by Devin M. Bartley
Inland Water Resource and Aquaculture Service,
Fishery Resources and Environment Division,
FAO Fisheries Department,
Viale delle Terme di Caracalla,
00100 Rome, Italy
and Dan Minchin
Fisheries Research Centre,
Department of the Marine,
Abbotstown, Dublin 15, Ireland
Introduced aquatic species are an established means to increase productivity and generate income in aquaculture and capture fisheries. Introduced species are also an inadvertent by-product of modern transportation, shipping and international trade. Both the intentional and inadvertent introductions are recognised as serious threats to aquatic biological diversity. Therefore, management must address both beneficial and negative aspects of species introductions. However, there is often an inadequate knowledge base on which to base policy and management decisions. Two basic unknowns exist concerning an introduced species: i) its impact on the receiving ecosystem and ii) its performance in the new ecosystem. Related to these unknowns are three general levels of uncertainty: i) uncertainty that arises from a lack of basic information; ii) uncertainty that arises from unknown interactions within a given system; iii) uncertainty that arises from shifts and interactions in physical, biological, social and political systems. Activities to reduce uncertainty and reduce the chance of adverse impacts are considered part of a precautionary approach to species introductions. There are several precautionary approaches that may help minimise adverse effects from exotic species. These range from getting resource managers to think about an introduction through education and use of a code of practice, documenting native resources that may be affected, maintaining registries of exotic species and their effects, up to incorporation of protocols and guidelines for implementing codes of practice and environmental impact assessments in legislation. Guidelines and codes of practice represent one of the best precautionary activities available for species introductions. However, several recommendations to minimise the chance of adverse impacts are controversial in that they may not be scientifically nor economically justifiable, may be difficult to implement, or may compromise human safety. Genetically modified organisms (GMOs) are recognized as an exotic organism, even if they may be conspecific with native organisms and derived by conventional breeding techniques. The product of the genetic modification, i.e. the change in phenotype, should be assessed rather than the process that lead to the modification in order to assess accurately the level of risk associated with GMOs.
The use of exotic species has been demonstrated to be an effective means to increase food production and generate income. The introduction1 of Kapenta, Limnothrissa miodon, into Lake Kariba in southern Africa created a fishery worth millions of dollars (Marshall, 1991, Bartley, 1993), exotic salmonids in Chile form the basis for a growing and internationally successful aquaculture industry (FAO, 1994). Grass carp, Ctenopharygodon idella, and the mosquito fish, Gambusia affinis, have been widely introduced as biological control of aquatic weeds and mosquitoes (Welcomme, 1988). However, bio-control and the development of fisheries and aquaculture based on exotic species poses risks to native aquatic resources and can significantly change the socio-economic structure of local human communities (Reynolds and Greboval, 1989).
Species are also introduced unintentionally through the aquarium trade, ships' ballast, on ships' hulls, in packing material, and even on fishing gear. The movement of exotic species by shipping has been reviewed (Carlton, 1985, 1987, 1989, 1992a,b; Carlton and Geller, 1993; Carlton et al., 1990; Williams et al., 1988 and Omori et al., 1994). Because of the limited survival time of many species most introductions have been to either side of the same ocean (Carlton et al., 1990; Hallegraeff and Bolch, 1991; Mills et al., 1993). Because of the large volumes of water used in ballast discharges, a variety of viruses, bacteria, single celled organisms and metazoa may become moved to a new locality and inoculated into a new ecosystem. It is likely that ports in partially enclosed bays with poor water exchange may be more likely to enable new populations to develop. Areas such the Baltic Sea, the Black Sea and the Mediterranean Sea, as well as ports situated close to tidal nodes are particularly at risk.
Introduced species are now regarded as a leading threat to native aquatic biodiversity (Williams et al., 1989). European crayfish, Astacus astacus, were adversely affected by a fungal disease inadvertently introduced to Europe with American crayfish, Orconectes limosus (Furst, 1984). The introduction of the Nile perch, Lates niloctica, to Lake Victoria may have caused, or contributed to, the extinction of nearly 200 species (Barel et al., 1985; Gophen et al., 1995). Fisheries in the Black Sea have been decimated by, inter alia, the introduction of an introduced ctenophore, Mnemiopsis leidyi (Travis, 1993). Epizootic ulcerative syndrome has expanded its range through Southeast Asia with fish movements and poor quarantine controls, and may be introduced elsewhere with further aquaculture species movements or aquarium fishes. This disease has resulted in a serious loss of cultured fish production through most of Asia (Roberts et al., 1994; M. Shariff, pers. comm.). Transfers of Atlantic salmon from the Baltic Sea to stock enhancement programmes in Norway, introduced a monogenean ectoparasite, Gyrodactylis salaris, that now threatens native stocks (Bakke, 1991). Although successful treatment using rotenone has eliminated the infected salmon in one catchment (Johnsen and Jensen, 1986), eradication of an introduced species once it is established is usually difficult or impossible (Carlton and Mann, 1981).
Introduced species may affect native resources via ecological, genetic, pathogenic, and socio-economic pathways. Ecological interactions include predation (Barel et al., 1985), competition (Chew, 1990; de Iongh and van Zon, 1993) and habitat modification (Chilton and Muoneke, 1992). Genetic impacts include hybridisation and introgression, loss of co-adapted gene complexes, reduction in fitness, and loss of genetic diversity (Bartley and Gall, 1991; Hindar et al., 1991; Waples, 1991). Pathogenic impacts include the transmission of disease and parasites (Bakke, 1991; Furst, 1991; Stewart, 1991) and socio-economic impacts include the changes in fishing methods, markets, price, labour force and activity patterns (Reynolds and Greboval, 1989). These effects may arise out of developments intended for aquaculture and fisheries, shipping, or by other sources. Once a species has been exported, i.e. introduced, transfer back to its native range may also cause impacts. For example the flat oyster, Ostrea edulis, introduced to north-east America, and from there to the Pacific coast, were subsequently transferred to France. The oysters carried a previously undescribed haplosporidian, Bonamia ostreae, which has resulted in a changes in oyster farming practice in affected areas of Northern Europe (Chew, 1990).
1 Introduction has been defined as the movement of a species to an area outside of its natural range, transfer has been defined as the movement of a species within its range (Welcomme 1988). To increase readability and to acknowledge that transfers of genetically differentiated populations and genetically modified organisms may be nearly equivalent to the introduction of a new species, in this paper introduction refers to both the introduction and transfer of organisms, including genetically modified organisms
Movements of species which are closely related may result in very different effects. For example the Chinese hat limpet, Calyptraea chinensis, was probably introduced with oysters to the west coast of Ireland from France, have little effect on benthic communities (Minchin et al., 1987). Whereas the related slipper limpet, Crepidula fornicata, introduced to northern Europe from the east coast of the USA, has modified the environment in several sea inlets and bays and can locally produce a biomass significantly greater than many commercial species (Minchin et al., 1995a). In the Baie de Granville the population biomass is calculated as 750,000 tonnes (Blanchard, 1995).
