seed Movements. A Report to the Bangor Mussel Growers Association, Wales; 2008:26.
Bax N, Hayes K, Marshall A, Parry D, Thresher R. Man-made marinas as sheltered islands for alien marine organisms: Establishment and eradication of an alien invasive marine species. In: Veitch CR, Clout MN, editors. Turning the Tide: the Eradication of Invasive Species. Gland and Cambridge: IUCN Invasive Species Specialist Group; 2002:26–39.
Anderson LWJ. California’s reaction to Caulerpa taxifolia: a model for invasive species rapid response. Biol Invasions. 2005;7:1003–1016.
Gollasch S. Overview on introduced aquatic species in European navigational and adjacent waters. Helgol Mar Res. 2006;60(2):84–89.
Boos K, Ashton GV, Cook EJ. The Japanese skeleton shrimp Caprella mutica (Crustacea, Amphipoda): A global invader of coastal waters. In: Galil BS, Clark PJ, Carlton JT, editors. In the Wrong Place – Alien Marine Crustaceans: Distribution, Biology and Impacts. Berlin, Germany: Springer; 2011:129–156.
Foster V. Blue Build and Biosecurity: Designing the Next Generation of Marinas for Preventing the Spread of Invasives. MSc Disseration. Scottish Association for Marine Science: University of St Andrews; 2013:54.
Gollasch S, Macdonald E, Belson S, et al. Life in ballast tanks. In: Leppäkoski E, Gollasch S, Olenin S, editors. Invasive Aquatic Species of Europe Distribution, Impacts and Management. Dordrecht: Kluwer Academic Publishers; 2002:217–231.
Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W. Marine invasive alien species: a threat to global biodiversity. Mar Pol. 2003; 27(4):313–323.
Connell SD. Floating pontoons create novel habitats for subtidal epibiota. J Exp Mar Biol Ecol. 2000;247:183–194.
Mineur F, Cook EJ, Minchin D, et al. Changing coasts: marine aliens and artificial structures. Oceanogr Mar Biol Annu Rev. 2012;50:187–232.
David M, Gollasch S, Pavliha M. Global ballast water management and the same location concept – a clear term or a clear issue? Ecol Appl. 2013;23(2):331–338.
Cook EJ, Davidson K, Fox C, Black K. Monitoring and Eradication of Invasive and Non-Native Species in Aquaculture Units. A Report to the Scottish Aquaculture Research Forum, UK; 2012:39.
Floerl O, Inglis GJ, Hayden BJ. A risk-based predictive tool to prevent accidental introductions of non-indigenous marine species. Environ Manage. 2005;35(6):765–778.
Nimmo F, Cook EJ, Moxey AP, Hambrey J, Black K. Cost-Benefit Analysis of Management Options for Didemnum Vexillum (Carpet Sea Squirt) In Scotland. A Report to the Scottish Government, UK; 2012:69.
Aldridge DC, Elliott P, Moggridge GD. Microencapsulated biobulletse for the control of biofouling zebra mussels. Environ Sci Technol. 2006;40:975–979.
Laing I, Bussell J, Somerwill K. Assessment of the Impacts of Didemnum Vexillum and Options for the Management of the Species in England. A Report To Natural England, FERA and Cefas, UK; 2010:62.
Denny CM. Development of a method to reduce the spread of the ascidian Didemnum vexillum with aquaculture transfers. ICES J Mar Sci. 2008:1–6.
Locke A, Doe KG, Fairchild WL, Jackman PM, Reese EJ. Preliminary evaluation of effects of invasive tunicate management with acetic acid and calcium hydroxide on non target marine organisms in Prince Edward Island, Canada. Aquat Invasions. 2009;4:221–236.
NIMPIS. Styela clava Species Summary. Centre for Research on Introduced Marine Pests, Clayton South, Australia. Available from: http://www.marine.csiro.au/crimp/nimpis/spsummary.asp?txa=6836. Accessed January 20, 2015.
Coutts ADM, Forrest BM. Development and application of tools for incursion response: Lessons learned from the management of the fouling pest Didemnum vexillum. J Exp Mar Biol Ecol. 2007; 342(1):154–162.
