16798 Hillside Drive
Sparwood, B.C.
CANADA V0B 2G3
2Inland Water Resources and Aquaculture Service
FIRI, FAO, Viale delle Terme di Caracalla
Rome 00100, ITALY
Arthur, J.R., and R.P. Subasinghe. 2002. Potential adverse socio-economic and
biological impacts of aquatic animal pathogens due to hatchery-based enhancement
of inland open-water systems, and possibilities for their minimisation. p. 113-126.
In: J.R. Arthur, M.J. Phillips, R.P. Subasinghe, M.B. Reantaso and I.H. MacRae.
(eds.) Primary Aquatic Animal Health Care in Rural, Small-scale, Aquaculture
Development. FAO Fish. Tech. Pap. No. 406.
The introduction of exotic fishes into natural waters, and the culture and stocking of both introduced and indigenous species to enhance production from freshwater artesianal fisheries has often produced significant socio-economic benefits to small-scale rural fishing communities. These include increased availability of freshwater fish as a source of dietary protein for the rural poor, and an increased and more stable income for small-scale fishermen, fish sellers etc., their immediate families, and rural communities at large. However, to avoid unanticipated adverse effects on local communities and aquatic ecosystems, such programmes for improvement of existing fisheries must be well designed, taking into consideration not only social aspects (e.g., local preferences and traditions with regard to fish consumption), but also potential impacts related to the biology (predation, spawning habits, competition with native species etc.), genetics (possibility of hybridisation with native species, possible over-exploitation of less abundant native species with increased fishing activity), and the disease status of the enhanced species. The introduction of exotic pathogens along with introduced aquatic animals has too often resulted in severe socio-economic and/or ecological impacts. In most cases, such impacts can be avoided, if fisheries managers follow internationally accepted procedures (e.g., the protocols of the International Council for the Exploration of the Sea, ICES) when importing exotic fish. Enhancement of artesianal fisheries by stocking of hatchery-reared fry of native or well established and widespread introduced fishes (such as the Chinese and major carps in Bangladesh), poses much less threat with regard to pathogen spread. If broodstock are obtained locally, all pathogens will already be present in the country and most will probably already be widely distributed in natural waters. However, good hatchery management practices, including rigorous screening of broodstock for pathogens and routine disease diagnostics and treatment of fry and fingerlings will do much to reduce the possibility of stocking unhealthy seed (with resulting poor survival and/or production) and the potential for spread of disease into new areas.
In this short discussion paper, we address, in a broad context, the potential socio-economic and biological risks associated with the introduction of exotic species for various purposes, among them inland-water fisheries enhancement and stocking in large water bodies and floodplains, and look at options to minimise these hazards. We will look at a few hard lessons learned from past experience, and then briefly examine the risks and benefits of hatchery-based enhancement and stocking programmes. We will also try to address these issues within the context of inland fisheries enhancement in Bangladesh.
The use of exotic aquatic species to increase food production and income has been an established practice since the middle of the Nineteenth Century. However, the practice dates back much further, to the ancient Romans and medieval European monks, who transported common carp, Cyprinus carpio, and perch, Perca fluviatilis, around Europe and the Roman Empire; and to the Greeks, who transplanted oysters around the Greek Islands during the Golden Age of Greece. Advances in controlling the spawning of salmonids, primarily rainbow trout, Oncorhynchus mykiss, in the mid-1800s led to increased exportation of these fish to other areas (Welcomme 1988). Recent advances in trade and transport have made large-scale movements of many different species over great distances possible.
Controversy over the use of exotic species stems from the many highly publicised and spectacular successes and failures. For example, Chile has become the world's second leading producer of farmed salmonids because of the introduction of coho salmon (O. kisutch), Atlantic salmon (Salmo salar) and rainbow trout. The Chilean salmonid culture industry provides foreign exchange and employment for thousands of people in areas where there are few other opportunities for development. In contrast, the introduction of the golden apple snail (Ampullaria canaliculata) to the Philippines to increase rural aquaculture production has lead to the infestation of 15% of the Philippine rice fields, with losses in some areas as high as 75%. Perhaps the most famous controversy is the introduction the Nile perch (Lates nilotcus) into Lake Victoria. As a result of this introduction, a primarily artesianal fishery turned into a multi-million dollar industrial fishery and processing operation. Tremendous income was generated, but the socio-economic system of the community surrounding the lake changed, and there have been estimates that perhaps hundreds of enzootic species of fish have been lost to predation by the Nile perch.