For a number of introduced species the full effects on its host or new environment remain unknown. For example, the introduction of half-grown Japanese oysters, Crassostrea gigas, to Europe (Grizel and Heral, 1991) has resulted in the recent expansion of the range of populations of the copepod gut-parasite, Mytilicola orientalis, from France to Ireland (Minchin and Holmes, 1995) and the Netherlands (Stock, 1993) and may affect the condition of its host if badly managed in culture.
The management of exotic species must address both beneficial and negative impacts resulting from their introduction. However, there is often an inadequate knowledge base on which to base policy and management decisions. Baltz (1991) states “… Our present understanding of how coastal marine communities function is poor. Until we understand the factors that regulate communities, the effects of species introductions will remain unpredictable…”. A similar situation is likely to exist in many freshwater systems (Ross, 1991).
There are two basic unknowns associated with the use of exotic species in fisheries:
Knowledge of the nature and extent of the impact will be crucial for protecting local resources, biological diversity and evaluating risk, whereas, the performance evaluation will be necessary for evaluating benefits. Although evaluation of impact and performance may only be possible following the introduction of the species, some indications may be obtained from information in areas where the species occurs naturally or at other introduced sites that have similar characteristics.
There are three areas of uncertainty that form a continuum from simple easily addressed uncertainties to complex uncertainties arising from interaction of physical, social and political systems (Costanza, 1993). The use and management of exotic species involve all of these:
Uncertainty that arises from a lack of basic information.
For example, the uncertainty of the composition of a lake's fish community could be addressed by faunistic surveys. Fishery biologists or systematists could address this uncertainty.
Uncertainty that arises from unknown interactions within a given system. For example, how an introduced fish will evolve in its new environment. Several hypotheses could be modelled or estimated based on previous introductions of similar organisms into similar environments. For this procedure to be effective a large volume of information is often necessary. Specialists, such as systems ecologists, could address this uncertainty where information gaps may be compensated for by informed judgement using a collection of data sets.
Uncertainty that arises from shifts and interactions in physical, biological, social and political systems. The effects that arise from such circumstances are often unpredictable. The introduction of the Nile perch into Lake Victoria was an example of this type of uncertainty where changes occurred in the physical and biological composition of the Lake, in the character of the fishing industry, in the community surrounding the Lake, and in the economic structure of the Lake's bordering countries. Changes even occurred in the forest community surrounding the Lake because timber was removed to smoke Nile perch flesh to make it more transportable and palatable. Uncertainty as to the causes of the changes to the lake continues because the introduction of the Nile perch was not the only perturbation to the system; overfishing, pollution and sedimentation also affect the Lake (Reynolds and Greboval, 1989).
Uncertainty is recognised and accepted in science, but policy, legislation and regulations require more certainty. In trying to maximize benefits of aquatic species introductions for human populations, the third and most complex form of uncertainty is often generated. However, as Costanza (1993) states, a scientific method of experimentation and observation can still be applied here to determine the level of our understanding. Thus, the management of exotic species becomes adaptive, based on the results and assessments of previous or ongoing introductions. This approach appears similar to the precautionary approach of adaptive management or internalized feedback (Hilborn and Peterman, this volume).
When uncertainty is acknowledged, it is necessary to install mechanisms or policies to safeguard against harmful effects. Such is the basis of the precautionary approach. That is, policy and commitment of resources should be established in anticipation of potential adverse impacts of a management decision that may relate to a detrimental effect of an introduction. The approach could be extended to the monitoring and evaluation of introductions to comply with Costanza's “experimentation and observation” as a means to reduce our uncertainty.
Within fisheries management there are two broad categories of exotic species, those that are introduced into the wild purposefully for fisheries, biological control, etc. and those that are introduced passively or by mistake, such as in ship's ballast, escapes from aquaculture facilities and from petfish tanks (Carlton, 1992a,b). Pathogens and parasites may occur with either type of introduction and are not treated separately as introductions. Precautionary measures will require different application depending on the vector involved and the biological characteristics of the introduced species. For example, many significant introductions have been associated with oysters, and some of these have been harmful. Oysters may carry many taxa as epifauna or epiflora on the often rough surface of the shell. In addition, parasites and diseases, of which there are many, can be associated with the living tissues, and within the shells of oysters that have died; algal cysts or infaunal invertebrates may be contained in sediments (Minchin, in press). Oysters are often transported in large numbers, and because of this, may contain a sufficient population of the associated exotic to provide an effective innoculum for a new locality.
However, the precautionary approach must be reasonable and should not unduly hinder potential development. Several recent international gatherings of experts in aquatic resource development and management have stressed the need for practical guidelines on the responsible use of introduced aquatic species, as well as the need for easily understood information on ecology, genetics, and fish health (FAO, 1993; Coates, 1995; Aquaculture for Local Community Development Programme (ALCOM) and FAO, unpub. reports). Precautionary guidelines that require extensive research, technology or intensive management may only be feasible in developed countries, and may leave developing countries and rural areas marginalized and unwilling to adopt any level of precaution (Coates, 1995; ALCOM unpub. report).
Precaution can, in theory, extend to the depths of our lack of understanding of aquatic systems. This depth can be extensive, especially in the areas of genetic resources, introduced species and their value to the continued existence of a fishery resource. Therefore, the precautionary approach must be associated with a risk:benefit analysis or a comparative risk analysis (Pullin, 1994; Shrader-Frechette, 1995). The risks and benefits must be evaluated in relation to local priorities and national sovereignty.
The management of introduced species will involve research, technology, and actual management. However, many previously proposed precautionary activities for introductions are controversial or involve an element of increased cost that may not be scientifically nor economically justifiable. The purposes of this paper are to examine how a range of precautionary approaches can be applied to research, technology and management of exotic species in the aquatic environment and to assess some previous recommendations concerning introduced species.
Fisheries and aquaculture
Aquatic species have been introduced to establish fisheries (commercial and sport), for aquaculture, as bait for fishing, and as forage for other important species (Welcomme 1988). The use of bait fishes can result in their establishment in new localities. This generally applies to freshwater species (Welcome, 1991), but also to marine species. The goldspot herring, Herklotsicthys quadrimaculatus, native to the Marshall Islands appeared in Hawaii, and may have been introduced there when used as a bait fish for tuna (Randall, 1987).
An introduction for aquaculture is considered to be similar to an introduction into the wild. Experience has shown that complete containment of exotic species in aquaculture facilities is nearly impossible and that an introduction to an aquaculture facility should be considered a step towards its eventual introduction into the wild (Welcomme, 1988, Coates, 1995). Furthermore, many extensive aquaculture impoundments are similar to intensively managed small water bodies and therefore difficult to distinguish from natural waterbodies.