Kleeman SN. Didemnum Vexillum – Feasibility of Eradication and/or Control. A Report to the Countryside Council for Wales, UK; 2009:53.
Aquenal Pty Ltd. Enclosure Treatment: A Biosecure Treatment for Oil Rig Pontoons. A Report to the MAF Biosecurity New Zealand; 2009:43.
Sandodden R, Johnsen SI. Eradication of introduced signal crayfish Pasifastacus leniusculus using the pharmaceutical BETAMAX VET.®. Aquat Invasions. 2010;5(1):75–81.
Maritime Journal. Impounded harbour creates new marina in South Wales; 2002. Available from: http://www.maritimejournal.com/news101/marine-civils/port,-harbour-and-marine-construction/impounded_harbour_creates_new_marina_in_south_wales. Accessed November 18, 2014.
Tsolaki E, Diamadopoulos E. Technologies for ballast water treatment: a review. J Chem Tech Biotech. 2009;85(1):19–32.
Cangelosi AA, Knight IT, Balcer M, et al. The Great Lakes Ballast Technology Demonstration project: biological effectiveness test program (including MV Regal Princess trials). In: Raaymakers S, editor. Proceedings of the 1st International Ballast Water Treatment R&D Symposium; 26–27 March 2001; London, UK. GloBallast Monograph Series. London: International Maritime Organization; 2001:88–94.
Daffron KA, Lewis JA, Johnston EL. Antifouling strategies: history and regulation, ecological impacts and mitigation. Mar Pollut Bull. 2011;62:453–465.
Srinivasan M, Swain GW. Managing the use of Copper-based antifouling paint. Environ Manage. 2007;39(3):423–441.
Floerl O, Inglis GJ. Starting the invasion pathway: the interaction between source populations and human transport as vectors. Biol Invasions. 2005;7:589–606.
Piola RF, Johnston EL. The potential for translocation of marine species via small-scale disruptions to antifouling surfaces. Biofouling. 2008;24(3):145–155.
Hewitt C, Martin R. Revised Protocols for Baseline Surveys for Introduced Marine Species- Survey Design, Sampling Protocols and Specimen Handling. A Report by the Centre for Research on Introduced Marine Pests, Hobart, Australia; 2001:46.
Inglis G, Gust N, Fitridge I, et al. Port of Auckland: Baseline Survey for Non-Indigenous Marine Species. A Report for the BNZ Post-clearance Directorate, New Zealand Government, New Zealand; 2005:91.
Pederson J, Bullock R, Carlton J, et al. Marine Invaders in the Northeast: Rapid Assessment Survey of Non-Native and Native Marine Species of Floating Dock Communities; 2003. Available from http://massbay.mit.edu/exoticspecies/exoticmaps/RAS-report11.pdf. Accessed December 18, 2014.
Ashton GV, Boos K, Shucksmith R, Cook EJ. Rapid assessment of the distribution of marine non-native species in marinas in Scotland. Aquat Invasions. 2006;1(4):209–213.
Nunn J, Minchin D. Rapid Assessment of Marinas for Invasive Alien Species in Northern Ireland. A Report for the Northern Ireland Environment Agency, Belfast, UK; 2013:116.
IMO. International Convention for the Control and Management of Ships’ Ballast Water and Sediments (BWM), London: IMO; 2004. Available from: http://www.imo.org/About/Conventions/ListOfConventions/Pages/International-Convention-for-the-Control-and-Management-of-Ships’-Ballast-Water-and-Sediments-(BWM).aspx. Accessed January 19, 2015.
IMO. Guidance for minimising the transfer of invasive aquatic species as biofouling (hull fouling) for recreational craft. London: IMO; 2012. Available from: http://www.imo.org/en/OurWork/Environment/Biofouling/Documents/MEPC.1-Circ.792.pdf. Accessed January 19, 2015.
This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms.php and incorporate the Creative Commons Attribution - Non Commercial (unported, v3.0) License. By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms.Download Article [PDF]