Statistics on the introduction of inland aquatic species provided by the Food
and Agriculture Organization of the United Nations (FAO) (see Table 1) show
that aquaculture development has been the primary reason cited for most introductions,
accounting for almost 40% of all cases. Other important reasons cited for the
introduction of exotic species include development of capture and sport fisheries,
accidental introductions (escapes), ornamental fish culture, research, control
programmes for insects and aquatic plants, use as bait etc.
Table 1. Reasons for introduction of exotic species.1
Welcomme (1988) listed 1,354 international movements of 237 species of inland fishes. Of the 237 species, the three most widely introduced were common carp, Nile tilapia (Oreochromis niloticus) and rainbow trout. These three and others, such as black bass (Micropterus spp.), mosquitofish (Gambusia affinis), and grass carp (Ctenopharyngodon idellus), now occur on every continent except Antarctica as the result of human-assisted movement (see Table 2).
Table 2. Most often introduced fishes.1
FAO statistics also show that there has been an exponential increase in the number of introductions since 1940 (Table 3), and that this trend has continued during the past 20 years. This increasing trend towards the international movement of live aquatic animals has been made possible by advances in transportation that allow rapid shipment of live fish and shellfish throughout the world, and to a large extent, is directly related to the global development of the aquaculture industry and the concomitant demand in many countries for new species for culture.
Table 3. Statistics by year of introduction.1
It has become increasingly clear that many of the human-assisted movements of aquatic animals into new areas have also been responsible for the introduction, establishment and spread of pathogens and parasites into new geographic areas. Hoffman (1970) and Bauer and Hoffman (1976) summarised the state of knowledge on the transfers of fish parasites along with host movements through human activities. Although Hoffman (1970) was able to document movement and establishment on new continents of at least 48 species of parasite (5 Protozoa, 31 Monogenea, 3 Nematoda, 5 Digenea, 1 Acanthocephala and 3 Copepoda), it is clear, given the number of host species that have been moved, that the actual number must be much higher. For example, Arthur (1995) noted that 50% (9 of 18) of the parasites known from Nile tilapia in the Philippines were probably introduced into the country along with the introduction of this fish for aquaculture and stocking in natural waters. Given that the number of transfers and introductions has increased significantly with the increased ease of air travel and the recent explosive growth of the aquaculture industry, and that movements of other types of pathogens (e.g., viruses, bacteria, fungi) have not been considered, the pathogens that have been moved and are now established in new localities must number in the thousands. In general, fisheries managers must be faulted for not giving pathogens adequate consideration when contemplating introductions and transfers of aquatic animals. In many cases this has led to serious pathogens becoming established in new areas and hosts. Once established in natural waters, such pathogens are usually impossible to eradicate. With proper planning, the introduction of many these disease agents could have been avoided.
There are a number of international codes of practice and guidelines which,
if followed by fisheries management, would do much to reduce the risk of introducing
pathogens into new areas along with the movements of their hosts. The Office
International des Épizooties (OIE) has developed recommendations and
protocols for the prevention of the international spread of diseases of aquatic
organisms as part of its International Aquatic Animal Health Code (OIE 2000),
which deals with the health surveillance of animals for domestic and international
trade. Recommendations for policies dealing with the introduction of aquatic
species and guidelines for their implementation, including methods to minimise
the possibility of disease transfers, have also been developed by the International
Council for the Exploration of the Sea (ICES) for marine introductions (ICES
1995). More regionally oriented guidelines are provided by the Great Lakes Fish
Disease Control Committee of the Great Lakes Fishery Commission (Meyer et al.