Biological control methods, particularly in the management of aquatic plants and mosquitoes. (Bennett, 1984; Welcomme, 1991) have been partially successful. The success of these methods encourages the further use of this option in the control of invasive species. Some important exotic pest species for which biological control is being researched include:
Mnemiopsis leidyi, introduced to the Black Sea in ballast water from the Western Atlantic, this ctenophore occurs in high densities and feeds on several phyla of plankton, including larval fishes that formerly sustained important commercial fisheries (Travis, 1993). Teleosts, such as sockeye, Oncorhynchus nerka, and chum salmon, O. keta, which feed on ctenophores and are commercially valuable are being considered as biological control (John Caddy, FAO, pers. comm.)
Carcinus maenas, the shore crab of European waters, has now become widely distributed beyond its natural range, probably as a result of ballast water transport. The shore crab is a significant predator of bivalves. Natural parasites of this species, such as Sacculina carcini, are being considered as a means for control. The parasites reduce the mechanical capabilities of the hosts chelae and in addition reduce the reproductive output (Lafferty and Kuris, 1994).
Dressina polymorpha and D. Bugensis, zebra mussels, are fresh water bivalves that have been introduced from the Black Sea to the Great Lakes of North America. Their abundance in the new environment has resulted in serious trophic changes and fouling. Studies for their control include research on predators from the zebra mussels' home range.
Biocontrol programmes, especially those that involve exotic species, should be weighted carefully against other control methodologies, such as physical and chemical techniques (ICES unpublished report). It is likely biological control techniques will take some time to evaluate, e.g. through establishment of field trials. However, the pressing need to manage some invasive species may conflict with the normal precautions and protocols observed for an introduction. The addition of further non-native species must be considered as having the potential to give rise to further and more complex management difficulties. Much may be learned by the studies on biological control in other disciplines such as entomology.
Research and a basic understanding of an organism's biology and ecological requirements will be necessary to evaluate potential impacts and performance in a new environment. The study of a species within its normal range has been suggested as a means to evaluate its impact in a new environment. However, a species' performance in its natural environment may be very different from its performance in a new setting which may have different physical and ecological constraints. The golden apple snail, Pomacea spp., and zebra mussel have proliferated to pest status in the Philippines and Great Lakes of North America, respectively, because of favourable environmental conditions and an absence of natural predators (Acosta and Pullin, 1991; May and Marsden, 1992). Ruffe, Gymnocephalus cernuus, switched from a zoobenthos feeder to a zooplantivore when introduced to a Norwegian lake with a different community structure from lakes in the ruffe's natural range (Kålås, 1995).
The US Government subscribes to a precautionary approach in the use of exotic species by establishing research guidelines and performance standards for researchers using genetically modified organisms (ABRAC, 1995). These guidelines, however, do not go as far as they might because these standards do not apply to organisms that are “ … modified solely by intraspecific selective breeding or captive breeding… ” (ABRAC, 1995). They consist of flow charts , decision trees, and worksheets to help researchers reduce environmental risk. Performance standards, that is, the level of precaution researchers must follow, are based on the type of genetic modification, the accessibility of natural ecosystems surrounding the research facility and the status of the natural resources of the adjacent ecosystem.
Pilot scale introductions for research have been proposed as a precautionary approach to species introductions (Turner, 1988; Tiedje et al., 1989). However, the validity of research results from pilot scale introductions has been questioned (World Aquaculture ad hoc Working Group on Hatchery Enhancement; ALCOM/FAO, unpublished report; DMB pers ob.). Ecological interactions at the population and community levels, as well as effects, of an introduction, are often the result of numbers of organisms (Lande, 1991); reducing the numbers may reduce the effect and reduce the probability of success of an introduction. Pilot scale introductions may lead to no effects, neither good nor bad. Pilot scale introductions for research purposes, in order to be of value, should involve large numbers of organisms and become nearly equivalent to full scale introductions.
The use of pilot scale introductions to a confined area has also been proposed as a means to assess adverse impacts (Turner, 1988; Tiedje et al., 1989). However, due to the interconnectedness of all things (Adams, 1985), especially in the brackish and marine environments, confinement may be difficult. Precaution would dictate that a species should be considered suitable for introduction well in advance of the implementation of a pilot scale research programme. A pilot scale programme may be seen by entrepreneurs and some agencies as an unnecessary delay and financial burden.
Reviews which have condensed research results so as to aid in selection of ‘new’ species (Bardach et al., 1972; Korringa, 1976a, b,c; Lutz 1980; New, 1982; Tucker, 1985; Manzi and Castagna, 1986) form a useful precautionary tool in the selection of species for aquaculture introductions. Lee and Wickens (1992) have compared the growth, productivity, stocking densities for a wide range of crustacea adapted for different habitats. General summaries of commercially important species or of those with potential are also of value such as the account on oysters by Arakawa (1990). There are synopses on diseases of organisms used in aquaculture (Bower et al., 1994) and disease transfers are summarised by Sindermann (1993). Sinderman outlines the importance of “transfer networks” of species in aquaculture along which pathogens move. In the case of shrimp these networks are extensive throughout tropical regions of the world (Lightner, 1990).
Technological aspects of managing an established fishery are discussed elsewhere in this volume and are not treated here. Because the use of introduced species requires active intervention by developers, technological intervention can be applied during the period of introduction. In this case the preferred use of technology is to prevent adverse impacts, but it may also be used to correct negative impacts should they occur.
Technologies with hypersensitive analytical tools such as disease diagnostics through enzyme-linked immunosorbent assay (ELISA) and DNA-fingerprinting are becoming applied more to fishery management to reduce the chance of disease introduction and to select appropriate genetic populations (Wirgin and Waldman, 1995). Pathogens and genetic polymorphisms are widespread, but the importance of these to aquatic populations is often unclear. Aquatic organisms that were once considered to be disease free, have now been shown to contain specific pathogens (R. Pascho USFWS in FAO, unpub. report). It is likely that most aquatic organisms carry low numbers of pathogens which will not normally result in problems should its environment remain suitable. Disease can be induced in healthy animals through improper husbandry or through environmental stress.
Researchers in the USA have produced and promoted a Specific Pathogen Free (SPF) strain of shrimp for aquaculture (Wyban et al., 1993). In areas where specific pathogens would be a serious threat, for example BKD in salmon producing areas, other SPF strains of introduced fish could be produced as a precautionary measure. The use of SPF organisms would be only to reduce the chance of the pathogen being introduced; the organism would not be resistant to the pathogen if it were encountered.
