Keywords

Introduction

The first possible occurrence of a non-indigenous species attributed to being introduced in ships’ ballast water was by Ostenfeld (1908) who reported the Asian phytoplankton species Odontella (Biddulphia) sinensis following its mass occurrence in the North Sea in 1903. It was not until 70 years later that the first biological ballast water sampling (BWS) study was undertaken by Medcof (1975). This was then followed by several others (e.g., Carlton 1986; Williams et al. 1988; Locke et al. 1991; Hallegraeff and Bolch 1992; Gollasch 1996, 2002; Hamer et al. 2000; Gollasch et al. 2000a, b, 2002; Murphy et al. 2002; David et al. 2007; McCollin et al. 2008; Briski et al 2010, 2011) working in different world regions.

The annual number of new species records world-wide since 1850 has paralleled trade, both by shipping and also aquaculture developments. Improvements to ship design allowing for the construction of faster and bigger vessels has led to shorter voyage durations which almost certainly provide for a higher survival of organisms in ballast tanks, and more frequent discharges of bigger quantities of ballast water.

For example, in ICES member countries these shipping species introduction vectors together with others result in a new introduction forming a new population beyond its natural range approximately every 9 weeks (Minchin et al. 2005).

Biodiversity and environmental health has been on the agenda of aquatic ecologists for several decades and of great concern is the potential of “loss of biodiversity” due to increased anthropogenic pressures. However, already in the early biodiversity debate, few scientists highlighted that we are not only facing a “loss of biodiversity” but also a “change” or “increase” of species diversity due to human intervention. These changes may also be considered as threats to ecosystem health and services (Rosenthal pers. comm.).

Species movements with ships ballast water are in the focus of this chapter, resulting in (a) transport of native species, i.e., movements within their natural region of occurrence, (b) introduction of non-indigenous (also named non-native, alien, exotic, immigrant) species, i.e., species movements to areas where they were previously unknown and (c) movement of cryptogenic species, i.e., those species where it is not known if they are native to a region or whether they have been introduced (Carlton 1996). In each of these three categories some species arrivals are simply an addition to the biological diversity of a region without causing negative impacts, whereas a smaller number of species are considered harmful, e.g., human pathogens, and some can cause drastic changes to the receiving environments with a capability of modifying economies and with consequences for human health (e.g. Gollasch et al. 2009).

Here we describe the extent of species movements with ships ballast water worldwide and also provide some examples of the species that have been transferred and have resulted in different impacts following their arrival.

Definition of Terms

There are many different terms and definitions used around the world describing introduced species and their impacts and there is no common agreement in the scientific community or embedded in regulative/management/policy. The following paragraphs define some of the key terms used in this chapter.

Non-indigenous species are species, or other viable biological substances, that entered an ecosystem beyond its historical known range, including all organisms that have been transferred from one country to another, this includes invasive species, i.e., species causing economic or environmental harm or harm to human health (ANS Task Force 1999). A similar definition refers to non-indigenous species as any individual, group, or population of a species, or other viable biological material, that is intentionally or unintentionally moved by human activities beyond its natural range or natural zone of potential dispersal, including moves from one continent or country into another and moves within a country or region; including all domesticated and feral species, and all hybrids except for naturally occurring crosses between indigenous species. Synonyms: alien, immigrant, introduced, and non-native (EPA 2001). The IMO Guidelines G7 (IMO 2007) defines non-indigenous species as “… any species outside its native range, whether transported intentionally or accidentally by humans or transported through natural processes.” This definition goes further compared to the previous ones as it includes natural transport processes while other definitions limit non-indigenous species to human-mediated species movements. It should also be noted that not all non-indigenous species are negatively impacting in the receiving environment.

The negatively impacting species, which are termed invasive species, i.e., are those species which threaten the diversity or abundance of native species; the ecological stability of infested ecosystems; economic (e.g., agricultural, aquacultural, commercial, or recreational) activities dependent on these ecosystems; and/or human health. Synonyms include harmful, injurious, invader, noxious, nuisance, pest, and weed (EPA 2001). As per this definition invasive species could be either native (see outbreak forming species below), cryptogenic or non-indigenous species. A second definition addresses invasive alien species (IAS, based on Olenin et al. 2010) as a subset of established non-indigenous species, which have spread, are spreading or have demonstrated their potential to spread elsewhere and have an adverse effect on one or more of the following: biological diversity, ecosystem functioning, socio-economic values or human health in invaded regions. However, there are also native species which cause concern which becomes in many cases clear when they occur in higher densities, examples include outbreaks of native jellyfish or mass developments of native harmful algae (outbreak forming species).

