Bothriocephalus acheilognathi
Index
- Pictures
- Identity
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Diseases Table
- Distribution
- Distribution Table
- History of Introduction and Spread
- Introductions
- Risk of Introduction
- Pathogen Characteristics
- Habitat List
- Host Animals
- Climate
- Latitude/Altitude Ranges
- Rainfall Regime
- Means of Movement and Dispersal
- Pathway Causes
- Pathway Vectors
- Vectors and Intermediate Hosts
- Economic Impact
- Environmental Impact
- Threatened Species
- Risk and Impact Factors
- Gaps in Knowledge/Research Needs
- References
- Principal Source
- Contributors
- Distribution Maps
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Top of pagePreferred Scientific Name
- Bothriocephalus acheilognathi Yamaguti, 1934
Other Scientific Names
- Bothriocephalus gowkongensis Yeh, 1955
- Bothriocephalus opsariichthydis Yamaguti, 1934
- Schyzocotyle acheilognathi (Yamaguti, 1934)
International Common Names
- English: Asian fish tapeworm; Asian tapeworm
Summary of Invasiveness
Top of pageThe Asian tapeworm or Asian fish tapeworm, Bothriocephalus acheilognathi, is native to East Asia and in the past few decades has been spread widely throughout the world via human activities to all continents except Antarctica. Examples of these activities include the movement of (mostly cyprinid) fish for aquaculture, the pet fish trade, aquatic weed control and mosquito control, and more recently in movement of bait fish. In addition, birds which eat infected fish may transport the cestode’s eggs and spread them through defecation. B. acheilognathi has been reported in over 300 species of freshwater fish (Kuchta et al., 2018), and this wide host range has assisted its establishment, but it is primarily reported from cultured and wild carp. It is a problem for aquaculture and is suspected of adversely affecting endangered wild species. It is listed as a Pathogen of Regional Importance (PRI) by the United States Fish and Wildlife Service (US Fish and Wildlife Service, 2015).
Taxonomic Tree
Top of page- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Platyhelminthes
- Class: Cestoda
- Subclass: Eucestoda
- Order: Pseudophyllidea
- Family: Bothriocephalidae
- Genus: Bothriocephalus
- Species: Bothriocephalus acheilognathi
Notes on Taxonomy and Nomenclature
Top of pageBothriocephalus acheilognathi Yamaguti, 1934 (Cestoda: Bothriocephalidae), commonly called the Asian tapeworm or Asian fish tapeworm, was described from the cyprinid Acheilognathus rhombeus collected from Lake Ogura on the Yoda River which flows south from Lake Biwa in Japan. Since its description, the worm has been identified under 20 different specific epithets (Kuchta and Scholz, 2007). The erroneous splitting into new species was often a result of variability in size and shape of the worms due to variability in fixation procedures (Brandt et al., 1981; Pool and Chubb, 1985), species of host (Molnár and Murai, 1973; Granath and Esch, 1983c), age of host and worm burden (Davydov, 1978) and environmental conditions where the host lived (Nedeva and Mutafova, 1988). Of the 20 names, the two most commonly reported apart from B. acheilognathi are B. gowkongensis Yeh, 1955 and B. opsariichthydis Yamaguti, 1934. After examining the described introduced species of Bothriocephalus, Pool and Chubb (1985), Pool (1987) and Kuchta et al. (2012) declared that all species descriptions of Bothriocephalus in cyprinids referred to the same parasite. Bean et al. (2007) provided molecular data to corroborate the synonomy. However, there is some indication that the Asian fish tapeworm may be a species complex (Liao, 2007; Luo et al., 2003; Choudhury and Cole, 2012), and further taxonomic study is needed.