1983) and the North American Commission of the North Atlantic Salmon Conservation
Organisation (Porter 1992), among others. Regionally, there have been a number
of initiatives (see Arthur 1996), the most recent being the FAO/NACA (Network
of Aquaculture Centres in Asia-Pacific) "Asia Regional Technical Guidelines
on Health Management for the Responsible Movement of Live Aquatic Animals and
the Beijing Consensus and Implementation Strategy" (see FAO/NACA 2000).
Despite these various codes, protocols, and guidelines, fish and shellfish continue
to be introduced into new areas with little consideration of potential disease
consequences. There exists an enormous number of documented cases where parasites
and diseases have been spread to new regions due to human activity (for examples,
see the summaries by Hoffman 1970, Bauer and Hoffman 1976, Bauer 1991, Williams
and Sindermann 1992, Humphrey 1995, and Arthur 1995). Most well-documented cases
involve international movements - diseases introduced along with exotic fishes,
and the subsequent spread of these exotic species and their pathogens within
national borders. Because transfers (movements of aquatic animals to areas within
their areas of historical distribution) are generally less controversial, they
appear to be less often documented, and the possible concurrent movement of
pathogens and parasites less well investigated. Never-the-less, there are equally
valid concerns regarding transfers of aquatic animals. One of these is the potential
for introducing new diseases and/or new strains of established pathogens that
may be specific to the host species being transferred. Because of this specificity,
these pathogens or strains may increase the chance of a disease incursion that
will severely impact existing wild and cultured populations of the species.
Introductions and transfers of aquatic animals have often occurred with little apparent repercussions due to exotic disease introduction (although, this may be due, to a large extent, to lack of any detailed pre- or post-introduction studies). However, there are many examples where ill-considered introductions of fish and shellfish have resulted in the spread of exotic pathogens that have caused unexpected and far ranging adverse impacts on host populations and commercial and sport fisheries, with accompanying severe socio-economic impacts on human populations. The following section presents three examples involving finfish, one of historical interest, and two of recent occurrence that continue to have major effects on inland capture and sport fisheries.
The first scientifically documented case of the devastating effects exotic pathogens can have on a previously unexposed fish population was apparently reported by Dogiel and Lutta (1937). In an investigation into mass mortalities of spiny sturgeon (Acipenser nudiventris) in the Aral Sea, these authors found that the gills this extremely valuable fish were severely infected by a large, blood-feeding monogenean, Nitzschia sturionis. This monogenean was unknown in the Aral Sea prior to 1936; however, in 1934 spawners of the Caspian stellate sturgeon (A. stellatus) were transferred by fisheries managers from the Caspian Sea into the Aral Sea without inspection by fish disease specialists. As all Caspian sturgeon were known to be suitable hosts for N. sturionis, it was clear that these mortalities were due to the introduction of this parasite into a new water body where it was able to infect and severely damage populations of a previously unexposed host species.
As a result of this study, Dogiel and Lutta (1937) made the following recommendations, which are still valid, but often unheeded today:
1. "When introducing new objects which are useful for the fishing industry, it is necessary to hinder the spread of harmful organisms. Further transfers and adaptations in order to make our basins richer in new valuable fish species must be carried out under the control of specialists in fish diseases."
2. "Transfers from infested basins are to be prohibited pending full cessation of liquidation of the epizootic. Thus, the further transfer of spiny sturgeon from the Aral Sea to other basins must be prohibited."
The story of the spread of Myxobolus cerebralis, the causative agent of whirling disease in rainbow and cutthroat trout, into the rivers of the western United States provides evidence of the serious impacts exotic diseases can have on natural fisheries. Myxobolus cerebralis is a myxozoan parasite first found in North America in 1956 in Pennsylvania (Bergersen and Anderson 1997), and is believed to have been imported into the United States along with shipments of infected European trout (see Hoffman 1963). The parasite infects, but causes no apparent disease, in brown trout (Salmo trutta), however, rainbow trout are highly susceptible (Hoffman 1970). Small trout are severely affected, the pathogen infecting and eroding cartilage and weakening the skeletal structure. By destroying the auditory capsule, equilibrium is affected, producing the characteristic clinical sign of whirling.