The term Harmful Aquatic Organisms and Pathogens (HAOP) appears in the IMO Ballast Water Management Convention (BWM Convention) and defines it as being any aquatic organisms or pathogens, which, if introduced into the sea including estuaries, or into fresh water courses, may create hazards to the environment, human health, property or resources, impair biological diversity or interfere with other legitimate uses of such areas (IMO 2004). As a result this term HAOP includes all potentially harmful non-indigenous, cryptogenic and impacting native aquatic species including pathogens.

Natural Species Movements

Many species have the potential to spread by their own means, for example, the migrations over long distances known for, e.g., birds that may carry associates with them that may either attach to them or otherwise infect them. Cladocerans, which are free swimming crustaceans that for part of their life cycle have a relatively smaller resting stage, have been found encrusted on birds feet and so explains how they can be spread between different separated water bodies. Otherwise their spread would not have been possible, as a result birds have been implicated in the spread of many species. Similarly, turtles have been found to spread several species found either entangled or attached to the turtle shell (e.g., Oliverio et al. 1992), such as macroalgae, bryozoans, barnacles, sea squirts, molluscs which were moved over long distances in this way (Pfaller et al. 2008).

Further, ocean currents can move species and under certain rare hydrodynamic conditions, with perturbations in the strength and direction of flow, species can be moved beyond their normal geographic range, perhaps also as a result of climate alterations, for example the increased spread of the sardine, a pilchard, which is occasionally found in the southern North Sea and western Baltic as a result of a rare northeast Atlantic Ocean water inflow and warmer water temperatures (Weber and Frieß 2003).

These natural phenomena result in changes to local species richness and may only appear on a temporary basis within a region, being known as rare guests, or vagrants. Such natural appearances, especially on the fringing ranges of a species where their ability to survive is just possible are a normal part of nature’s biodiversity and is often seen as an advantage. In contrast are the human-assisted species movements which can cause irreversible negative impacts.

Human-Assisted Species Movements

In contrast to natural spread, species have been transported since humans started to explore the world. Early movements will have been with solid ballast (and the damp ballast conditions will have allowed for several attaching, sediment dwelling, or otherwise associated, near-shore and intertidal species to survive and become carried) used to stabilise wooden vessels, as attached hull fouling, with boring organisms in hulls, and what might have been carried as cargo (Eldredge and Carlton 2002; Minchin et al. 2005). Many of the movements will have been unintentional and there is little historic record of what might have been transferred several centuries ago. There will have been many further transmissions during the periods of colonisation and wrecks of vessels may have seeded species in new regions. The more modern forms of transit will have dispensed organisms with solid ballast and utilised water in its place. With this, all ships had, and have, the capacity of spreading species unintentionally (e.g., with ships fouling or ballast, associated with the cargo of vessels or transported on deck) (e.g., Gollasch et al. 2002b; Fofonoff et al. 2003; Minchin et al. 2006, 2009; Carlton and Eldredge 2009).

Ships may transfer organisms over long distances (e.g., across oceans and seas), termed a primary introduction, whereas regional transport is considered as the facilitator of secondary transfer. It should be noted that even short distance transfers are of concern (e.g., Ruiz et al. 2000; David et al. 2007) in order to avoid negative impacts of species when being moved within, e.g., one regional sea or neighbouring waterbodies via inland canals.

In aquatic environments there are seven principal categories as to how species are spread (pathways). Each pathway enables several ways a species may be transferred (vectors). Overall, there are more than 50 recognised vectors (ICES 2005; Minchin et al. 2005). Shipping is considered to be the principal pathway worldwide, by which species are spread. The prime vectors involving shipping are ballast water and sediments accumulated at the tank bottom as well as hull fouling, where also free-living (non-fouling) species were found (Faubel and Gollasch 1996; Gollasch 2002). Species have also been transported as fouling and free living stages in sea chests (Coutts and Dodgshun 2007), as fouling inside ballast tanks, with anchor chains and as fouling in the engine cooling water pipework as well as with cargo. In some cases several vectors may be responsible for the transmission of a single species (Minchin et al. 2007a, b, c).