The use of marine hatcheries to enhance fisheries is an established practice in many parts of the world and some have utilised introduced species (Bartley, 1995). The use of hatcheries has also generated controversy and there are potentially adverse effects that could arise from this technology (MacCall, 1988; Hilborn, 1992; Bartley, 1995a). The dependence of a fishery on a hatchery provides a level of control should adverse impacts arise. Hatcheries may also provide a useful tool for the management of exotic species in environments which are unsuitable for spawning. Species such as the Pacific oyster and the Manila clam Tapes philippinarum seldom spawn in Britain and Ireland and the culture activities depend on hatchery spat for their production. Spawning does occur in warm summers but recruitment is normally small (Eno, 1995; Minchin, 1993). Hatcheries may release only sterilised fish, thus preventing their establishment in natural waters. However, it is often the desire of a hatchery supported introduction to create self sustaining populations or to contribute to natural recruitment through interbreeding with natural stocks (Bartley et al., 1995).
The ICES/EIFAC protocols (Turner 1988) recommended the use of sterilised individuals to minimise risk of adverse effects from introductions. Triploidization and inter-specific hybridization are two common technologies capable of producing sterile organisms (Khan et al., 1990; Mair, 1993). Using sterile animals gives the importer or hatchery a measure of control over the introduced group of organisms such that if problems arise, releases or further introductions can be stopped. Grass carp used for aquatic weed control are often made sterile by triploidization (Winn 1992); Atlantic salmon cultured in Nova Scotia, Canada must be triploid (therefore sterile) to reduce their genetic impact on natural stocks (McGeachy et al., 1994). Triploid animals should be inspected and certified to be triploid before their use is permitted. The introduction of monosex populations of fish will also reduce the chance of establishing self-sustaining populations in the wild, provided of course that the ‘other’ sex is not present. Groups of fish of a single sex can be produced through combinations of chromosome manipulation, hormone treatment, gamete manipulation, and hybridization (Mair, 1993). However, the use of triploids, hybrids, or mono-sex groups requires either their continuous importation, and therefore continuous inspection and quarantine, or the maintenance of fertile broodstock in country to provide sterile offspring.
Codes of practice governing the use of introduced species have been produced and are probably the single best precaution against the adverse effects of exotic species (Turner, 1988). Codes of practice, such as ICES2(Turner, 1988; ICES, 1995) and NASCO (Porter, 1992) represent a precautionary approach in that they are an a priori policy that forces importers to submit a proposal to use an introduced species and forces managers to evaluate the proposal. The ICES code also calls for a commitment of resources in the form of an advisory panel, quarantine, disease screening, environmental impact assessments, species documentation, monitoring etc., before an introduction is allowed. Codes of practice or guidelines that deal with specialised topics within the broad category of “introductions” have also been created. The North Atlantic Salmon Conservation Organization (NASCO) has promoted guidelines on management of the Atlantic salmon (Porter, 1992). The Office International des Épizooties (OIE, 1995) has developed a prototype aquatic animal health code that contains guidelines for risk assessment, evaluation by competent authorities, and zoning in order to reduce the chance of spreading pathogens when transporting fish.
Figure 1. Main elements of a code of practice for the introduction of aquatic species (Truner, 1988; Bartley, 1995; ICES, 1995)
2 The currently available ICES Code (ICES 1995) is modified from the previous ICES/EIFAC Code in Turner (1988). EIFAC is expected to incorporate further modifications before finalizing their version
The main elements of the ICES Code are summarized in Figure 1 and its historical roots are discussed in Courtenay and Robins (1989). Principle activities to implement the element of the ICES code include, inter alia:
Conduct comprehensive disease and ecological studies in the native habitat in advance of the introduction.
Transfer the introduced species to a secure system within the recipient area
Maintain and regularly sample the contained population, and the water quality therein.
Develop a broodstock in quarantine.
Grow isolated F1 individuals in quarantine
Introduce small numbers to natural waters and continue disease and ecological studies (but see previous Research section).
Implement a monitoring plan to evaluate the introduction.
The ICES Code also recommends with normal trade that regular inspections of live consignments take place. Should unwanted species be found, trade should discontinue until the problem is rectified. Similar approaches should also be taken outside of ICES areas.
Although the elements of the ICES Code appear simple, they may be difficult to carry out. Therefore, protocols and guidelines have been created (ICES, 1984; Turner, 1988;ANSTF, 1994) to facilitate implementation. Practical guidelines must present a range of options that can be utilised depending on available finances, materials, personnel, the state of knowledge on native resources and the introduced species, as acknowledged in Article 15 of the Rio Declaration. This will be especially important in rural and developing areas where facilities, finances and baseline biological information may be scarce.
In the case of temperate marine bivalves, Utting and Spencer (1992) have concluded that there is little requirement for the introduction of further marine species to Britain. This is because of the availability of a wide range of temperate species, including exotics already introduced, for successful management and development of shellfish aquaculture programmes for the foreseeable future. Grizel (1994) considers that with the expansion of aquaculture careful management and continued studies of shellfish must include protective strategies in relation to possible epizootic diseases. Recently in China, production of the bay scallop, Argopecten irradians, has been affected by a haplosporidian disease (Chu et al., 1995). It is not clear whether the parasite came with the original transfer of 26 individuals used as broodstock in 1982, or arose due to adaptations by an opportunistic native species.
In the interest of free trade, some local areas may become subjected to introduced species, as has taken place under the EC Council Directive 91/67/EEC. This Directive permitted transfers of Pacific oysters which previous Irish legislation had controlled (Minchin et al. , 1993). The pacific oysters in cultivation in Ireland before the Directive had been introduced via a quarantine station, Conwy North, Wales and consequently no associated organisms were introduced with them. However, large scale movements of unquarantined oysters are high risk vectors for algal cysts, pests and parasites (O' Mahony , 1993;Dijkema, 1992). The movement of spat, results in a smaller biomass being transferred and consequently a reduced risk of introducing attached organisms, but this may not be adequate in control of the spread of disease causing organisms.
To reduce potential ecological impacts, the use of native species has been proposed, as has the importation of a species into a “vacant niche” in the receiving ecosystem (Coates, 1995). Clearly the use of native species would not be an introduction unless the species was genetically modified prior to release (see following section). However, native species may not be considered as suitable for exploitation because of unknown culture or performance data (Marshall, unpublished report). In addition, local species may be undervalued because they are too common or they are not internationally marketable (Bartley, 1993).
Codes of practice and guidelines that aid implementation should acknowledge uncertainty and avoid making excessive recommendations that require absolute certainty. For example, many conservation geneticists strive to preserve the “evolutionary potential” of a species (Waples, 1991a; FAO, 1993). such a recommendation is a worthy goal, but nearly intractable for policy makers, because of our ignorance of the value of specific genetic resources, how they change over short periods of time, and how they change on an evolutionary time-scale.
