Myxobolus cerebralis (whirling disease agent)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Diseases Table
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Pathogen Characteristics
- Host Animals
- Latitude/Altitude Ranges
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Pathway Causes
- Pathway Vectors
- Economic Impact
- Environmental Impact
- Threatened Species
- Risk and Impact Factors
- Links to Websites
- Principal Source
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Myxobolus cerebralis Hofer
Preferred Common Name
- whirling disease agent
Other Scientific Names
- Lentospora cerebralis Plehn
- Myxobolus chondrophagus Hofer
- Myxosoma cerebralis Kudo
- Triactinomyxon gyrosalmo Wolf and Markiw
Summary of InvasivenessTop of page
Myxobolus cerebralis, the myxozoan that causes whirling disease in salmon and trout, was first reported in Germany in the late 1890s. The resistance of European brown trout and the fact that whirling disease was not detected outside Europe for over 50 years suggest that it originated in that region. M. cerebralis has primarily been spread by transfers of subclinically infected fish but parasite establishment has been facilitated by the fact that its invertebrate host, Tubifex tubifex, occurs worldwide across a broad range of conditions. Impacts on aquaculture have been significant, but fundamental changes in trout culture and improvements in diagnostics have reduced impacts in hatcheries. Disease in wild populations, with significant impacts on these populations, is reported from the US Rocky Mountain region; the effectiveness of efforts to reduce impacts is difficult to assess. M. cerebralis is not regulated by the World Organisation for Animal Health; however, some countries require imports to be certified free of the parasite and most US states require inspection and certification.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Cnidaria
- Subphylum: Myxozoa
- Class: Myxosporea
- Class: Myxobolus cerebralis
- Order: Bivalvulida
- Suborder: Platysporina
- Family: Myxobolidae
- Genus: Myxobolus
- Species: Myxobolus cerebralis
Notes on Taxonomy and NomenclatureTop of page
Myxozoan taxonomy is based primarily on the morphology and morphometrics of the myxospore stage and species descriptions follow the guidelines of Lom and Arthur (1989), although contemporary descriptions incorporate DNA sequence information (primarily the ssurRNA gene), which helps to distinguish between phenotypically similar species. Before the first life cycle was elucidated in 1984, actinospores and myxospores were assigned independent binomens in separate classes; the class Actinosporea was suppressed in 1994 by Kent et al. (1994). The current taxonomical scheme is outlined in Lom and Dyková (2006).
Myxobolus cerebralis Höfer 1903 is one of more than 2000 species of the phylum Myxozoa Grasse, 1970 (Lom and Dykova, 2006). It is a member of the predominant class Myxosporea Butschli, 1881 and the most speciose genus, Myxobolus Butschli, 1882 (syn. MyxosomaThelohan, 1892). The name is associated with its myxospore stage, known from fishes. The parasite has undergone several name changes over the decades after its discovery, but its binomen has reverted back to the original (Lom and Noble, 1984). Previous names include: Myxobolus chondrophagus Hofer, 1904; Lentospora cerebralis Plehn, 1905; and Myxosoma cerebralis Kudo, 1933. The actinospore stage in its life cycle was originally assigned an independent name, Triactinomyxon gyrosalmo (Wolf and Markiw, 1984), but has since been synonymised (Kent et al., 1994).
The phylum Myxozoa was initially considered part of the Protozoa but its affinities with Metazoa (multicellularity and phylogenetic position) have been recognised for several decades (Siddall et al., 1995), although its exact relationship has altered between the Bilateria and Cnidaria. The most recent study of new genomic sequences firmly places the Myxozoa within the phylum Cnidaria (Nesnidal et al., 2013); however no-one has proposed how to apply this knowledge taxonomically. The subphylum Myxozoa Grassé, 1970 is also currently unranked due to recent changes.
DistributionTop of page
M. cerebralis was first described in Europe and is now exotic on four other continents (Asia, Africa, North America and Oceania). The parasite is not an OIE listed pathogen, and there are few published reports of its current distribution in US States. Information has been compiled by the Whirling Disease Foundation, showing detailed occurrence in hatcheries and watersheds, and most of this data can be found on the Whirling Disease Initiative website (Whirling Disease Initiative, 2014). However, inconsistencies in survey methods and differences in the sensitivity of parasite detection methods have caused confusion about where the parasite occurs. Although there are many reports documenting detection of M. cerebralis, several points should be considered when interpreting this data.