Ballast water also contains sediments, usually obtained in estuarine areas and shallow turbid bays. These sediment accumulations, that can range from silt to sands, settle on the bottom ballast tanks, providing a niche for infaunal organisms. As a consequence ballast tanks offer three different habitats to species (1) the water itself, (2) sediments at the tank bottom and (3) the tank walls for fouling organisms.

Species in Ballast Water Tanks

According to expert estimates, 3,000–4,000 different species are moved each day around the globe by ships (Carlton and Geller 1993; Gollasch 1996). More recent estimates indicate that the number of species in transit with ships is most probably in the range of 7,000 every day (Carlton 2001) and this does not take into account the transfer of microorganisms such as bacteria and pathogens. While even the general estimates vary greatly, the dimension of species transmission must be regarded as being exceptionally high (often referred to as colonization pressure) and it was concluded that each vessel has the potential to introduce a species (Gollasch 1996).

It is the free-living, often larval, stages in the species life-cycle that are most likely to be transported with ballast water (Hewitt and Campbell 2010). The Fig. 1 shows some examples of organisms which were found in ballast water samples. Very often such stages may be taken-up during the night, since many planktonic organisms undergo vertical migrations to appear higher in the water column during darkness. These vertical migration patterns are widely recognised within marine and freshwater environments. Adult stages of bottom living organisms may also become entrained in ballast water uptake once they occur in the water column. This may be due to strong currents, storm activity or nearby dredging operations which stir up bottom sediment and organisms.

Fig. 1
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Variety of species found in ballast water samples documenting that also fragile organisms survive the ballasting processes

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Ballast water studies conducted since the 1980s in different parts of the world have shown that ships, to an enormous extent, facilitate the transfer of aquatic organisms across natural barriers (e.g., Williams et al. 1988; Hallegraeff and Bolch 1992; Carlton and Geller 1993; Hay 1990; Gollasch 1996; Macdonald and Davidson 1998; Ruiz et al. 2000; Gollasch et al. 2000a, b, 2002; Olenin et al. 2000; Murphy et al. 2002; David et al. 2007; Briski et al. 2010, 2011). A summary of European shipping studies revealed that 1,598 ballast water samples were collected between 1992 and 2003 on 565 vessels of different origin (see Table 1).

Table 1 Summary of European BWS studies indicating each study source, when it was conducted, number of vessels sampled, number of samples and number of taxa identified
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The diversity of living organisms (including native, cryptogenic and non-indigenous species) found during the European BWS studies included viruses, bacteria including human pathogens, fungi, protozoa, algae (unicellular phytoplankton algae and macroalgae), invertebrates and fish. Crustaceans, molluscs and polychaetes, as well as algae, were the dominant groups found in samples and consisted of more than 1,000 identified species. The majority that occurred within ballast were small in body dimensions and better able to survive the physical forces generated by the vessel pumps during the ballasting process. Nevertheless, fishes of up to 15 cm have been found within tanks (Gollasch et al. 2002) which was also documented during BWS events when testing the performance of ballast water treatment systems (Gollasch and David, own observation). A list of all animals, plants and bacteria groups found in the European BWS studies undertaken until 2002 is available in Leppäkoski et al. (2002a, b). Since this study was completed, further studies were conducted (e.g., David et al. 2007; Drake et al. 2007; Dobbs 2008; McCollin et al. 2008; Briski et al. 2010, 2011) and altogether they provided sufficient information to support the need for ballast water management actions.

The majority of organisms taken-up in ballast water expire at an exponential rate during the first 3–5 days in a ballast tank due to a wide range of conditions that occur within them (e.g., McCollin et al. 2008; Gollasch et al. 2000a, b; Olenin et al. 2000). Ballast tanks are, for most organisms, unfavourable habitats, there is an absence of light and there can be limited resources such as oxygen, food, lack of shelter and the varying temperatures that may take place during a voyage that may considerably differ from the ballast water uptake area. Some inter-oceanic ship voyages can expose ships ballast water to wide ranges of temperature between tropical and temperate regions, this is because the ballast water gradually assumes a similar temperature to that of the ambient sea surface a ship passes through, as can happen with passages between the Pacific and Atlantic (see Fig. 2). In winter these changes can be extreme.