Legislation has been enacted in many areas to help control the use and spread of introduced species (Wingate, 1991; Thys van den Audenaerde, 1992; ANSTF, 1994; Anon., 1994a; Windsor and Hutchinson, 1994; S. Sen, unpub. report). The European Union has also established Directives aimed at governing fish movements within the Union (Howarth and McGillivray, 1994). The recently ratified Convention on Biological Diversity (UNCED, 1992) contains articles that specifically address the use of exotic species. Article 8 (g) on in situ conservation states that “ … Each party shall … Establish or maintain means to regulate, manage or control the risks associated with the use and release of living modified organisms resulting from biotechnology…” and 8 (h) states, “ … Prevent the introduction of, control or eradicate those alien species which threaten ecosystems, habitats or species…”.
Coates stated that in regards to introduced species, “… educationis better than legislation…” (ALCOM Technical Consultation, Zambia, November 1994). The U.S. Office of Technology Assessment suggested that Congress, inter alia, expand environmental education on the use and dangers of exotic species (Anon., 1994b; ANSTF, 1994). We could perhaps expand Coates' statement to, “… education and information are better than legislation…”. Toward that end, documentation and dissemination of information on introduced species have been undertaken by FAO (Welcomme, 1988) and are continuing(Bartley and Subasinghe, unpub.) in collaboration with the International Center for Living Aquatic Resource Management (ICLARM) on a relational database on important fishes, FishBase (1995).
Although our knowledge of most aquatic systems is poor or incomplete, the interactions of past introductions may provide information on what might be expected with future introductions and would provide a valuable tool for resource managers and potential importers. The first global coverage of international introductions of inland fishes (Welcomme, 1988 ) is being augmented to include marine and invertebrate species by means of an internationally distributed questionnaire (Bartley and Subasinghe, unpub.); records of introductions are also being complied by H.Rosenthal (in prep.). Many past introductions have not been adequately studied making it difficult to evaluate impacts on ecological or socio-economic systems (Fernando and Holcik, 1991; Bartley and subasinghe, unpub.). Because the use of exotic species will continue, resource managers could help increase the usefulness of these databases by reporting all introductions and their success/failures to international organisations that maintain registries, such as FAO and ICLARM.
The precautionary approach to fishery management as described in FAO's Code of Conduct for Responsible Fisheries has been criticised by the fishing industry as being overly restrictive and placing undue burden of proof on the industry (Anon., 1994c). The International Coalition of Fisheries Associations (ICFA) in raising this criticism stated that a lack of scientific information on fisheries targeting undeveloped or under-utilised species is insufficient reason for setting conservation harvest levels (Anon., 1994c). The precautionary approach with intended introductions must be distinguished from natural capture fisheries because the act of introduction bears some costs in both time and money.
A fishery based on a newly introduced species must be given time to develop and conservative harvest goals are needed, at least initially. The criticism of the ICFA that the precautionary approach should not set conservative quotas on under-utilised or new fisheries (Anon., 1994c) can not be extended to newly created fisheries. In hatchery enhancement or culture based fisheries fishers may expect to increase pressure on a population in light of the large amounts of fish/larvae released from hatcheries. Management must be based on actual contribution of hatcheries to the fishery and not on numbers of fish released. Furthermore, in mixed stock fisheries management needs to set quotas based on the least abundant or most critical stock. Otherwise, the rare stock may be eliminated by fishing regulations that are based on more abundant components of the mixed stock fishery.
In capture fisheries the resource users (fishers) and the resource managers may oppose each other on management issues. However in regards to introductions, there may not be this antagonism as government agencies accounted for approximately 40% of the documented introductions, whereas private individuals and industry account for 15 and 18%, respectively (Bartley and Subasinghe, unpublished data). International organizations were responsible for 7% and 20% of the introductions were made by unknown sources. Resource managers should not be exempt from applying existing codes of practice and guidelines.
A private importer may choose to be very precautious because of legislation, legal responsibilities and the loss of production from choosing the wrong species to import. A common philosophy in environmental management is “the polluter pays”. Exotic species that adversely affect the environment could be considered a form of pollution. The precautionary approach, as defined by Garcia (1994), would seem to dictate that exotic species were pollutants until proven otherwise. Therefore, the importer would be financially responsible for correcting adverse impacts. An importer of exotic species that is financially liable for mistakes should be motivated to make good decisions.
Genetically Modified Organisms
Genetically modified organisms (GMOs) may be considered a special category of exotic species. The underlying difference among all species is their genetic makeup. Therefore, organisms that have had their genome modified by humans, could be considered exotic in relation to the original population. There are a variety of methods available to modify the genomes of aquatic species that include hybridization, chromosome manipulation, selective breeding and gene transfer (Okada and Nagahama, 1993); each has advantages and risks (Hallerman and Kapuscinski, 1992).
There is no universally accepted definition of a GMO. The European Economic Community defines a GMO as “…an organism in which the genetic material has been altered in a way that does not occur naturally by mating and/or natural recombination…” (EEC, 1990). This is elegant in its simplicity and generality, but the EEC goes on to cloud the issue by excluding polyploid induction; the products of selective breeding are not mentioned, neither as a technique that results in a GMO nor as one that does not result in a GMO. ICES has adopted a narrow definition of GMO that refers to basically modern gene transfer techniques in their Codes of Practice (ICES, 1995) and have not included products of conventional selective breeding (J. Carlton, ICES Working Group, personal communication, unpublished report of the EIFAC working group on introductions, Rome, 1994). The Convention on Biological Diversity also adopted a broad definition similar to the EEC's, but then exempts the products of traditional selective breeding. Although the Ecological Society of America suggests regulating GMOs based on their “…biological properties (phenotypes), rather that according to the genetic techniques used to produce them…” (Tiedje et al., 1989), the US Department of Agriculture appears to exclude products of selective breeding from their performance standards (see Research section; ABRAC, 1995). In the United Kingdom GMOs refer to organisms that have genetic material transferred from other species, i.e. transgenic organisms (Woodwark et al., 1994).
Based on the history of animal and plant selective breeding programmes, the Convention on Biological Diversity (UNCED, 1992) wishes to exclude products of conventional technology from excessive regulation (Krattinger and Lesser, 1994). However, terrestrial breeding programmes may not be appropriate models upon which to base regulations for the aquatic sector, partly because so much of aquatic biological diversity is found in wild populations. Norway leads the world in Atlantic salmon production (FAO, 1994), but now farmed salmon may threaten natural runs of salmon through escapes and accidental releases (Gausen and Moen, 1991).
The reasons for the exclusions an ddefinitions of limited scope are fear of consumer rejection of fishery products should they be associated with a ‘mysterious’ scientific technique and fear of excessive regulatory and bureaucratic oversight of such technologies. The precautionary approach to GMOs should require that all genetic modifications be subject to examination and assessment for introduction, regardless of the technology used to create the modification. There may be more uncertainty associated with the production of transgenic organisms, e.g. how and where the new genetic material is incorporated in the genome, how it is inherited, if it is sterile, how it's expressed, and traits that are affected (J. Beardmore, pers. comm.). However, these uncertainties require a thorough examination of the transgenics phenotype. No organism, whether it is transgenic, polyploid, hybrid, or the product of selective breeding, should be released without answering these fundamental questions concerning the phenotype. Simply because a fish is a transgenic, it should not evoke fear; because a fish is the result of conventional breeding should not evoke complacency. Scientists, farmers, resource managers and administrators must look at the end product, not the process that created the product.