Myxobolus cerebralis has gradually spread westward, and was first detected west of the Mississippi River in 1965 in both California and Nevada (Bergersen and Anderson 1997). It is now distributed in 21 states having self-sustaining trout populations. Until the 1990s, whirling disease was considered a manageable problem affecting rainbow trout in hatcheries. However, it has recently become established in natural waters of the Rocky Mountain states (Colorado, Wyoming, Utah, Montana, Idaho, New Mexico) where it is causing heavy mortalities in several trophy sportfishing rivers. An example is its impact on the rainbow trout population in the Madison River, Montana.
The Madison River is one of the best known sportfishing rivers in western North America and is a Mecca for fly fishing enthusiasts from around the world. Although the rainbow trout populations in the Madison first began a noticeable decline in 1991, it was only in December 1995, when brown trout and rainbow trout collected in the upper river were found to be positive with spores of M. cerebralis, that the cause of this decline became known. This discovery was the first known finding of this parasite in Montana, and culminated a four-year search for factors which could explain the large population decline in wild rainbow trout in this important sport fishing river. As a result of declines in annual recruitment due to M. cerebralis infections, the adult population of rainbow trout experienced steady decline such that by 1994, the total number of two-year-old and older trout in the river had decreased nearly 90%. Prior to the introduction of whirling disease (pre-1991), wild populations of rainbow trout one-year-old and older averaged about 3,800 per mile, with yearling trout comprising about 58% of this number. Numbers of yearling rainbow trout ranged between 1,172-2,602 per mile and averaged 2,198 per mile. During the immediate eight years post-whirling disease introduction, the average number of yearling rainbow trout was 507, a decline of 77%. As a result of this decimation of the juvenile trout population, the number of two-year old and older trout showed an even more dramatic decline (89%), the average number being slightly less than 500/mile of river (Vincent and Byorth 1999). An example of the impact of whirling disease on one section of the river is shown in Table 4.
Table 4. Example of the impact of whirling disease on Madison
The history of epizootic ulcerative syndrome (EUS) in South and Southeast Asia is well known to all fish health workers in the region, as this condition has been the major cause of losses of freshwater fishes for more than two decades (see Lilley et al. 1992, Roberts et al. 1994, Das 1997).
The socio-economic impacts of exotic aquatic animal diseases have been severe, and many instances involving freshwater fishes and brackishwater prawns are documented in other papers contained in this volume. An example of the impacts exotic diseases can have on rural communities is provided by EUS.
Among the diseases affecting freshwater aquaculture and capture fisheries in developing countries of Asia, EUS has had by far the most serious socio-economic impacts. These include direct economic losses to small-scale fishermen and aquaculturists due to high mortalities of wild and cultured fish, and indirect losses due to collapsed markets for fish, resulting in loss of employment opportunities to fish sellers, transporters, processors and those involved in selling supplies and equipment used by all these sectors.
Examples of the effects of this disease on local economies, and its severe impacts on rural fishing communities are provided for Bangladesh by Barua (1994) and for India by Das (1994). EUS was first confirmed in Bangladesh in 1988, before which such large-scale fish mortalities had never been seen in the country. The disease first appeared in irrigation canals in the Chandpur District, about 200 km from the Myanmar border, and may have occurred in water bodies in districts bordering Myanmar the previous year. The disease then spread in all directions, affecting the entire eastern and central parts of the country within nine months, then spreading northward during the flooding of September 1988. The first outbreak, which lasted 13 months, was followed annually by less severe outbreaks during October to March. EUS caused severe socio-economic impacts, including a sharp drop in the price of fish, as consumers avoided eating fish. As in other countries, this was based on unfounded fears that consuming EUS-affected fish would affect human health, causing illnesses ranging from skin lesions to death. The nature of the disease was irresponsibly reported by some sectors of the media, resulting in fear and confusion among the rural population. The result was a drop in demand and supply of fish by some 64.5%, with prices falling 50-75% in badly affected districts. Total economic losses due to EUS were estimated at $US3.38 million during the first outbreak and some $2.24 million during the second occurrence.