Fig. 2
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Ballast water tank temperatures and sea surface temperatures during a voyage from Singapore to Bremerhaven (Reprinted from Gollasch et al. 2000a, copyright 2000, with permission from RightsLink Service, Oxford University Press)

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Although voyage duration affects the survival of organisms in ballast water, it is not a ballast water management option to retain the water onboard for long periods in order to ensure that all organisms die. Some organisms can survive 3 or more months between ballast uptake and discharge. In one case, where daily samples of ballast were taken during a voyage, a crustacean (a harpacticoid copepod), greatly increased their numbers, and had most probably reproduced inside the ballast tank during the voyage (Gollasch et al. 2000a). Some organisms can survive in ballast sediments for long periods when they develop resting stages. Some phytoplankton species, in particular dinoflagellates, several of which can generate toxins, form such resting stages (cysts) which may settle to the bottom sediment in a ballast tank. These may remain viable (in a dormant state) despite unfavourable conditions from months to years. This poses a risk since as viable cyst-forming species may be discharged during deballasting with disturbed sediments after several voyages from their uptake or with sediments when removed during tank cleaning (Hallegraeff and Bolch 1992).

There is not only a high diversity of species in transit with ships, but also large numbers of individuals that may be transported and that might survive to a destination port region. The overall numbers of organisms recorded from ballast water have been reported by the ICES/IOC/IMO Study Group on Ballast and Other Ships Vectors (SGBOSV) under the four headings: virus-like particles, bacteria, phytoplankton and zooplankton (see Table 2). The purpose was to provide guidance for the development of ballast water discharge standards for the BWM Convention. Any estimates of the numbers of the different groups to be in transit are likely to be underestimates because species that reside within sediments, and those planktonic species that pass through the plankton nets, using the standard mesh sizes 55 and 80 μm, during BWS, do not get considered (Gollasch and McCollin 2003). During the performance test of ballast water treatment systems more than 29,000 zooplankton organisms greater than or equal to 50 μm in minimum dimension per m3 and more than 47,000 phytoplankton cells greater than 4 μm in minimum dimension per milliliter have been found in pumped ballast (Gollasch and David, unpublished). Such great numbers of living organisms taken up during ballasting indicates a high probability of a viable population evolving following discharge in new environments, often referred to as propagule pressure.

Table 2 Summary of numbers of different organisms per litre
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Chain of Events for a Species Introduction

The previous section of this chapter has shown that an enormous number of species in high organism concentrations are being transferred with ballast water. However, only the transport of a species does not result in a colonization of a new region, there is a chain of events that a species must endure in order to become established within a new environment (Carlton 1986; Hayes 1998). This starts with the uptake of ballast water. As many species have seasonal planktonic stages it is during those periods of abundance that sufficient surviving numbers may go on to later form a viable inoculum at discharge. Suspended sediments can also result in cysts and benthic biota becoming transmitted with the same ultimate capability. Having survived the uptake process the voyage(s) must be endured followed by the trauma during discharge. On arrival sufficient numbers will be needed to establish a population. The numbers required to develop new populations is generally unknown but theoretically some species can generate new populations with low numbers (Bailey et al. 2009). Survival depends on their tolerance to the conditions in the new environment and the degree of dispersal following discharge. Very often these windows of opportunity for establishment may depend on the precise location of ballast release. The colonization success may depend on the season during which arrival takes place, in cold climate regions warm water species may only survive discharge in summer, and might not subsequently survive any winter. Unless a species can reproduce a colonisation cannot evolve. Once a founder population is formed a species can then be spread by a wider range of human activity processes but also by natural processes.

Transfer and Impacts of Non-indigenous Species

Hewitt and Campbell (2010), Hayes and Gollasch (both unpublished) suggest >2,000 aquatic non-indigenous species have been introduced world-wide, of which in minimum 850 are thought to have been introduced by ships (Hayes and Sliwa 2003). There are some world regions that have greater numbers of recorded aquatic non-indigenous species present, these have often been in port regions, in sheltered bays and estuaries in regional seas (see Fig. 3).