In the 1800's ballast was normally in the form of sand or stone. This required special ballasting and deballasting points in order to maintain clear shipping fairways. The process was labour intensive and the first usage of water as ballast provided an immediate advantage as it was less labour intensive and consequently economically more effective. However, the use of water resulted in the movement of species across distinct biological provinces.
Some of the introduced species became invasive. For example, the diatom, Odontella (Biddulphia) sinensis, a tropical species appeared in 1903 in the North Sea forming a dense bloom. This species today inhabits the Baltic Sea (Leppäkoski, 1984) and may have been introduced in ballast water. Similarly, in 1912 the Chinese mitten crab, Eriochir sinensis was introduced to Germany in ballast and subsequently spread its range. In the new environment the crab caused damage to river banks in brackish water areas and siltation in rivers and estuaries, thus contributing to the cost of maintaining shipping channels (Jansson, 1995).
Introductions are taking place throughout the world on a regular basis. Although some notable catastrophes have resulted (see below), the majority of species introduced in ballast water have little major impact on their new environment. For example, the American razor-fish, Ensis directus, is now expanding its range in the southern North Sea (Essink, 1985; Beukema and Dekker, 1995). Those that become established may not become apparent for some time, either because they have little effect in the new environment or because of their size are overlooked. Additionally, the inadvertent or unknown movement of organisms may make determination of their natural range difficult. For example, Cryptonemia hibernica, principally found in the Pacific, has been described from Cork Harbour, Ireland (Guiry et al., 1973); its presence in Ireland is difficult to explain by means other than shipping.
The widespread occurrence of algal blooms throughout the world may in part be due to ship movements. In Australia studies on ballast water by Hallegraeff and Bolch (1991) have revealed 31 viable dinoflagellate species. Five of these were toxic, and included Alexandrium catanella and A. tamarense with estimates of 300 million cysts present in the sediment of some ships. Recent investigations on high liquid performance chromatography of toxins, bioluminescence capacity, morphology and mating compatibility of Alexandrium species in the north-west Atlantic Ocean suggests that there are several strains that can be distinguished according to their geography (Anderson et al., 1994). Similar studies of dinoflagellate bloom species elsewhere may enable the identification of likely transport routes.
Ballast water introductions have been responsible for two recent and notably destructive cases; the introduction of the zebra mussels, Dreissena polymorpha and D. bugensis from the Black Sea to the Great Lakes (Carlton, 1992a). These species have resulted in trophic competition in the Great Lakes, with modification of the abundance of the organisms in the normal food chain. Zebra mussels can remove up to 6.4 million tonnes of phytoplanton, about 26% of the primary production in western Lake Erie (Madenjian, 1995) and occur in sufficient numbers that the dead shells accumulate and stagnate on beaches. The zebra mussels are small, have a high reproductive capability, have few predators in their new environment and can, therefore, spread rapidly. They can sustain some desiccation and hence can be readily transferred among river systems on boats and fishing equipment; their spread is aided by seasonal flooding. The species fouls drinking and industrial water pipes, which require extensive servicing and new management methods . The species still continues to expand and the public is generally aware of its expansion in a well publicised series of messages in newsletters, broadcasts and posters. This species resulted in damages of an estimated $5 billion, primarily through clogging water pipes (Kiernan, 1993).
North Americas ‘exchange gift’ to the Black Sea has been a ctenophore, Mnemiopsis leidyi, introduced in 1982. The ctenophore ranges from Cape Cod, USA to Brazil and consists of a complex of at least six forms, generally considered to be one species (Harbison and Volovik, 1994).In its native habitat it is a voracious consumer of zooplankton and the abundance of copepods is at times negatively correlated with increasing concentration of ctenophores. In The Black Sea and particularly in the Sea of Azov the anchovy, Engraulis encrasicolus and the pilchard, Clupeonella cultriventris, fisheries declined to low levels by 1994 resulting in serious economic and social difficulties and additional pressures on other resources. There have been trophic changes in the normal plankton assemblages (Zaitev, 1993) with a wet ctenophore biomass exceeding 50g/m³ during July to September over large areas of the Sea of Azov (Volovik, et al., 1993). This ctenophore has spread into the eastern Mediterranean since 1992; it is extending its range westwards by natural dispersion, and perhaps in ballast water, and may spread into the Indian and Atlantic Oceans. Sufficient are these problems that the United Nations Environmental Programme (UNEP) have a Working Group including all effected countries to determine how this species may be managed.
Ships with large ballast capacity and fast transit times provide greatest risk for inoculation of exotic species and may even include organisms that affect human health. For example, Vibrio cholerae, the causative agent for cholera, has been transferred from South America to Alabama (McCarthy and Khambaty, 1994) and Clostridium botulinum has been found in ballast water in the United States, Australia and Japan (Anderson, 1992). Harmful species continue to be described such as, pfeisteria piscimorte, a ‘phantom’ dinoflagellate which hatches from a cyst and releases a toxin that kills fish. They feed on fish then re-encyst and have a very complex set of life-history stages (Burkholder et al., 1992). Species such as this and those that cause amnesic shellfish poisoning may be transported in ships' ballast.
Many species have been spread as fouling organisms within and on ships' hulls. Wooden hulls have distributed gribbles, Limnoria spp. and the shipworm, a mollusc, Toredo navalis, throughout most parts of the world in the early years of regular sailing transportation (carlton, 1992a). Following the Second World War the New Zealand barnacle, Elminius modestus, introduced to the south coast of England, has spread to much of northern Europe. Although abundant in several harbours and bays, it does not impinge on local resources significantly .It can beabundant in estuarine regions where it may displace native barnacles. However, the introduction of the Koran sea squirt, Styela clava, to Europe following the Korean War has had some impact on localised industry particularly in port and oyster growing areas (Minchin and Duggan, 1988).
Ships may be capable of transporting organisms in other ways, such as within chain lockers or within other water holding facilities on board. Specialized vessels such as well boats, designed for carrying sea products in trade or for culture, may also facilitate species movements. The transport of oil platforms (Carlton, 1987) or flying boats (Eno, 1995) may also be implicated.
With increased knowledge of ballast movements and the harmful effects that some species can inflict in a new area, a precautionary approach to ballast discharge should be developed. The difficulty is that there is insufficient research undertaken to determine what species are most likely to become invasive or cause adverse impacts, except for the known exceptions mentioned above. It is therefore, prudent to assume that all ballast water will have potential to carry harmful species. Biocides, concentrating and collecting mechanisms, and ballast replacement are methods that, once effectively implemented, will reduce establishment of exotic species introduced via ballast.