By May 1988, the disease had spread into the northeastern states of India (Das 1994), and by 1990 outbreaks had occurred throughout much of the country. As in Bangladesh, sectors dependent upon capture and culture of fish were severely affected. A study conducted in five districts of Kerala showed that EUS had completely disrupted the inland fish market. The economic situation of small-scale fishermen and fish vendors, many of them women, was particularly affected, farther marginalising this segment of the rural poor and forcing many to seek employment in the most impoverished sectors such as agricultural labourers, head-load and quarry workers etc. with little success. The disease also affected small-scale aquaculturists. In five districts of West Bengal, for example, 73% of aquaculture operations were adversely affected. Aquaculturists suffered direct losses due to mortalities in the ponds. Some 42% suffered losses of 31-40% of their stock, while another 25% had losses of between 21 and 30%. Additional indirect losses were also felt due to severely affected markets.
Similar scenarios have been played out in many of the developing countries in South and South East Asia (see Lilley et al. 1992, Roberts et al. 1994). Total losses due to EUS in the region are impossible to calculate with any degree of accuracy, however, estimates for only four countries (Thailand, Bangladesh, Sri Lanka and Nepal) for limited periods up to 1990 total more than $US15 million (see Lilley et al. 1992) (Table 5). A substantially larger estimate for Thailand is given by Chinabut (1994), who suggested that Thai losses due to EUS may exceed $US100 million.
Table 5. Some estimates of economic losses due to EUS.
It is only recently that the potential effects of pathogens on aquatic biodiversity have begun to be investigated. However, it is becoming increasingly clear, from both a theoretical and field perspective, that pathogens may determine aquatic community structure and regulate host abundance (see, for example, Marcogliese and Cone 1997, Marcogliese and Price 1997). Some of the effects of parasites (and of other pathogens) on their hosts, which may affect community structure and host abundance, include altered energetic demands, altered behaviour, increased mortality, reduced fecundity, altered nutritional status, reduced growth, modified interspecific competition, enhanced susceptibility to predation, altered mate choice and sex ratio (see Marcogliese and Cone 1997). It would thus seem logical that introduction of exotic fish and shellfish pathogens into new ecosystems may have far-reaching, if unpredictable, impacts on aquatic biodiversity.
The unanticipated results of transfer of stellate sturgeon infected with Nitzschia sturionis from the Caspian into the Aral Sea was the devastation of the local population of spiny sturgeon in the Aral Sea, which was depleted for more than two decades (see Bauer and Hoffman 1976). Another parasite, the monogenean Gyrodactylus salaris, believed to have been introduced from Sweden to Norway about 1975 as a result of movements of Atlantic salmon for stock enhancement, has been responsible for the complete destruction of more than 30 populations of Norwegian Atlantic salmon (Heggberget et al. 1993).
Because of its high pathogenicity to wild rainbow trout, whirling disease can pose a threat to genetic diversity by severely effecting local populations or strains. For example, Walker and Nehring (1995) provided the first account of a wild rainbow trout population in Colorado so severely affected by whirling disease that its continued existence as a self-sustaining fishery was seriously in doubt. Because certain strains of rainbow trout may have innate resistance to whirling disease, it is possible that genetic diversity could be reduced by the selective mortality of non-resistant populations. Also, the identification and use of resistant strains of trout as an enhancement strategy by fisheries managers might also, as a by-product, contribute to the reduction or extinction of non-resistant strains. Any such reduction in genetic diversity could lead to increased genetic homogeneity, reducing the ability of a species to respond to challenges posed by subsequent new pathogens.