Fig. 3
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Hot spots of invasive marine species. Small circles: <150 species, medium circles: 150–250 species and large circle: >250 species (see text for references)

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In Europe >1,000 non-indigenous species are recorded from coastal and adjacent waters. The numbers of non-indigenous species in European seas have different patterns to all other world regions, this is because more than 50 % of the introductions occur in the Mediterranean Sea with more than 650 species records of which, at least 325 are established. The North Sea makes up 16.2 % of the known non-indigenous species. The lowest numbers occur in Arctic waters where 18 non-indigenous species were recorded, making up only 1.3 % of the European component (Vermeij 1991; O’Mahony 1993; Boudouresque et al. 1994; Leppäkoski 1994; Eno and Clark 1994; Gollasch 1996; Olenin and Leppäkoski 1999; Reise et al. 1999; Leppäkoski and Olenin 2000; Ricciardi and MacIsaac 2000; Zaitsev and Ozturk 2001; Aladin et al. 2002; Berger and Naumov 2002; Eldredge and Carlton 2002; Golani et al. 2002; Gomoiu et al. 2002; Goulletquer et al. 2002; Hopkins 2002; Carlton and Eldredge 2009; Leppäkoski et al. 2002a, b, 2009; Minchin and Eno 2002; Occhipinti-Ambrogi 2002; Ozturk 2002; Grigorovich et al. 2003; Hewitt et al. 2004, 2007, 2009; Zenetos et al. 2004; CIESM 2005; Jensen and Knudsen 2005; Pancucci-Papadopoulou et al. 2005; Reise et al. 2005; Streftaris et al. 2005; Wolff 2005; Olenin 2005; Cardigos et al. 2006; Gollasch and Nehring 2006; Gollasch 2006; Gollasch et al. 2009; Alexandrov et al. 2007; Gittenberger 2007; Kerckhof et al. 2007; Cook et al. 2008; Olenina et al. 2010; Verlaque et al. 2010; AquaNIS 2013.Footnote 1 Katsanevakis et al. 2013).

Most species introductions almost certainly go unnoticed. Some species, either gradually or rapidly expand their populations to become invasive, a time when they become easily recognised, usually some years after an arrival. However, the great majority of non-indigenous species that are introduced are not perceived to cause harm, but it is those, that result in some form of impact, that are of concern.

The impacts of introduced species vary greatly and can cause considerable harm by modifying natural environments with consequent long-term impacts (see Box 1). While there are a comparatively small number of invasive species among all non-indigenous species that arrive, those that have impacts may have serious consequences that may endure for a considerable time. In the extreme cases these negative consequences are almost catastrophic and seemingly irreversible (e.g. Hayes and Sliwa 2003).

Not all introduced species are considered harmful, in some cases this is quite the reverse, as some provide for important industries providing employment and the sustained production of valued products. Examples include the many clam species, oysters and shrimp that have been cultivated. However, some may become so prolific to create some unwanted effects, such as the recent expansion and fouling of the Pacific oyster in the North Sea following increased recruitment, arising from changes in climate (Reid and Valdés 2011). However a latent threat to the environment, human health, property or resources remains as a non-impacting species may turn into an invasive species at a later stage.