- Detections based on disease signs (whirling behaviour) or characteristic spore morphology are unreliable because disease signs are not exclusive to M. cerebralis and because it is often difficult to distinguish between similar myxobolid spores. Confirmation by histological or molecular methods is essential. Thus some records should be considered unconfirmed or unreliable (eg. Japan, Mexico, South America, Canada).
- Detections of parasite DNA alone, although indicative of parasite presence, should be confirmed with further sampling to determine that parasite establishment has occurred. Establishment in some areas (e.g. Alaska hatcheries, some rivers in Oregon) appears transient.
- Many reports fail to distinguish between parasite introduction and establishment of the life cycle. Thus in many cases detection is based on shipments of infected fish received from Europe, but it is likely that the parasite never became established in the new region and there has been no subsequent work to confirm presence (e.g. South Africa, Lebanon and Morocco).
- Although M. cerebralis may have become established in fish culture facilities, hatchery practices have improved and many of these facilities are no longer positive or have been closed, yet remain on distribution lists.
- Surveys of natural fish populations are rare, so invasiveness and effects on natural populations are often unknown.
- Inclusion of some countries in distribution surveys resulted from misinterpretations of original reports (e.g. Korea, Venezuela) and should be considered invalid or unreliable records.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 17 Dec 2021
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Morocco||Absent, Intercepted only|
|South Africa||Absent, Intercepted only|
|Lebanon||Absent, Intercepted only||Based on FAO report, 1972|
|Austria||Present||1972||Based on FAO report, 1972|
|Belgium||Present||1972||Based on FAO report, 1972|
|Federal Republic of Yugoslavia||Present|
|Finland||Present||1932||Source cites report from 1932 of infections in natural salmon populations|
|Germany||Present, Widespread||Native||First reported in non-native rainbow trout reared in earthen ponds|
|Hungary||Present||Based on FAO report, 1972|
|Ireland||Present||Based on FAO report, 1972|
|Liechtenstein||Present||Based on FAO report, 1972|
|Luxembourg||Present||Based on FAO report, 1972|
|Netherlands||Present||Based on FAO report, 1972|
|Russia||Present||Present based on regional distribution.|
|-Northern Russia||Present||Reports infections in natural salmon populations|
|-Russian Far East||Present||Initial report of widespread enzootic focus of infection in the Sakhalin Islands, in cultured and natural populations. However, no subsequent evidence of infection or disease and status unclear|
|United States||Present||Present based on regional distribution.|
|-Alaska||Absent, Formerly present||2007||2006||M. cerebralis DNA detected at one rearing facility in fish with no clinical disease. Parasite DNA no longer detected in the 3 years after changes in hatchery management; hatchery subsequently closed.|
|-Arizona||Present||Introduced||2000||Initial introduction of parasite in private ponds did not appear to result in establishment. Subsequent detection within the Glen Canyon National Recreation Area in 2007 and 2011|
|-Massachusetts||Absent, Intercepted only||1966||1966|
|-New Jersey||Absent, Formerly present||1967||One hatchery positive in the 1980s is no longer in operation. Parasite does not appear to have become established in the wild|
|-New York||Present, Widespread||Introduced||1984|
|-Ohio||Present, Few occurrences||1970||Introduced||1968||One private facility reported in 1970; no further information|
|-Pennsylvania||Present, Widespread||Introduced||1956||First record in USA confirmed in 1958 following an outbreak at a state hatchery in 1956|
|-West Virginia||Present, Few occurrences||Introduced||No current information; last detected at a small private hatchery in the 1970s; Last reported: 1970s|
|New Zealand||Present||Introduced||Although confirmed in 1971, introduction likely occurred prior to 1952|
History of Introduction and SpreadTop of page
M. cerebralis is believed to be indigenous to Europe and Western Russia and to have been introduced elsewhere through movements of subclinically infected fish. In Europe, whirling disease was first detected in Germany in the late 1890s, when rainbow (Oncorhynchus mykiss) and cutthroat (Salvelinus fontinalis) trout, both non-native species, were imported and reared at hatcheries to supplement the culture of native brown trout (Salmo trutta). During the first half of the twentieth century, the parasite spread within Germany and to two Denmark and Finland, but by the 1970s it was reported throughout Europe and the former Soviet Union. It is unclear whether this perceived rapid spread was as a result of the unrestricted transfers of subclinically infected trout that occurred following WWII or if the parasite was already present in the more resistant native brown trout, which then served as a reservoir of infection for the susceptible introduced species. The presence of fish culture facilities on the same rivers where the parasite is detected in natural populations also makes it difficult to determine whether the parasite was introduced or enzootic.