Distribution
Top of pageB. acheilognathi is native to eastern Asia but has been spread widely throughout the world (including all continents except Antarctica) by human activities (Bauer and Hoffman, 1976). It seems to be widely distributed in China (Nie et al., 2000) but its status in Japan appears uncertain (Choudhury and Cole, 2012). The records of Bothriocephalus spp. from native cyprinids in Africa and India are considered to be B. acheilognathi (Pool, 1987; Kuchta and Scholz, 1997; Kuchta et al., 2012) but this needs to be confirmed by molecular analyses that include tapeworms from native barbs in the interior of Africa and from native cyprinids in streams of the Himalayan foothills (Malhotra, 1984). This is particularly important since there is some indication that the Asian fish tapeworm may be a species complex (Liao, 2007; Luo et al., 2003; Choudhury and Cole, 2012). Reports from clariid catfishes in Africa need to be verified because Kuchta et al. (2012) stated that the species could be confused with another similar tapeworm, Tetracampos ciliotheca. Molecular data indicate that isolates from continental North America, Hawaii, and Central America closely match B. acheilognathi isolates from Eurasia (Bean et al., 2007; Choudhury et al., 2013; Salgado-Maldonado et al. 2015; A. Choudhury, St Norbert College, De Pere, Wisconsin, USA, unpublished data).
In the U.S., the parasite seems to be particularly established in the western and southwestern parts of the country (Heckmann, 2000; Kuperman et al., 2002; Warburton et al., 2002; Choudhury et al., 2006; Archdeacon et al., 2009; Kline et al., 2009). In Mexico, it appears to be widely distributed (Salgado-Maldonado and Pineda-López, 2003; Rojas-Sánchez and García-Prieto, 2008). In Australia, it is established in the eastern part of the continent (Dove and Fletcher, 2000). In Europe, it is absent from northern European (Scandinavian) countries; the current status in many central and eastern European countries seems unclear. In South Africa, it is common in carp in certain areas and remains well established.
Distribution Table
Top of pageThe 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: 02 Feb 2021Continent/Country/Region | Distribution | Last Reported | Origin | First Reported | Invasive | Reference | Notes |
---|---|---|---|---|---|---|---|
Africa |
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Algeria | Present, Localized | Introduced | Lake Oubeira | ||||
Congo, Democratic Republic of the | Absent, Unconfirmed presence record(s) | Lake Kivu; record is of B. kivuensis, synonymized with B. acheilognathi, but synonymy is questionable (see Choudhury and Cole, 2012) | |||||
Egypt | Absent, Unconfirmed presence record(s) | Record is of B. aegyptiacus, synonymized with B. acheilognathi, but synonymy should be validated. | |||||
Ethiopia | Present | ||||||
Mauritius | Present | Introduced | Paperna reported a personal communication from J.G. Van As, University of the Free State, Bloemfontein, South Africa. | ||||
Nigeria | Present | Introduced | Niger and Benue River confluence, Lokoja | ||||
Rwanda | Absent, Unconfirmed presence record(s) | Lake Kivu, as B. kivuensis, synonymized with B. acheilognathi, but synonymy requires validation (see Choudhury and Cole, 2012) | |||||
South Africa | Present | Introduced | Invasive | ||||
Asia |
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Afghanistan | Present | Introduced | |||||
Azerbaijan | Present | Introduced | |||||
China | Present | Present based on regional distribution. | |||||
-Chongqing | Present | Native | |||||
-Fujian | Present | Native | In grass carp, but not in common carp | ||||
-Gansu | Present | Native | In grass carp, but not in common carp | ||||
-Guangdong | Present | Native | Originally described by Yeh, 1955, as B. gowkongensis | ||||
-Guizhou | Present | Native | In common carp and grass carp | ||||
-Heilongjiang | Present | Native | In common carp, but not in grass carp | ||||
-Hubei | Present | Native | Lakes in the flood plains of the Yangtze River, in cultrinin cyprinids | ||||
-Inner Mongolia | Present | Native | Dong Lake | ||||
-Jiangxi | Present | Native | |||||
-Jilin | Present | Native | |||||
-Liaoning | Present | Native | |||||
-Ningxia | Present | Native | In common carp, but not in grass carp | ||||
-Shanxi | Present | Native | |||||
-Sichuan | Present | Native | |||||
-Xinjiang | Present | Introduced | In common carp, but not in grass carp | ||||
-Yunnan | Present | Introduced | |||||
Georgia | Present | Introduced | In closed reservoirs | ||||
India | |||||||