Great harm can be caused by the introduction of one harmful species. For instance, the Chinese mitten crab Eriocheir sinensis has resulted in economic damage to pond fisheries and damage to river banks from burrowing with the resultant accumulations leading to increased dredging costs (e.g. Gollasch 1999). The zebra mussel Dreissena polymorpha, originally from the Black Sea region, has expanded its range in Europe and now is extensively distributed in North America. It has resulted in environmental changes to lakes and rivers; but, on account of its ability to attach to surfaces with byssal threads, has fouled abstraction piping and thrash racks of power stations and municipal water supplies, and continues to do so (Hebert et al. 1989; Carlton and Geller 1993; Johnson and Padilla 1996; van der Velde et al. 2010). The predatory sea star Asterias amurensis arrived to Australia from the north-west Pacific and has caused significant changes to bottom dwelling communities, some of economic importance (Buttermore et al. 1994; Byrne and Morrice 1997; Rossa et al. 2003). A further predator, the comb-jelly Mnemiopsis leidyi, was inadvertently introduced to the Black Sea from the eastern coast of the Americas. Its vast numbers resulted in heavy predation on zooplankton, including the larval stages of commercially important fishes (GESAMP 1997; Vinogradov et al. 2005). Although as a result of a further comb-jelly introduction that fed on M. leidyi its abundance declined in the Black Sea it appeared in the Caspain Sea carried by shipping using the interconnecting Volga-Don-Canal (Ivanov et al. 2000). It has since appeared in the Kiel Bight and has spread to several Baltic countries and to the southern North Sea (Javidpour et al. 2006) and it also expanded southwards to the Eastern Mediterranean. The North Sea invasion was overlooked for some time as the species was initially misidentified as a native comb-jelly (Faasse and Bayha 2006). Using taxonomic identification with microsatellites it was possible, for the first time for comb-jellies, to show that there have been two separate invasions of M. leidyi colonizing European waters from two North American source areas. The results show one originating from or near the Gulf of Mexico having arrived to the Black Sea and the North and Baltic Seas population was traced to New England populations (Reusch et al. 2010).

All of the summed impacts amount to a considerable economic cost which is difficult to quantify. In the USA alone a comprehensive study concluded that the estimated annual damage and/or control costs addressing introduced aquatic non-indigenous species is $14.2 billion (Pimentel et al. 2005). A recent summary for Europe that includes costs for repair, management and the mitigation of impacts results at more than 12 billion Euros annually (Shine et al. 2010). However, this cost includes terrestrial impacts on habitats and on services. For the aquatic sector the costs are thought to be 10–15 % of this amount.

Box 1: Nature of Impacts

Impacts on biodiversity: predation on native communities, alteration of habitat structure and re-organisation of the trophic web, importation of diseases and disease agents, alterations of the genome (Olenin et al. 2007).

Economic losses: impacts on aquaculture production, impacts on fisheries resources, fouling of abstraction piping, impact on recreational resources.

Human health concerns: infectious cholera strains, other diseases, toxins generated by algae that contaminate foods, outbreaks of stinging jellyfish affecting swimmers, bathers cut feet on bivalve shells.

Transfer and Impacts of Potentially Harmful Phytoplankton Species

Ballasted seawater may contain 30–>100 phytoplankton species including those being potentially toxic or others forming harmful algal blooms. These are unicellular microalgae, most usually these are diatoms and dinoflagellates, and may occur at levels of a thousand to a million or more cells per litre (Hallegraeff 1993, 1995, 1998). As a result these have great potential for global transfer and ‘successfully’ introduction of these species.

Over 100 years ago it was claimed that the centric diatom Odontella sinensis, known from tropical and subtropical coasts of the Indo-Pacific, had arrived in the ballast water of a merchant vessel, and had spread to become sufficiently abundant in the North Sea to result in plankton blooms in 1903 (Ostenfeld 1908). These blooms had no known harmful effects. It was not until the 1970s, the introduction of further centric diatom, Coscinodiscus wailesii, to the North Sea which clogged fishing nets due to extensive mucilaginous accretions (Boalch and Harbour 1977; Laing and Gollasch 2002). For many other phytoplankton species their origin is unknown which is also due to the taxonomic uncertainties with many phytoplankton species (see cryptogenic species below).

In Australia, an investigation found that 80 % of vessels contained approximately 30 culturable diatom species, including the potentially toxic Pseudonitzschia species that can cause Amnesic Shellfish Poisoning (ASP) (Forbes and Hallegraeff 1998) which can debilitate humans following consumption of contaminated shellfish. Further, cultures of viable dinoflagellates Alexandrium catenella, A. tamarense and Gymnodinium catenatum, all known for the toxins they can produce and consequent impacts on human health, were extracted from the ballast water of 5 % of the vessels arriving from Japan and Korea (Hallegraeff and Bolch 1992). Studies of vessels entering British ports confirmed the presence of A. minutum, A. catenella and A. tamarense in 17 % of ballast water samples (Hamer et al. 2001). In one case, a single ballast tank contained as many as 300 million viable Alexandrium tamarense cysts (Hallegraeff and Bolch 1992). The occurrence of such numbers in ballast water discharges may well have contributed to the widespread distribution of this species. In addition, the potentially ichthyotoxic dinoflagellate Pfiesteria piscicida has been confirmed using molecular probes in ballast water entering US ports (Doblin et al. 2002). In conclusion, the presence of potentially harmful marine microalgae in ballast water has been firmly established.