Outside Europe, dissemination was most likely a result of transport of infected fish. It is unknown precisely when introduction of M. cerebralis to North America occurred, but exchanges of live fish, fish eggs, and frozen fish were common between Europe and the US and the parasite was probably introduced unintentionally through the transfer of infected fish or fish products (Hoffman, 1990). The first confirmations of whirling disease occurred nearly simultaneously in Pennsylvania and Nevada in the late 1950s, but suspected infections were present in New York as early as the 1930s. Subsequent spread in the US was largely by interstate movements of subclinically infected fish and through stocking of natural waters. The recent introduction of the parasite into the US is supported by the low level of intraspecific variation between DNA sequences (small subunit ribosomal DNA (ssu rDNA; <1%) and internal transcribed spacer-1 (ITS1; 1.7%)) of European and North American isolates of M. cerebralis (Whipps et al., 2004; Arsan et al., 2007a). For further discussion see Hoffman (1990), Bartholomew and Reno (2002) and Steinbach et al. (2009).
A second highly visible introduction occurred in New Zealand. Clinical disease signs had been reported as early as 1955, but M. cerebralis was not confirmed until 1971. By the time of its detection there was a complete ban on importations of salmonids except in a heat-treated form.
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|Nevada||Europe||1950s||Aquaculture (pathway cause)||Yes||No||Hoffman (1990)||Importation of fish resulted in parasite introduction|
|New Zealand||Europe||1950s||Aquaculture (pathway cause)||Yes||No||Hewitt and Little (1972)||Importation of fish eggs resulted in parasite introduction, likely in the packing material|
|Pennsylvania||Europe||1950s||Aquaculture (pathway cause)||Yes||No||Hoffman (1990)||Importation of fish resulted in parasite introduction|
Risk of IntroductionTop of page
The movement of M. cerebralis-infected fish is thought to be the primary vector by which the parasite has spread (Hoffman, 1970, 1990; Hedrick et al., 1998; Bartholomew and Reno, 2002). Salmonid eggs cannot serve as vectors for M. cerebralis as the parasite is not transmitted vertically (O’Grodnick, 1975a), and eggs do not become infected if exposed to triactinomyxons (Markiw, 1991). However, contaminated water or packing material containing eggs could transmit the parasite.
Movement of M. cerebralis-infected fish can occur naturally or through human activities. Legal transfers of infected fish occur primarily as a result of fish stocking activities. Improvements in diagnostic methods have reduced this risk; however, difficulty in timely detection of M. cerebralis infection continues to result in accidental introductions of the parasite. Illegal transfers of M. cerebralis-infected fish are now perhaps the highest-risk human activity spreading the parasite. The construction of ponds on private property has become extremely common, and individuals may stock their ponds by purchase of fish through the private aquaculture industry (Steinbach et al., 2009).
Other pathways for spread of M. cerebralis include movement of water, or sediments containing the parasite, by anglers, boaters, and other recreational enthusiasts. Piscivorous wildlife, including fish, birds and mammals, which ingest M. cerebralis-infected fish, can spread the parasite between drainages. Passage of viable myxospores through the digestive system of piscivorous birds has been demonstrated (Taylor and Lott, 1978; El-Matbouli and Hoffmann, 1991). Other potential means of spread include the release of infected T. tubifex from the aquarium trade (Lowers and Bartholomew, 2003; Hallett et al., 2005, 2006), improper disposal of infected fish parts, use of infected fish parts as bait, and effluent from commercial fish processing (Arsan and Bartholomew, 2008), although these have not been demonstrated.
Pathogen CharacteristicsTop of page
M. cerebralis has two microscopic phenotypically distinct spore types - a triactinomyxon-type actinospore and a myxobolus-type myxospore; the spore is the infectious stage for the next host. It is presporogonic development of the myxospore stage of M. cerebralis in fishes that can cause whirling disease. A comprehensive description of development in the fish host is provided by El-Matbouli et al. (1995). Stages prior to sporogony resemble those of other myxozoans. Myxospores are bilaterally symmetrical, broadly oval in frontal view, broadly lenticular in side view with length 8.7 µm, width 8.2 µm and thickness 6.3 µm (Lom and Hoffman, 1971). Two hard valve cells surround a binucleate sporoplasm and two polar capsules, which each contain a coiled (5-6 turns), extrudable polar filament. Actinospores are triradially symmetrical and anchor shaped once waterborne (they are folded within the worm host). The actinospore is composed of three valve cells that form an axis (~150 µm) and three caudal processes (each ~194 µm) (El-Matbouli and Hoffmann, 1998). Within the apical end of the axis there are three polar capsules that each contain a coiled polar filament (5 turns). Below the polar capsules is a sporoplasm that contains 64 germ cells.