Although more than 100 species of fish have been affected by EUS (see Lilley et al. 1992, Chinabut and Roberts 1999), some species are much more affected by the disease. Populations of snakeheads (Channa striata, and to a lesser extent other Channa spp.) are reported to be most severely impacted, such that during the outbreak of EUS that occurred in 1988 in Bangladesh, investigators were unable to find any healthy snakeheads in affected waters (Roberts et al. 1989). Other species considered to be highly affected by EUS include air-breathing fishes such as Fluta alba, Trichogaster pectoralis, Mastacembelus armatus, Anabas testudineus, Clarias batrachus, Heteropneustes fossilis, and the major carps (Catla catla, Cirrhinus cirrhosus and Labeo rohita). Although it seems likely that outbreaks of EUS have changed the population structure and perhaps, species composition of many water bodies in South and Southeast Asia, detailed quantitative studies have not been conducted. However, observations made my many workers suggest the effects on some species, such as striped snakehead, have been dramatic. For example, Barua (1994) noted that following the outbreaks of EUS in Bangladesh in 1988 and 1989 snakehead populations were so severely decreased that few fish were seen in local markets during this period.
Data given by Das (1994) comparing landings at the Jorhat Fish Assembly Centre
in Assam for species of EUS-affected fish from the capture fishery in the Brahmaputra
River system before (1987-88) and during the initial (1988-91) three years in
which outbreaks occurred in India show declines for highly susceptible species
of as much as 98% (Table 6). Species most severely affected included Channa
punctata, C. striata, Nandus nandus, Puntius spp., Amblypharyngodon mola, Labeo
rohita, L. bata and C. cirrhosus. Such data indicate that the fish population
structure in this major river system was severely altered by the introduction
of EUS.
Table 6. Impact of EUS on local abundance of highly susceptible species.1
The use of hatcheries to provide fry and fingerlings for stocking into natural waters and man-made ponds offers many potential benefits to rural communities. These include increased fish production, increased protein availability, increased and/or stable incomes for fishermen, fish sellers etc., and mitigation of losses caused by development due to dams, embankments for flood control, road ways, agriculture etc.
The use of hatcheries, as opposed to other means of stock enhancement (protection of habitat etc) has been the subject of much discussion (see, for example, LaPatra et al. 1999, Hilborn 1999, Waples 1999). Concerns include genetic issues (e.g., loss of intra-species variability, impacts on biodiversity through increased fishing pressure on less common species), ecological issues (e.g., effects due to habitat destruction, competition and predation) and diseases issues (introduction and/or spread of exotic pathogens). While there remain concerns related to genetic issues (i.e., "domestication" of wild stocks) that may be inherent in hatchery-based enhancement, issues surrounding possible pathogen introductions can, for the most part, be addressed by the careful use of existing protocols to insure that fish being introduced are free of potential pathogens.
With regard to Bangladesh, many of the concerns related to introduced pathogens and to proposals for enhancement of native fish stocks expressed above may not come fully into play. Because Bangladesh shares major waterways with the neighbouring countries of India, Nepal and China, it is impossible to prevent the spread of diseases into the country from neighbouring countries by natural means (e.g., by movements of fish hosts or by water currents). Bangladesh is also subject to annual flooding, which permits almost unrestricted host movements throughout the country through interconnected waterways. As a result, most parasites and pathogens, once present in Bangladeshi waters, are likely to obtain widespread distribution by natural means. Also, this absence of natural boundaries probably leads to relative genetic homogeneity (i.e., an absence of races or stocks) of fish in these flood plain systems.
The proposed stocking of native species (major carps) using locally obtained broodstock should not pose major threats with regards to the spread of pathogens, as any pathogens infecting the offspring will be species which are already enzootic in the area. Finally, in a country suffering such severe pressures from population growth and for which flood control and water utilisation (dyking and damming) is a high priority for development, it may be impossible to retain pristine natural ecosystems. In such cases, hatchery-based enhancement may be the only practical way to increase or maintain food fish production.