Dinoflagellates do not always need to form blooms in order to result in toxic events. They can occur at comparatively low densities sufficient to render cultured filter-feeding molluscs toxic. However, there are national programmes that regularly monitor for these toxins to ensure that both cultured and wild molluscs are safe for human consumption. Sudden outbreaks of toxic dinoflagellate species have taken place world-wide and have been attributed to ballast water releases (Hallegraeff 1993; David et al. 2007). On occasion their occurrence and also collapses of blooms of non-toxic species can cause de-oxygenation events to result in losses to aquaculture production, fishery landings and high mortalities of bottom living species. Although monitoring programmes exist, human casualties are also reported each year due to consumption of toxin contaminated seafood and it was found that ballast water and the sediment contained in the tanks, are one of the main (if not the main) transfer vectors of potentially toxic dinoflagellates (Hallegraeff 1993; David et al. 2007).

Transfer and Impacts of Cryptogenic Species

There are many species whose status is unclear because they may be native species that have recently been recognised or undergone an outbreak and their native range is not clearly known. Those species not demonstrably native or introduced are termed cryptogenic species (Carlton 1996). There are several examples that include the fouling brackish water barnacle Balanus improvisus, the bivalve Mya arenaria and the ship-worm Teredo navalis. Due to the taxonomic uncertainties many phytoplankton species (i.e., dinoflagellates and diatoms) are seen as cryptogenic species as many are now known from many different world regions and their identification is often a highly specialised skill, improved in recent decades using new technologies (Gómez 2008). This group of species is of special concern as many are potentially toxin producers which affects many resource users (see above).

Mya Arenaria

Already the Vikings sailed the seas and their activities may have resulted in the introduction of the North American bivalve Mya arenaria to Europe (Petersen et al. 1992). It was suggested that Vikings when returning from North America may have kept live Mya arenaria onboard either intentionally as fresh food, or unintentionally may have imported them with the solid ballast on their vessels. Excavations at Haithabu, Germany, a Viking trade hub in the Baltic Sea, revealed enormous numbers of ballast stones at and near the landing pier (see Fig. 4), supporting the probability of a species introduction with this solid ballast.

Fig. 4
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Ballast stones excavated near the vessel landing pier of the Viking trade hub Haithabu, Germany

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Viking ships are likely to have explored sheltered estuaries in North America, and these environments would likely have had large numbers of Mya arenaria. Very likely, on account of the great importance of each vessel when not in use they were likely to have been carried on muddy shore, a habitat the soft clam also occupies, and so before any journey a supply of food may have been readily available. However, Wolff (2005) stated that the transfer of Mya to Europe by the Vikings poses a problem. Except for an occasional event when a vessel may have been driven off course by gales, there was no direct Viking shipping activity between North America and Europe (Marcus 1980). Greenlanders sailed to North America more frequently and also travelled between Greenland and Norway. However these voyages were not undertaken by the same vessels. It may therefore be possible that Mya was first introduced from North America to Greenland and subsequently from Greenland to Europe (Ockelmann 1958; Petersen 1978, 1999). In contrast, a different scenario describes that there was a gradual re-expansion of this mussel into Europe following the last glaciation period from a southern locality. So in this case it remains uncertain whether this mussel was introduced or it naturally re-colonised Europe.