Myxospore valve cells contain a protective complex polysaccharide matrix (Lom and Hoffman, 1971); the actinospore stage is relatively fragile. Myxospores become nonviable after: freezing at -20°C for 7 days, holding at 20°C for 2 months, drying, treating with alkyl dimethyl benzyl ammonium chloride at 1500 mg/L for 10 minutes, a dose of ultraviolet (UV) of 40-480 mJ/cm² and chlorine bleach at 500 mg/L for 15 minutes (Hedrick et al., 2008).
Host AnimalsTop of page
|Animal name||Context||Life stage||System|
|Hucho||Domesticated host; Subclinical; Wild host||Aquatic|Fry||Enclosed systems/Ponds; Enclosed systems/Raceways / running water ponds; Open water systems/Enhancements and culture-based fisheries (inc. ranching and stock enhacement); Open water systems/Hard substrate, bottom culture; Open water systems/Soft substrate/sediment, bottom culture|
|Oncorhynchus||Domesticated host; Subclinical; Wild host||Aquatic|Fry||Enclosed systems/Ponds; Enclosed systems/Raceways / running water ponds; Open water systems/Enhancements and culture-based fisheries (inc. ranching and stock enhacement); Open water systems/Hard substrate, bottom culture; Open water systems/Soft substrate/sediment, bottom culture|
|Oncorhynchus mykiss (rainbow trout)|
|Prosopium||Domesticated host; Subclinical; Wild host||Aquatic|Fry||Enclosed systems/Ponds; Enclosed systems/Raceways / running water ponds; Open water systems/Enhancements and culture-based fisheries (inc. ranching and stock enhacement); Open water systems/Hard substrate, bottom culture; Open water systems/Soft substrate/sediment, bottom culture|
|Salmo||Domesticated host; Subclinical; Wild host||Aquatic|Fry|
|Salvelinus||Domesticated host; Subclinical; Wild host||Aquatic|Fry|
|Thymallus||Domesticated host; Subclinical; Wild host||Aquatic|Fry|
ClimateTop of page
|C - Temperate/Mesothermal climate||Preferred||Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C|
|Cf - Warm temperate climate, wet all year||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year|
|Cs - Warm temperate climate with dry summer||Tolerated||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|Cw - Warm temperate climate with dry winter||Tolerated||Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)|
|D - Continental/Microthermal climate||Tolerated||Continental/Microthermal climate (Average temp. of coldest month < 0°C, mean warmest month > 10°C)|
|Df - Continental climate, wet all year||Tolerated||Continental climate, wet all year (Warm average temp. > 10°C, coldest month < 0°C, wet all year)|
|Ds - Continental climate with dry summer||Tolerated||Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)|
|Dw - Continental climate with dry winter||Tolerated||Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)|
Latitude/Altitude RangesTop of page
|Latitude North (°N)||Latitude South (°S)||Altitude Lower (m)||Altitude Upper (m)|
Notes on Natural EnemiesTop of page
No specific natural enemies for M. cerebralis have been identified. However, it is assumed that once the integrity of the spore has been compromised, the organism is vulnerable to degradation by other microbiota. Non-target hosts aid in the reduction of infectious stages. For example, actinospores will attach to non-salmonids (Kallert et al., 2009) and thus be deactivated. Similarly, resistant lineages of T. tubifex will consume and deactivate myxospores, thus preventing infectious stages reaching susceptible lineages (Beauchamp et al., 2006).
Means of Movement and DispersalTop of page
Both spore stages are disseminated naturally in water (Steinbach et al., 2009).
The parasite can be disseminated both locally and over long distances through the movement of infected salmonid fish (Hoffman, 1990). Natural fish migrations may move the parasite locally or stocking of subclinically infected fish may result in long distance and local dissemination of the parasite. Piscivorous birds and wildlife may also disseminate myxospores but the likelihood of this occurrence is highest over short distances (Koel et al., 2010). The release of infected T. tubifex from the aquarium trade (Lowers and Bartholomew, 2003; Hallett et al., 2005, 2006) could also result in release of the parasite.