The following actions can be taken to minimise disease concerns in hatchery-based enhancement projects:
As previously highlighted, the inland fisheries of Bangladesh have recently been severely affected by epizootic ulcerative syndrome, a disease believed to be exotic to the country. There is no evidence to suggest that EUS has been disseminated in Bangladesh by stocking of hatchery-raised fry and fingerlings, or that hatchery enhancement would lead to increased outbreaks of this disease. In Bangladesh, there is ample possibility for disease dissemination by natural means, and, in fact, EUS already occurs widely throughout the country in many fish species.
Until recently, concern around the introduction and transfer of aquatic animal pathogens has centred mainly on their potential impacts on aquaculture. However, as shown by the devastating losses of wild rainbow trout in the western United States due to Myxobolus cerebralis, and of Atlantic salmon in Norway due to Gyrodactylus salaris, the potential for damage to capture and sport fisheries is at least as significant as that posed to culture operations. The following are some major points we believe should be taken into consideration when contemplating stock enhancement programmes in the developing countries of Asia:
Arthur, J.R. 1995. Efforts to prevent the international spread of diseases of aquatic organisms, with emphasis on the Southeast Asian Region. p. 9-25 In: M. Shariff, J.R. Arthur and R.P. Subasinghe. (eds.) Diseases in Asian Aquaculture II. Fish Health Section, Asian Fisheries Society, Manila.
Arthur, J.R. 1996. Fish and shellfish quarantine - the reality for Asia-Pacific. p. 11-28. In: R.P. Subasinghe, J.R. Arthur and M. Shariff. Health Management in Asian Aquaculture. Regional Expert Consultation on Aquaculture Health Management in the Asia and the Pacific. FAO Fish. Tech. Pap. No. 360.
Barnu, G. 1994. The status of epizootic ulcerative syndrome of fish of Bangladesh. p. 13-17. In: R.J. Roberts, B. Campbell and I.H. MacRae. (eds.) ODA Regional Seminar on Epizootic Ulcerative Syndrome at the Aquatic Animal Health Research Institute, Bangkok, Thailand, 25-27 January 1994.
Bauer, O.N., and G.L. Hoffman. 1976. Helminth range extension by translocation of fish. p. 163-172. In: L.A. Page. (ed.) Wildlife Diseases. Plenium Publishing, New York.
Bergersen, E.P., and D.E. Anderson. 1997. The distribution and spread of Myxobolus
cerebralis in the United States. Fisheries, 22(8): 6-7.
Chinabut, S. 1994. EUS in Thailand. p. 58-60. In: R.J. Roberts, B. Campbell
and I.H. MacRae. (eds.) ODA Regional Seminar on Epizootic Ulcerative Syndrome
at the Aquatic Animal Health Research Institute, Bangkok, Thailand, 25-27 January
1994.
Chinabut, S., and R.J. Roberts. 1999. Pathology and histopathology of epizootic ulcerative syndrome (EUS). Aquatic Animal Health Research Institute, Department of Fisheries, Bangkok, 33 p.
Das, M.K. 1994. Outbreak of the fish disease, epizootic ulcerative syndrome in India - an overview. p. 21-38. In: R.J. Roberts, B. Campbell and I.H. MacRae. (eds.) ODA Regional Seminar on Epizootic Ulcerative Syndrome at the Aquatic Animal Health Research Institute, Bangkok, Thailand, 25-27 January 1994.
Dogiel, V.A., and A. Lutta. 1937. Mortality among spiny sturgeon of the Aral Sea in 1936. Rybn. Khoz. 12: 26-27. (Transl. from Russian by Fish. Res. Board Transl. Ser. No. 528, 1965).
FAO/NACA. 2000. Asia Regional Technical Guidelines on Health Management for the Responsible Movement of Live Aquatic Animals and the Beijing Consensus and Implementation Strategy. FAO Fish. Tech. Pap. 402, 53 p.
Heggberget, T.G., B.O. Johnsen, K. Hindar, B. Jonsson, L.P. Hansen, N.A. Hvidsten and A.J. Jensen. 1993. Interactions between wild and cultured Atlantic salmon: a review of the Norwegian experience. Fish. Res. 18: 123-146.
Hillborn, R. 1999. Confessions of a reformed hatchery basher. Fisheries, 25 (5): 30-31.