Research and Technology
The general concern over the transmittal of exotic species in ballast water and sediment has resulted in several suggestions for their control. However, because of the wide range of taxa and varying resistance of these to different treatment methods, further research is required to determine the most cost effective and practical treatment, or combination of treatments. Current studies into treatment measures include: heat (Anon. 1992), a cooper/silver electrode system (K. Müller, pers. comm.), uv light, hydrogen peroxide, sodium hypochlorite, salt, ozone, reduction in oxygen (Rigby et al., 1993). Mid-ocean exchange for freshwater ballast enables dilution and a change of physical conditions. This will have an effect on the planktonic organisms, but the biota in sediments may not be affected. Apart from removal of sediments in dry-dock and reballasting at sea; there are no other generally accepted or applied control techniques.
Apart from tankers, most vessels are unable to pump their ballast ashore. For most ships the treatment of ballast water is not feasible. Because of difficulty of access, even sampling of ballast is difficult. Bulk carriers are the easiest to sample and the majority of studies to date have been on this type of vessel. It is not known whether studies on bulk carriers will reflect the patterns of diversity and survival found in vessels with more sealed ballast units. Studies of organisms in ballast water, where they may be deprived of light, with consequent changes in their rate of assimilation of food and behaviour may provide useful information that would aid new vessel design, either of continuously flushed ballast while in transit or positioning of equipment to make treatments more effective.
Dinoflagellates are of particular concern, their resistant cysts accumulate in sediments, and may remain viable for some years. The ballasting of dinoflagellate contaminated water may lead to inoculations in ports in succeeding years. Consequently the removal of ballast sediment of ships when dry-docked is a wise precaution. It would also be prudent to enable settlement of ballast sediments should ballast discharges in port be inevitable. The turnover of these cysts in sediments either by bioturbation or resuspension as a result of ballasting or poor sea state remains unstudied. Research projects involving ballast water and sediment need to be expanded. The early studies conducted on bulk carriers arriving in Australia from Japan demonstrated that significant numbers of toxic dinoflagellate cysts were indeed carried by this means (Hutchings, 1992). The Smithsonian Environmental Research Center has a current programme which includes work between the USA and Germany examining the prevalence of various taxa, including algal cysts, and application of IMO guidelines (see following section). This follows the work of the United States National Biological Invasions Shipping Study.
It would appear that those countries most affected by ballast water discharges are currently the most concerned. In northern Europe and North America there are a number of desk studies undertaken to quantify the diversity of introduced species, likely introduction sites and relative risk of different introduction vectors (Carlton, 1992a, b; Mills et al., 1993: Jansson, 1995: Eno, 1995; Minchin and Sheehan, 1995; Carlton, 1993; Mac Donald, 1995). The EU are likely to support studies in this area as a result of the serious economic consequences of introductions elsewhere.
Ballast may require different treatments depending on where the ship originated. However, research within this area is still needed. Little is known on the biological effects of light deprivation, ship vibration, duration within ballast tanks of marine organisms. Certain taxa will predominate within ballast water on account of their behaviour and whether they have planktonic stages may be more prone to being removed in ballast (Carlton, 1993). The survival of organisms in ballast water will depend on voyage duration, with few species expected to survive journeys of 24 days (Williams et al., 1988). Dinoflagellate cysts, may be capable of resting several years and some have a required dormancy period before hatching (Anderson, 1980). Studies by Locke et al. (1991) demonstrate that re-ballasting at sea of vessels due to enter the Great Lakes in about 67% effective in eliminating freshwater organisms despite compliance of re-ballasting at sea by 90% of vessels.
Those areas most likely for establishment of an introduced species are lagoons and port areas (Boudouresque, 1994). Care must be taken to find suitable ways of reducing the overall impact of ballast water in areas of partial containment which may enable a small innoculum to establish an exotic population.
The utilisation of effective antifouling applications, such as the use of organotins have reduced the overall biomass of fouling organisms. Such substances are sufficiently toxic that they can also result in species eradication near ports. The use of these substances is being reviewed and several alternative methods are being investigated so that a similarly effective antifouling substance can be produced that will deter fouling yet be more acceptable environmentally. Future antifouling applications will need to be equally as effective as organotin preparations.
The International Maritime Organisation (IMO) has produced “…Guidelines for preventing the introduction of unwanted aquatic organisms and pathogens from ships' ballast water and sediment discharges…” (Anon., 1993). It is generally accepted that prevention is unrealistic and efforts should stress “…minimizing the introduction of unwanted organisms…” (Anon., 1994a,d). These guidelines are actively pursued in Australia and New Zealand and are endorsed by the United States and Canadian Coast Guard for vessels entering the Great Lakes (Anon., 1991).
The first control measures on ballast water were introduced by the Canadian Coast Guard in 1989 based on voluntary management of ballast water in ships entering Canadian waters. These procedures resulted from the introduction of a number of invasive species into the Great lakes, principally imported from Europe (Mills et al., 1993). The voluntary requirement was that ships entering the Great Lakes would flush their tanks at sea before entry into the St Lawrence Seaway. Legislation was enacted in the United States under the Non-indigenous Aquatic Nuisance Prevention and Control Act in 1990.
Formalization of present guidelines into legislation or a code of practice for ballast water, is urgently required, but is hindered by the lack of research information on which to base useful decisions and the knowledge that ballast tank or ship design for most vessels will not change for several years, except perhaps in the commissioning of new vessels. In Australia, Canada, and the USA there are measures for the control of ballast water by shipping. Due to difficulties in the mid-ocean exchange of ballast compliance may be difficult because of structural limitations and the dangers to the ship and crew. Secondary deballasting areas exist for those vessels entering the Great Lakes that have these difficulties.
A code for the management of ballast water needs to evolve from scientific studies on control of durable and potentially harmful species likely to be carried in ballast water and discharged in recipient ports. Control mechanisms may require studies of the resting stages of diverse phyla that may respond to different stimuli or be subject to different chemotheraputic techniques. The present guidelines are based on dilution of the numbers of organisms by the recommended mid-ocean exchange, or by flusing the tanks with water with properties unsuited for the organisms contained in the ballast. These methods probably reduce the potential of an innoculum establishing populations in a new locality. Future control methods may be greatly aided by changes in the design of ships ballast tanks that facilitate access and treatment methods.
As a result of finding viable cysts of toxic dinoflagellates and other non-native species in ballast waters and sediments, the Australian Quarantine and Inspection Service developed special quarantine measures in February 1990 which requested shipping to comply with one of the following options (Hallegraeff and Bolch, 1991);
Have a certificate to indicate that the port of origin is free from toxic dinoflagellates, (this is difficult because such events are often sporadic and can occur within hours, ballast water and in particular sediments may have accumulated as a result of previous re-ballasting in other ports. Dredging activities may result in suspension of cysts, which otherwise may have remained unavailable to ballasting.).