-Jammu and Kashmir | Absent, Unconfirmed presence record(s) | Reported from hill streams in a native cyprinid. Species identification should be validated | |||||
-Meghalaya | Present | 2016 | Found in aquacultured grass carp (Ctenopharyngodon idella) | ||||
-Uttar Pradesh | Present | Introduced | Reported in 1984 as B. teleostei -- that identification needs to be validated. In 2015 reported again, and identified by molecular methods, from introduced Xiphophorus hellerii. | ||||
Iran | Present | Introduced | Invasive | ||||
Iraq | Present | Introduced | Invasive | ||||
Israel | Present | Introduced | |||||
Japan | Present | See Choudhury & Cole (2012) for a discussion of its status as a native or introduced species | |||||
Kazakhstan | Present | Introduced | Invasive | ||||
Kyrgyzstan | Present | Introduced | |||||
Malaysia | Present | Introduced | |||||
Mongolia | Absent, Unconfirmed presence record(s) | Dubinina does not specifically mention Mongolia, only the Amur River drainage | |||||
Philippines | Present | Introduced | |||||
South Korea | Present | Introduced | Kim et al. (1986) cited in Paperna (1996) | ||||
Sri Lanka | Present | Introduced | |||||
Tajikistan | Present | Introduced | |||||
Turkey | Present | Introduced | |||||
Turkmenistan | Present | Introduced | |||||
Uzbekistan | Present | Introduced | |||||
Europe |
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Albania | Present | Lake Ohrid | |||||
Austria | Present | Introduced | Carp ponds | ||||
Belarus | Present | ||||||
Bosnia and Herzegovina | Present | Introduced | Carp ponds | ||||
Bulgaria | Present | Introduced | |||||
Croatia | Present | Introduced | Kezic et al. (1975) cited in Hoffman (1999) | ||||
Czechoslovakia | Present | ||||||
France | Present | Introduced | |||||
Germany | Present | Introduced | Invasive | ||||
Hungary | Present | Described as B. phoxini, in Phoxinus phoxinus | |||||
Italy | Present | Introduced | Invasive | ||||
Latvia | Present | Introduced | Carp ponds. Vismanis and Jurkane (1967) cited in Kirjušina and Vismanis (2007) | ||||
North Macedonia | Present | Introduced | Lake Ohrid | ||||
Poland | Present | Introduced | |||||
Romania | Present | Introduced | |||||
Russia | Present | Present based on regional distribution. | |||||
-Central Russia | Present | Introduced | Invasive | Mainly in aquaculture facilities | |||
-Eastern Siberia | Present | Native | Amur River drainage | ||||
-Russian Far East | Present | Native | Amur River drainage | ||||
-Southern Russia | Present | Introduced | Invasive | Mainly in aquaculture facilities | |||
-Western Siberia | Present | Introduced | Invasive | Mainly in aquaculture facilities | |||
Ukraine | Present | Introduced | |||||
United Kingdom | Present | Introduced | |||||
North America |
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Canada | Present | Present based on regional distribution. | |||||
-British Columbia | Absent, Invalid presence record(s) | Specimens reported by Arai and Mudry (1983) were misidentified | |||||
-Manitoba | Present | Introduced | Lake Winnipeg below Lockport Dam, not likely upstream of Pine Falls on Winnipeg River or Grand Rapids on Saskatchewan River (Patrick Nelson, North South Consultants Inc., Winnipeg, Manitoba, Canada, personal communication) | ||||
-Ontario | Present, Localized | Introduced | Detroit River, hence likely present in Lakes Huron, St. Clair and Erie. Muzzall et al. (2016) confirm its presence on the Michigan side of Lakes Huron and St. Clair. | ||||
Honduras | Present | Introduced | |||||
Mexico | Present, Widespread | Introduced | Invasive | Widespread | |||
Panama | Present | Introduced | |||||
Puerto Rico | Present | Introduced | |||||
United States | Present | Present based on regional distribution. | |||||
-Arizona | Present, Widespread | Introduced | Invasive | ||||
-Arkansas | Present | Introduced | In a hatchery | ||||
-California | Present | Introduced | 1980 | Southern California | |||
-Colorado | Present | Introduced | |||||
-Florida | Present | Introduced | |||||
-Hawaii | Present | Introduced | |||||
-Indiana | Present | Introduced | |||||
-Kansas | Present | Introduced | |||||
-Kentucky | Present | Introduced | |||||
-Louisiana | Present | Introduced | In mosquitofish, Gambusia; Original citation: W. Font, Southeastern Louisiana University, Hammond, Louisiana, USA, personal communication, 2015 | ||||
-Michigan | Present | Introduced | In wild in Detroit River, Lake Huron and Lake St. Clair; likely present in Lake Erie. Widespread in mostly wild-caught baitfish in retail stores. | ||||
-Nebraska | Present | Introduced | |||||