Myxospores in sediment can be accidentally transported on anglers' waders (Gates et al., 2008). Other means of spread could include the improper disposal of infected fish parts as bait and the discharge of effluent from commercial fish processing (Arsan and Bartholomew, 2008), although these have not been demonstrated.
Pathway CausesTop of page
|Aquaculture||Yes||Yes||Bartholomew and Reno (2002)|
|Fisheries||Yes||Yes||Bartholomew and Reno (2002)|
|Hitchhiker||Potential movement on anglers' gear||Yes||Gates et al. (2008)|
|Interbasin transfers||Stocking of subclincally infected fish||Yes||Yes||Bartholomew and Reno (2002)|
|Interconnected waterways||Natural fish migration||Yes||Bartholomew and Reno (2002)|
|Stocking||Stocking of subclinically infected fish||Yes||Yes||Bartholomew and Reno (2002)|
Pathway VectorsTop of page
|Aquaculture stock||Most frequent means of dissemination. Parasite not easily detected||Yes||Yes||Hoffman (1990)|
|Clothing, footwear and possessions||Myxospores in sediment can be moved on anglers' waders||Yes||Gates et al. (2008)|
|Host and vector organisms||Dissemination mainly through movement of salmonoid fish; possibly by wildlife over shorter distances||Yes||Yes||Koel et al. (2010)|
|Water||Both spore stages are disseminated naturally in water||Yes||Steinbach et al. (2009)|
Economic ImpactTop of page
Historically, the economic impacts of whirling disease have been in relation to the loss of cultured trout. In Europe and the US, both private and publicly owned fish culture operations have sustained large financial losses costs because of M. cerebralis. The parasite has impacted fish culture by causing fish mortalities and reducing fitness, necessitating the destruction of infected fish, requiring disinfection and renovation of facilities, causing the quarantine and closure of facilities and reducing the number of fish available for sale and stocking. In the US, facilities in Utah, California and Colorado were quarantined while millions of dollars were spent to disinfect and renovate them, or they were forced to close when the costs of parasite removal were too great. In 2005, the total value of Utah trout sales dropped almost 30% or approximately $220,000 from the previous year for reasons that included the closure of six privately owned facilities as a result of M. cerebralis detection (House, 2006). In Colorado, the state spent more than $11 million to modernize hatcheries for whirling disease prevention and management between 1987 and 2006 and the federal government completed a multi-million dollar renovation of a National Fish Hatchery to eliminate M. cerebralis (Steinbach et al., 2009). In Europe, although epizootics of whirling disease were widespread in the past century, changes in hatchery practices have greatly minimized losses and the disease is no longer considered a major problem in private fish culture. This transition involved considerable costs but there are no financial reports to support this.
Economic impacts due to the loss of wild fish are often associated with recreational trout fishing. When wild trout population declines were first linked to whirling disease, financial losses due to declines in recreational fishing and tourism were expected. Despite these concerns, no large impact has been documented. In an evaluation of recreational fisheries in Montana and Colorado, no negative effects upon angler satisfaction and local fishing economics could be detected five years after whirling disease caused severe declines in wild trout population (Duffield et al., 1999).
Environmental ImpactTop of page
Impact on Biodiversity
There is evidence of change in the composition of local trout populations in the Madison River, Montana USA, where rainbow trout numbers declined but overall trout populations remained constant because of the increase in brown trout numbers. However, both of these species are introduced in that system. Two native fish in the Rocky Mountain region of the USA, Mountain whitefish (Prosopium williamsoni) and cutthroat trout (Oncorhynchus clarki), may undergo local population declines as a result of infection (Pierce et al. 2011; Koel et al. 2006).
Threatened SpeciesTop of page
Risk and Impact FactorsTop of page
- Proved invasive outside its native range
- Abundant in its native range
- Has propagules that can remain viable for more than one year
- Reproduces asexually
- Changed gene pool/ selective loss of genotypes
- Host damage
- Negatively impacts aquaculture/fisheries
- Reduced native biodiversity
- Threat to/ loss of endangered species
- Threat to/ loss of native species
- Negatively impacts trade/international relations
- Parasitism (incl. parasitoid)
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
- Difficult/costly to control
ReferencesTop of page
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Hansen RW, Bell L, Sloane M, Evans L, 2002. Whirling disease investigations. In: Statewide Fisheries Management Grant F-63-R, Santa Fe, New Mexico, USA: Department of Game and Fish.
Hastein T, 1971. The occurrence of whirling disease (Myxosomiasis) in Norway. In: Acta Veterinaria Scandinavica, 12 297-299.