Provide evidence that they have reballasted at sea (this may not result in the purging of ballast sediment).
Provide evidence that they have treated the ballast water (no single treatment method is currently recognized).
Discharged their sediment in designated and ‘safe’ areas (this assumes that this practice reduces the risk of a successful inoculation).
That ballast does not contain sediment and was not loaded during a toxic bloom (sediment inevitably will collect in ballast tanks).
That ballast will not be discharged in Australian waters.
Similar guidelines have been adopted by the IMO (Anon., 1991, 1993).
Because effective management still requires much research, according to ships port origin, duration at sea, volume of ballast, deballasting provisions etc., a precautionary approach considers that the following measures would reduce the chance of a successful inoculation:
Intake of ballast water should be avoided when “coloured” water is present because this may contain algal blooms or organisms associated with sediments.
Dilution of the organisms in the ballast.
Changes, such as temperature and salinity, in ballast water may create unfavourable conditions for the contained organisms. This, together with the effect of dilution is the principle involved in mid-ocean exchange.
De-ballasting before entering port.
Treatment of the ballast
Special ballasting facilities ashore.
Do not de-ballast.
The establishment of a database of harmful, toxic or potentially nuisance species would aid the management of ballast water. The International Oceanographic Commission has established a reporting structure of Harmful Algal Blooms. This database could be entered into a global shipping network register so that port authorities may be alerted of ballast posing potential risk in advance of a ship entering port. A computer alarm system based on the port of origin, or ship track, could be used to provide a warning system in advance of the ship arriving in port so that appropriate methods for dealing with the ballast water might be considered and employed.
The physical conditions of ports could be registered in a database. When a ship leaves one port for another, these physical characters could be compared between the two ports. Close similarities between the two would indicate a higher probability of ballast water discharge producing a new population in the recipient port. Harmful species known to occur in some port areas should be entered into a similar database, together with recent account of any algal blooms. Such information, if it were made readily available, would aid in the management of ballast water. However, at present, this information is not generally available.
Although not intended to prevent introductions of species the application of biocidal films have reduced fouling in order to reduce the costs incurred by hydrodynamic drag. The economic savings by utilising an efficient biocide will mean faster ship travel and reduced fuel consumption. Effective antifouling applications, such as the use of tributyl-tin have reduced overall biomass of fouling organisms and approximately 69% of ships are being painted with TBT antifouling (Ambrose, 1994).
Such substances, however, are sufficiently toxic to result in environmentally toxic conditions for a wide spectrum of organisms within some estuaries and bays. The IMO have proposed a ban on the use of TBT on all vessels less than 50m (Anon., 1994d). Legislation in many countries has controlled its use, with a general ban on vessels, most usually, below 25m. Shipping port areas continue to have environmentally high levels of TBT (Davies and Bailey, 1991; Uhler et al., 1993; Minchin et al., 1995a,b,c) and this may have some effect on the suppression of biotic innocula. The IMO are anxious to find a practical alternative for the replacement of this substance because of its toxic nature and several alternative methods are being investigated so that a similarly effective antifouling substance can be produced that will deter fouling and will be more environmentally acceptable.
Other vectors for the inadvertent introduction of aquatic species into nature are associated with the careless actions of many individuals, such as boaters, recreational fishermen, and pet-fish owners. For example, the range of the crayfish plague within Europe may have been extended, in part, by transferral of contaminated fishing gear. There is an extensive trade in freshwater and marine aquarium species throughout the world which may result in the introduction of organisms and diseases (Courtney and Stauffer, 1990). Establishment of the benthic alga Caulerpa taxifolia, in the Mediterranean probably resulted from fragments being released from a public aquarium facility, where it had been on display for some years (Meinesz and Hesse, 1991; Boudouresque, et al., 1992). This Pacific species has become invasive within the western Mediterranean and appears to have mutated to produce a more tolerant cold water form (Sabatini, pers. comm.).
Disposal of live packing materials may have lead to the establishment of the exotic shore crab Carcinus maenas in San Francisco Bay (Cohen et al., 1995). It may have arrived there within ballast water transfers, or with seaweed packing used in shellfish shipments from the Atlantic coast. The algae Fucus spp. and knotted wrack, Ascophyllum nodosum are used for this purpose and small shore crabs are common within these materials. These Atlantic algae have also been found in San Francisco Bay. The careless disposal of materials considered to be waste may be a frequent; the disposal of unwanted food items which were considered unfit as food or dead, but were in fact alive, may also be common.
Thus, the application of codes or guidelines is difficult and enforcement of controlling legislation, if any exists, is difficult or impractical. Public education and awareness campaigns are probably the best means to reduce these types of inadvertent introductions and promote responsible actions by the many individuals using the aquatic environment. Some pet-fish retailers are already distributing pamphlets on the dangers of escaping or released aquarium fish. Sterilisation of fishing equipment and boat hulls is being undertaken to help restrict the movement of zebra mussels (J. Carlton, pers. comm.). Now that we understand that animals can be introduced in algae used in packing, research on practical disposal and treatment, such as immersion of algae packing material in hypo-osmotic water, or replacing algae with biodegradable material may help avoid future inadvertent introductions.
The purposeful introduction of aquatic species is a management strategy to increase production and profits from fisheries. There are research and technological aspects of this strategy to which the precautionary approach can be applied. Implementation of Codes of Practice such as ICES represent the single best form of precaution in the purposeful import of exotic species. The codes require planning, approval, containment and both ecological and social evaluation. The methods and level of implementation will depend on local circumstances and resources. The documentation of the impacts of species introductions will also provide an increasing store of information that should be readily available through international organisations. By following the principles in the code, updating databases and other sources of information and then referring to these information sources, uncertainty can be reduced and the use of exotic species can proceed in a responsible manner.
Unintended introductions continue, the vectors by which these take place are known and measures to reduce the impact via these sources will require careful management to identify precisely how these risks may be minimised. A positive approach is to advise the public generally about the likely methods and consequences of introductions so that responsible action from the public is possible, recommendations to the trade and codes of practice should help to reduce unwanted introductions. The highest risk would appear to be from ballast water and sediments, further research into control methods and the biology of taxa contained in ballast water is needed to aid in ultimate recommendations for treatment. The use of the IMO Code, which recommends re-ballasting in the ocean may significantly reduce the viability of a ballast inoculation. If actions are not taken there will be a continuing trend toward cosmopolitan flora and fauna which will continue to impact human activities.
We gratefully acknowledge the contributions of J. Beardmore (UK), S. Bellan-Santini (France), J. Caddy (FAO), J. Carlton (U.S.A.), D. Coates (FAO), C. Eno (U.K.), B. Marshall (Zimbabwe), K. Muller (U.K.), R. Pascho (USA), H. Rosenthal (Germany), S. Sen (UK), M. Sharriff (Malaysia), and R. Subasinghe (FAO).
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