-Nevada | Present | Introduced | 1987 | Muddy River, Virgin River, bait shops | |||
-New Hampshire | Absent, Unconfirmed presence record(s) | ||||||
-New Mexico | Absent, Unconfirmed presence record(s) | Pecos River | |||||
-New York | Present | Introduced | |||||
-North Carolina | Present | Introduced | Invasive | In a reservoir | |||
-Texas | Present | Introduced | Invasive | Rio Grande/Río Bravo del Norte, Pecos River | |||
-Utah | Present | Introduced | Virgin River | ||||
-Wisconsin | Present | Introduced | Land-o-Lakes lakes | ||||
Oceania |
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Australia | Present | Introduced | Invasive | ||||
-New South Wales | Present | Introduced | |||||
-Victoria | Present | Introduced | |||||
New Zealand | Absent, Intercepted only | Arrived with grass carp imports from Hong Kong but intercepted during quarantine. | |||||
South America |
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Argentina | Present, Localized | Introduced | |||||
Brazil | Present, Localized | Introduced |
History of Introduction and Spread
Top of pageBauer and Hoffman (1976), Chubb (1981), Paperna (1996) and Hoffman (1999) reviewed the spread of B. acheilognathi.
The year that the parasite was first reported from a country is an unreliable indication of when it was introduced. In countries such as Russia, the U.S.A., Mexico, and several European countries, there have been multiple shipments of carp and other potentially infected species. For example, grass carp, Ctenopharyngodon idella, were first introduced into the Czech Republic in 1961 (Lusk et al., 2010) but the parasite was not reported from there until the early 1970s. Similarly, infections in English fish farms were first documented in the early 1980s (Andrews et al., 1981) but were tentatively traced to imports of European common carp, Cyprinus carpio, a decade earlier. These cases could mean that the parasite was present but not detected until later or that it was introduced with a subsequent shipment/introduction, or even by another host. Occasionally, the interval between the parasite’s actual introduction and its detection can be decades long, such as in Australia and Panama (Koehn, 2004, Dove et al., 1997; Dove and Fletcher, 2000; Choudhury et al., 2013). This is also true for Mexico, where new records continue to accumulate as previously unexplored areas are surveyed (Rojas-Sánchez and García-Prieto, 2008; Pérez-Ponce de Leon et al., 2009; Méndez et al., 2010; Aguilar-Aguilar et al., 2010). The records from Mexico indicate that the parasite may have been introduced by more than one species of host (Salgado-Maldonado and Pineda-López, 2003).
The parasite was first described by Yamaguti (1934) from cyprinids in Japan. It was subsequently reported from southern China (Yeh, 1955) as B. gowkongensis, which was later synonymized with B. acheilognathi. It was known to be native to the Amur River grass carp in the 1950s (Bykhovskaya-Pavlovskaya et al., 1962). Beginning in the 1950s, it was detected in western parts of the former Soviet Union, largely because infected carp were moved to and between fish farms. Consequently it became common and widespread in cultured grass carp and common carp (Bauer and Hoffman, 1976). By the late 1950s and early 1960s, it was known from Ukraine and the Moscow area (Bykhovskaya-Pavlovskaya et al. 1962) as well as from Romania (Radulescu and Georgescu, 1962). In the early 1970s, it spread across eastern and western Europe (Scholz et al., 2012). A steady stream of reports indicated its worldwide presence, for example in Sri Lanka (Fernando and Furtado, 1963), Malaysia (Fernando and Furtado, 1964), Uzbekistan (Osmanov, 1971), Hungary (Molnar and Murai, 1973), Croatia (Kezic et al., 1975, cited in Hoffman, 1999), Germany (Korting, 1974), continental U.S.A. (Hoffman, 1976, 1980; Granath and Esch, 1983a,c), the former Czechoslovakia (Faina and Par, 1977), Afghanistan (Moravec and Amin, 1978), England (Andrews et al., 1981), South Africa (Boomker et al, 1980; Brandt et al., 1981; Van As et al., 1981; Van As and Basson, 1984), Mexico (López-Jiménez, 1981), Philippines (Velasquez, 1982; Arthur and Lumanlan-Mayo, 1997), Hawaii (Hoffman, 1999), France (Denis et al., 1983), Italy (Minervini et al., 1985; Scholz and Cave, 1992), Iraq (Khalifa,1986), Korea (Kim et al., 1986, cited in Paperna, 1996), Puerto Rico (Bunkley-Williams and Williams, 1994), Brazil (Rego et al., 1999), Australia (Dove et al., 1997; Dove and Fletcher, 2000), Turkey (Aydogdu et al., 2003), Canada (Choudhury et al., 2006), Panama (Choudhury et al., 2013), and most recently Honduras (Salgado-Maldonado et al., 2015).