Hauck AK, Landin S, Wavra S, 1988. Whirling disease in Idaho. In: American Fisheries Society Fish Health Section Newsletter, 16 (2) 5.
Hewitt GC, Little RW, 1972. Whirling disease in New Zealand trout caused by Myxosoma cerebralis (Hofer, 1903) (Protozoa:Myxosporidia). In: New Zealand Journal of Marine and Freshwater Research, 6 1-10.
Hnath JG, 1970. Whirling disease in the state of Michigan. In: Second International Conference of Parasitology, 56 Washington DC, Journal of Parasitology. 149-150.
Hofer B, 1903. About the rotational disease of rainbow trout. (Ueber die Drehkrankheit der Regenbogenforelle). In: Allgemeine Fischerei Zeitung, 28 7-8.
Hoffman GL, Dunbar CE, Bradford A, 1962. Whirling disease of trouts caused by Myxosoma cerebralis in the United States. In: United States Fish and Wildlife Service, Special Scientific Report, 427 Washington DC, USA: US Fish and Wildlife Service. 427.
Holt RA, Amandi A, Banner CR, Kreps TD, 1987. Whirling disease in Oregon. In: American Fisheries Society Fish Health Section Newsletter, 15 (1)
Johansson N, 1966. First identification of Myxosoma cerebralis in Sweden. In: Report LFI, Swedish Salmon Research Institute. 94 pp.
Kocylowski B, 1953. (Choroby ryb i ich Knalkanie). In: Gospodarka ryb, 5 24-26.
Margaritov NM, 1960. Whirling disease of trout in DRS-Samokov. In: Ribno stopanstvo, 2 Sofia, 15-18.
Meyers TU, 1969. Whirling disease. In: FAO Aquaculture Bulletin, 2 13.
Mitchum DL, 1995. Parasites of Fish in Wyoming., Wyoming, USA: Wyoming Game and Fish Department. 304 pp.
Preudhomme JG, 1970. Whirling disease of trout in Morocco. In: FAO Aquaculture Bulletin, 2 14.
Scolari C, 1954. (Sull'impiego dello stovarsolo nelle profilassi del 'capostan' o 'lentosporiasi' delle trote d'allevamento). In: La Clinica Veterinaria, 77 50-53.
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Tidd WM, Tubb RA, 1970. Investigations of whirling disease in Ohio. In: Journal of Parasitology, 56 632.
Tomasec I, 1960. (Lutte contre les principles maladies infectieuses des poisons). In: Bulletin of the Office International des Epizootics, 54 55-57.
Uspenskaya AV, 1955. Biology, distribution and economic importance of Myxosoma cerebralis, the causative agent of whirling disease of trout. In: Lectures of the Academy of Science USSR, 105 1132-1135.
Uspenskaya AV, 1957. The ecology and spreading of the pathogen of trout whirling disease-Myxosoma cerebralis (Höfer 1903, Plehn 1905) in the fish ponds of the Soviet Union. In: All-Union Research Institute of Lake and River Fishery, 42 47-55.
Vanco F, 1952. (Contribution á l'étude de la pathologie des alevins de truits)., Paris, France: Foulon.
Vincent ER, 1996. Whirling disease and wild trout: The Montana experience. In: Fisheries, 21 32-33.
Walker PG, Nehring RB, 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, USA: Colorado Division of Wildlife. 134 pp.
Wilson JC, 1991. Whirling disease comes to Utah. In: The Ichthyogram, Newsletter of the Fisheries Experiment Station, Utah Division of Wildlife Resources, 2 Utah, USA: Utah Division of Wildlife Resources. 1-2.
Wyk GF van, 1968. Annual report No. 24, 1967. In: Jokershoek Hatchery, Division of Inland Fisheries, Province of Good Hope, Republic of South Africa: Department of Nature Conservation. 24.
Yasutake WT, Wolf H, 1970. Occurrence of whirling disease of trout in the western United States. Second International Congress of Parasitology. September 6-12. Washington, DC. In: Journal of Parasitology, 56 375-376.
Yoder WG, 1972. The spread of Myxosoma cerebralis into natural trout populations in Michigan. In: Progressive Fish-Culturist, 43 103-106.
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18/10/2013 Original text by:
Jerri Bartholomew, Dept. of Microbiology, Nash Hall 220, Oregon State University, Corvallis, Oregon 97331, USA
Sascha Hallet, Dept. of Microbiology, Nash Hall 220, Oregon State University, Corvallis, Oregon 97331, USA
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