Teredo Navalis

The shipworm, which is not actually a worm, but a ‘worm-like’ mollusc, which bores into wood, is one of the oldest invaders known. They naturally spread with wooden material, within the hulls of wooden vessels from early times and is so widely spread that its native origin has become obscured. It was first recorded in Europe in 1731 (Sellius 1733), when it destroyed wooden dyke gates in the Netherlands, causing a terrible flood. At this time the Dutch believed it was introduced from Asia, possibly sent as a punishment from God (www.waddensea.org). Many naval engagements at sea may have been lost on account of the weakening effects of the boreholes on the hull and many vessels will have been disabled and wrecked on account of this damage. It was also proposed that the vessels of the Spanish armada, while waiting in French and Portuguese harbours to prepare for the invasion of England in 1588, may have been weakened in stability by the ship-worm so that the fight was lost. It was proposed that the ‘shipworm’ originated in the North Atlantic area (Schütz 1961) on account of its tolerance to low temperatures. This could support a possible origin from northern or southern Atlantic waters. Nowadays T. navalis is known to occur in Northern Europe, Indonesia, Japan, Australia, Brazil, the Atlantic and Pacific US and Canadian coasts. Many attempts were made to deter their colonisation of hulls over the centuries. Today they continue to have impacts, but on account of the usage of steel as vessel hull material, these impacts are to harbour pilings, as has happened in recent years on the Kiel Canal, Germany.

Transfer and Impacts of Human Pathogens

Human pathogens and microorganisms are also transferred with ship’s ballast water (Ruiz et al. 2000; Drake et al. 2001, 2007; Casale 2002; Dobbs and Rogerson 2005; Dobbs 2008).

Particular strains of cholera, have and continue to, threaten human health worldwide. There is evidence that ships spread the pathogenic strain of this bacterium, Vibrio cholera O1. In 1991 the virulent form was found in Mobile Bay, Alabama, in the Gulf of Mexico (McCarthy and Khambaty 1994). It appeared in oysters that had filtered the virus arising from the discharges of ballast water (Motes et al. 1994). During a standard inspection, the US Food and Drug Administration isolated Vibrio cholerae O1 from the stomach content of a fish caught in Mobile Bay. The strain was similar to that found in Latin America where many humans died (Casale 2002). Indeed, the epidemic occurring in Peru was directly related to ships ballast discharges and spread to many regions in South America. In 1991 more than a million people had become infected; and by 1994 there were >10,000 victims although it is believed that their number was underestimated due to inappropriate coverage. This particular form of cholera had previously been known only in Bangladesh (Casale 2002) thereby highlighting the likelihood that ballast water transport contributed to this disease outbreak.

A study of ships in Hamilton and Toronto (Canada), at the entrance to the Great Lakes of North America, conducted in 1995 found within 71 ballast water samples a frequency of 45 % of the faecal coliform bacteria, Escherichia coli, and 80 % of the samples contained enterococcal bacteria (Whitby et al. 1998). Furthermore, streptococcal bacteria were found in four ballast water samples taken during this Canadian study.

Future Issues and Concerns

Monitoring of ballast water receiving habitats to document newly introduced species is rarely undertaken. Coastal monitoring programmes exist, but in many cases they lack sampling stations in ports where the ballast water is discharged or taken up. Only when new introduced species are recognized soon after introduction an eradication programme is advisable, should the newly found species cause concern. Regular monitoring using a rapid assessment approach is more likely to encounter targeted species at an earlier time (Minchin 2007b) so that those found at an early stage might be eradicated (Bax 1999). The longer a species occurs unnoticed the more unlikely an eradication programme will be successful, as during the intervening time, the species is likely to have spread over a wider area.

The identification of species is often dependent upon taxonomic skills which are not easily acquired. It may well be possible that such services, due to the reducing number of specialists, will become less available creating a consequent confusion in the area of biogeography and biological invasion science. Taxonomic skills are needed as the invasion status of an organism can normally only be assessed when the species level is identified. The lack of taxonomic expertise may also lead to overlooking introduced species, as had happened with Mnemiopsis leidyi in the North Sea. The presence of this species was possibly overlooked for almost a decade as the comb jellies found were confused with native species (Van Ginderdeuren et al. 2012).

Although there is an impressively high number of new non-indigenous and/or harmful species being introduced every day all around the world, relatively few cases of ‘successful’ invasions have been recognised. Despite relatively few invasions, a number of cases have had significant (almost catastrophic) and seemingly irreversible impacts. Consequently, a precautionary approach suggests that every vessel transporting ballast water should be treated as a potential risk by enabling introductions of harmful species.