Introductions
Top of pageIntroduced to | Introduced from | Year | Reason | Introduced by | Established in wild through | References | Notes | |
---|---|---|---|---|---|---|---|---|
Natural reproduction | Continuous restocking | |||||||
Australia | Europe | 1960s | Hitchhiker (pathway cause) | Yes | No | Harris (2013) | Boolarra strain of common carp may be main cause of spread -- deliberate introduction of carp | |
Panama | USA | 1960s | Hitchhiker (pathway cause) | Yes | No | Choudhury et al. (2013) | Probably imported with grass carp imported for control of aquatic vegetation. Documented | |
Romania | Russian Federation | 1950s | Hitchhiker (pathway cause) | No | No | Radulescu and Georgescu (1962) | Probably transported with fish imported for aquaculture | |
UK | Europe | 1972-1973 | Hitchhiker (pathway cause) | No | No | Andrews et al. (1981) | With fish imported for aquaculture. Europe stated as a “likely” source for one hatchery | |
Ukraine | Russian Federation | 1950s | Hitchhiker (pathway cause) | No | No | Bykhovskaya-Pavlovskaya et al. (1962) | With fish imported for aquaculture. Documented | |
USA | Malaysia | 1960s | Hitchhiker (pathway cause) | Yes | No | Choudhury and Cole (2012); Hoffman and Schubert (1984) | With fish imported for aquaculture; original shipments documented |
Risk of Introduction
Top of pageB. acheilognathi is mainly spread by the introduction of infected fish hosts. Because it is able to colonize a wide range of fish and copepod hosts, over a broad latitudinal range, accidental introduction of infected fish (which can occur for a variety of reasons – see Movement and Dispersal section) poses a high risk in any freshwater ecosystem. Movement of water containing tapeworm eggs or infected copepods, especially from water bodies where parasite and copepod densities may be high, also contributes to the risk. As well as its apparently low host specificity, its simple two-host life cycle using copepods (Hanzelová and Žitnan, 1986; Marcogliese and Esch, 1989b) as the intermediate host with fish as the definitive host have underpinned its great success in invading every continent except Antarctica (Bauer and Hoffman, 1976; Dove and Fletcher, 2000). Post-cyclic transmission where small fish infected with larval B acheilognathi can serve as a source of infection to larger fish can also facilitate wide spread of the parasite (Hansen et al, 2007).
Pathogen Characteristics
Top of pageMature specimens of Bothriocephalus acheilognathi have a segmented body with an arrowhead-shaped or heart-shaped scolex with bothria (slits) situated dorsoventrally along the scolex terminating with a weak apical disc (Yeh, 1955). The worm’s length is variable depending on the host, the ecological setting and age of the host, the age of infection and the number of worms; 3.5-8 cm is typical, although specimens up to 1 m in length have been reported. In addition, the shape of the scolex and bothria are affected by fixation and how they are mounted on glass slides. The medial position of the genital opening on the segments is of taxonomic importance. Morphological identification should be corroborated with molecular analyses (Bean et al., 2007). Three species that are easily misidentified as B. acheilognathi are Eubothriumtulipai, E. rectangulum and Bathybothrium rectangulum as they also have a similar scolex with bothria; however, they have lateral rather than medial genital openings (Dubinina, 1987).