Hoffman, G.L. 1963. Whirling disease in trouts and its prevention in hatcheries. U.S. Trout News, Sept.-Oct. 1963, p. 8-13, 18.
Hoffman, G.L. 1970. Intercontinental and transcontinental dissemination and transfaunation of fish parasites with emphasis on whirling disease (Myxosoma cerebralis). p. 69-81. In: S.F. Snieszko. (ed.) A Symposium on Diseases of Fishes and Shellfishes. Am. Fish. Soc. Spec. Publ. No. 5.
Humphrey, J.D. 1995. Australian Quarantine and Policies and Practices for Aquatic Animals and their Products: a Review for the Scientific Working Party on Aquatic Animal Quarantine. Part 2: Appendices. Bureau of Resource Sciences, Canberra.
ICES. 1995. ICES Code of practice on the introductions and transfers of marine organisms - 1994. ICES Co-op. Res. Rep. No. 204.
LaPatra, S.E., S.C. Ireland, J.M. Groff, K.M. Clemens and J.T. Siple. 1999. Adaptive disease management strategies for the endangered population of Kootenai River white sturgeon. Fisheries, 24(5): 6-13.
Lilley, J.H., M.J. Phillips and K. Tonguthai. 1992. A Review of epizootic ulcerative syndrome (EUS) in Asia. Aquatic Animal Health Research Institute and Network of Aquaculture Centres in Asia-Pacific, Bangkok, 73 p.
Marcogliese, D.J., and D.K. Cone. 1997. Food webs: a plea for parasites. Trends in Ecology and Evolution, 12: 320-325.
Marcogliese, D.J., and J. Price. 1997. The paradox of parasites. Global Biodiversity, 7(3): 7-15.
Meyer, F.P., J.W. Warren and T.G. Carey. (eds.) 1983. A guide to Integrated Fish Health Management in the Great Lakes Basin. Great Lakes Fish. Comm. Spec. Publ. 83-2, 262 p.
OIE. 2001. International Aquatic Animal Health Code. 4th edn. Office International des Épizooties, Paris.
Porter, T.R. 1992. Protocols for the Introduction and Transfer of Salmonids. North Atlantic Salmon Conservation Organization, North American Commission, NAC 92(24), 119 p.
Roberts, R.J., B. Campbell and I.H. MacRae. (eds.) 1994. ODA Regional Seminar on Epizootic Ulcerative Syndrome at the Aquatic Animal Health Research Institute, Bangkok, Thailand, 25-27 January 1994. 282 p.
Roberts, R.J., R. Wootten, I. MacRae, S. Millar and W. Struthers. 1989. Ulcerative disease survey, Bangladesh. Final report to the Government of Bangladesh and the Overseas Development Administration. Institute of Aquaculture, Stirling University, Scotland. 104 p.
Vincent, E.R., and P. Byorth. 1999. Chronology of the whirling disease epizootic in the Madison River. p. 95-98. In: Proceedings of the Whirling Disease Symposium, 18-20 February, Missoula, Montana, Whirling Disease Foundation, Bozeman, Montana.
Walker, P.G., and R.B. Nehring. 1995. An investigation to determine the cause(s) of the disappearance of young wild rainbow trout in the upper Colorado River, in Middle Park, Colorado. Colorado Division of Wildlife, Denver.
Waples, R.S. 1999. Dispelling some myths about hatcheries. Fisheries, 24(2): 12-21.
Welcomme, R. L. 1988. International introductions of inland aquatic species. FAO Fish. Tech. Pap. No. 294.
Williams, E.H., and C.J. Sindermann. 1992. Effects of disease interactions
with exotic organisms on the health of the marine environment. p. 71-77. In:
M.R. Devoe. (ed.) Introductions & Transfers of Marine Species. Achieving
a Balance Between Economic Development and Resource Protection. Proceedings
of the Conference & Workshop, October 30 - November 2, 1991, Hilton Head
Island, South Carolina. S.C. Seagrant Consortium.