Host Animals
Top of pageAnimal name | Context | Life stage | System |
---|---|---|---|
Aristichthys nobilis (bighead carp) | Aquatic|Adult | Enclosed systems/Ponds | |
Carassius auratus auratus (goldfish) | |||
Ctenopharyngodon idella (grass carp) | Domesticated host; Wild host | Aquatic|Adult; Aquatic|Fry | Enclosed systems/Ponds; Enclosed systems/Tanks |
Cyprinus carpio (common carp) | Domesticated host; Wild host | Aquatic|Adult; Aquatic|Fry | Enclosed systems/Ponds; Enclosed systems/Tanks |
Gambusia affinis (western mosquitofish) | Wild host | Aquatic|Adult | |
Gila bicolor mohavensis (Mohave tui chub) | |||
Gila cypha | Wild host | Aquatic|Adult | |
Gila elegans | Experimental settings | Aquatic|Adult | Enclosed systems/Freshwater recirculating systems |
Gila robusta (roundtail chub) | |||
Hypophthalmichthys molitrix (silver carp) | Aquatic|Fry | Enclosed systems/Ponds | |
Notropis topeka | |||
Plagopterus argentissimus (woundfin) | Wild host | Aquatic|Adult | |
Profundulus hildebrandi |
Climate
Top of pageClimate | Status | Description | Remark |
---|---|---|---|
A - Tropical/Megathermal climate | Tolerated | Average temp. of coolest month > 18°C, > 1500mm precipitation annually | |
Af - Tropical rainforest climate | Tolerated | > 60mm precipitation per month | |
Am - Tropical monsoon climate | Tolerated | Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25])) | |
As - Tropical savanna climate with dry summer | Tolerated | < 60mm precipitation driest month (in summer) and < (100 - [total annual precipitation{mm}/25]) | |
Aw - Tropical wet and dry savanna climate | Tolerated | < 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25]) | |
B - Dry (arid and semi-arid) | Tolerated | < 860mm precipitation annually | |
BS - Steppe climate | Tolerated | > 430mm and < 860mm annual precipitation | |
BW - Desert climate | Tolerated | < 430mm annual precipitation | |
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 | Preferred | Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers | |
Cw - Warm temperate climate with dry winter | Preferred | 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 Ranges
Top of pageLatitude North (°N) | Latitude South (°S) | Altitude Lower (m) | Altitude Upper (m) |
---|---|---|---|
50 | 30 |
Means of Movement and Dispersal
Top of pageB. acheilognathi is mainly spread by the introduction of infected fish hosts such as the common carp (Cyprinus carpio) and grass carp (Ctenopharyngodon idella), often for aquaculture (Bauer et al., 1969; Minervini et al., 1985; Fuller et al., 1999; Bauer and Hoffman, 1976). One of the major hosts, C. idella, has been widely used for controlling aquatic weeds and this has resulted in the tapeworm invading places such as North America and Panama (Hoffman, 1999; Choudhury et al., 2013; López-Jiménez, 1981; Maitland and Campbell, 1992; Fuller et al., 1999). Another suitable host, the mosquitofish Gambusia, is commonly used to control mosquitoes and stocking of this fish probably introduced the tapeworm to California (Hoffman, 1999; Warburton et al., 2002; Choudhury et al., 2006; Heckmann, 2009). The movement of infected baitfish resulted in the parasite’s successful colonization of the U.S. Southwest (Heckmann et al., 1993; Choudhury et al., 2004). The aquarium fish trade is also a potential contributing factor (Scholz et al., 2012; Edwards and Hine, 1974; Evans and Lester, 2001). There have been cases of infected fish escaping from confinement due to flooding (Choudhury and Cole, 2012), or being introduced for ecosystems research (Choudhury et al., 2006). Movement of water (and probably vegetation) contaminated with tapeworm eggs or infected copepods can also spread the parasite (R. Cole, US Geological Survey, National Wildlife Health Center, Madison, Wisconsin, USA, personal communication, 2015). Piscivorous birds have also been reported to act as phoretic agents, transporting viable cestode eggs from infected prey and spreading them via defecation (Prigli, 1975).
Pathway Causes
Top of pageCause | Notes | Long Distance | Local | References |
---|---|---|---|---|
Hitchhiker | Moved worldwide in host fish, especially carp for aquaculture | Yes | Yes | Bauer and Hoffman (1976); Choudhury and Cole (2012); Scholz et al. (2012) |
Pathway Vectors
Top of pageVector | Notes | Long Distance | Local | References |
---|---|---|---|---|
Aquaculture stock | Rearing of grass carp and common carp brood stock, fingerlings etc. | Yes | Bauer and Hoffman (1976) | |
Bait | Bait fish transfers spread the parasite into the U.S. southwest | Yes | Yes | Heckmann et al. (1993); Scholz et al. (2012); Boonthai et al. (2017) |
Host and vector organisms | Fish act as final hosts, copepod crustaceans as intermediate hosts; piscivorous birds can carry eggs | Yes | Yes | Bauer and Hoffman (1976); Choudhury and Cole (2012); Prigli (1975); Scholz et al. (2012) |
Pets and aquarium species | Aquarium fishes such as koi and goldfish | Yes | Yes | Scholz et al. (2012) |
Plants or parts of plants | Infected copepods may attach to aquatic vegetation. | Yes | Yes | |
Water | Water may contain propagative stages such as eggs, and copepods infected with parasite larvae | Yes | Yes |
Vectors and Intermediate Hosts
Top of pageVector | Source | Reference | Group | Distribution |
---|---|---|---|---|
Acanthocyclops bicuspidatus | Dubinina (1987) | Crustacean | Former USSR | |
Acanthocyclops robustus | Hansen et al. (2006) | Crustacean | ||
Acanthocyclops vernalis | Dubinina (1987) | Crustacean | Former USSR | |
Acanthocyclops viridis | Dubinina (1987) | Crustacean | Former USSR | |
Cyclops strenuus | Dubinina (1987) | Crustacean | Former USSR | |
Cyclops vicinus | Dubinina (1987) | Crustacean | Former USSR | |
Diacyclops thomasi | Marcogliese and Esch (1989b) | Crustacean | North America | |
Eucyclops agilis | Marcogliese and Esch (1989b) | Crustacean | North America | |
Eucyclops serrulatus | Dubinina (1987) | Crustacean | Former USSR | |
Macrocyclops | Scholz et al. (2012) | Crustacean | Old world | |
Megacyclops | Scholz et al. (2012) | Crustacean | Old world | |
Mesocyclops edax | Marcogliese and Esch (1989b) | Crustacean | North America | |
Paracyclops poppei | Marcogliese and Esch (1989b) | Crustacean | North America | |
Thermocyclops | Scholz et al. (2012) | Crustacean | Old world | |
Thermocyclops oithonoides | Dubinina (1987) | Crustacean | Former USSR | |
Tropocyclops prasinus | Marcogliese and Esch (1989b) | Crustacean | North America |
Economic Impact
Top of pageB. acheilognathi was first reported in Asia and Eastern Europe as an important disease agent (Bauer et al., 1969; Heckmann, 2009). Moderate to heavy B. acheilognathi infections can be fatal to fish fingerlings. This has been documented in cultured grass carp (Ctenopharyngodon idella), common carp (Cyprinus carpio) and koi (Yeh, 1955; Bauer et al. 1969; Han et al., 2010); Liao and Shih (1956) reported severe losses in grass carp of the young-of-the-year age class in China, with a mortality rate of 90% in winter months (Liao and Shih, 1956). Costs to aquaculture, beyond loss of fish, are due to disruption of normal hatchery and fish farming operations, increased cost of operation as a result of treating fish (with medication administered in diet), and draining and disinfecting tanks and ponds. Aquaculture operations have to invest in additional quarantine and inspection infrastructure and personnel.
Environmental Impact
Top of pageImpact on Biodiversity
The impact of B. acheilognathi on biodiversity is still largely unknown, and assessing the population-level impact is difficult, but it is suspected of impacting populations of two IUCN-listed endangered North American fish species, the woundfin (Plagopterus argentissimus) and the humpback chub (Gila cypha), and potentially threatens others such as the U.S. federally listed endangered Tui Mohave chub Siphateles bicolor mohavensis (Heckmann, 2000, 2009; Hoffnagle et al., 2006; Choudhury and Cole, 2012; Archdeacon et al., 2008; Stone et al., 2007). Also in the USA, it hinders growth of the Near Threatened roundtail chub Gila robusta (Brouder, 1999) and the US-listed Topeka shiner Notropis topeka (Koehle and Adelman, 2007); experimental infections in the Critically Endangered bonytail chub (Gila elegans) resulted in reduced growth, decline in health condition indices, and accelerated mortality when food was reduced (Hansen et al., 2006). Velázquez-Velázquez et al. (2011) found a high prevalence of infection in the Endangered Chiapas killifish (Profundulus hildebrandi) in Mexico.
Threatened Species
Top of pageThreatened Species | Conservation Status | Where Threatened | Mechanism | References | Notes |
---|---|---|---|---|---|
Gila bicolor mohavensis (Mohave tui chub) | USA ESA listing as endangered species | USA | Parasitism (incl. parasitoid) | Archdeacon et al. (2008) | |
Gila cypha | EN (IUCN red list: Endangered) | USA | Parasitism (incl. parasitoid) | Choudhury and Cole (2012); Hoffnagle et al. (2006); Stone et al. (2007) | |
Gila elegans | CR (IUCN red list: Critically endangered) | USA | Parasitism (incl. parasitoid) | Hansen et al. (2006) | |
Gila robusta (roundtail chub) | NT (IUCN red list: Near threatened) | USA; Arizona; California; Nevada | Parasitism (incl. parasitoid) | Brouder (1999); US Fish and Wildlife Service (2013) | |
Notropis topeka | USA ESA listing as endangered species | USA | Parasitism (incl. parasitoid) | Koehle and Adelman (2007) | |
Plagopterus argentissimus (woundfin) | EN (IUCN red list: Endangered); USA ESA listing as endangered species | USA | Parasitism (incl. parasitoid) | Heckmann (2000); Heckmann (2009) | |
Profundulus hildebrandi | EN (IUCN red list: Endangered) | Mexico | Parasitism (incl. parasitoid) | Velázquez-Velázquez et al. (2011) |
Risk and Impact Factors
Top of page- Proved invasive outside its native range
- Has a broad native range
- Abundant in its native range
- Highly adaptable to different environments
- Is a habitat generalist
- Fast growing
- Has high reproductive potential
- Host damage
- Negatively impacts animal health
- Negatively impacts livelihoods
- Negatively impacts aquaculture/fisheries
- Threat to/ loss of endangered species
- Threat to/ loss of native species
- Parasitism (incl. parasitoid)
- Highly likely to be transported internationally accidentally
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
Gaps in Knowledge/Research Needs
Top of pageRecent work on B. acheilognathi in Africa (Kuchta et al., 2012) and in China (Luo et al., 2002, 2003) shows that our understanding of the distribution, biogeography and systematics of this worm is still fragmentary. We still do not understand its host associations and why some hosts are susceptible and others not. We also need to develop a clearer understanding of how it affects natural populations, as well as early warning systems related to its invasiveness. Parasitologists will need to work closely with fisheries biologists and local and national agencies to develop comprehensive strategies to monitor natural fish populations.
References
Top of pageÖztürk, T., Özer, A., 2014. Comparative invasive Asian tapeworm Bothriocephalus acheilognathi on the lower Kizilirmak delta fishes, 1(1), 1-7. http://dergipark.ulakbim.gov.tr/jadfa/article/view/5000105735
Aguilar-Aguilar R, Jose-Abrego A, Pérez-Ponce León G de, 2010. Cestoda, Bothriocephalidae, Bothriocephalus acheilognathi Yamaguti, 1934: Nematoda, Rhabdochonidae, Rhabdochona canadensis Moravec and Arai, 1971: New host records for the state of Puebla, Mexico, and a new fish host. Checklist, 6(3):437-438.
Akhmerov AK, 1960. Fish cestodes of the Amur River. Trudy Gel'mintologicheskoi Laboratorii Akademiya Nauk SSSR, 10:15 - 21.
Akhter S, Fayaz A, Chishti MZ, Tariq KA, 2008. Seasonal dynamics of Bothiocephalus [Bothriocephalus] acheilognathi in Schizothorax spp. and cyprinid spp. from the Kashmir Valley. Indian Journal of Applied and Pure Biology, 23(1):67-72.
Andrews C, Chubb JC, 1974. Helminth parasites from Yorkshire fishes. Bulletin of the European Association of Fish Pathologists, 4(2):22-23.
Archdeacon TP, Bonar SA, Kline J, Iles A, Hughson D, 2008. Effects of the Asian Tapeworm on the endangered Mohave Tui Chub. Arizona, USA: Arizona Cooperative Fish and Wildlife Research Unit, 50 pp. [Fisheries Research Report 02-08.]
Bauer ON, Musselius VA, Strelkov YuA, 1969. Diseases of Pond Fishes. Moscow, USSR: "Kolos". [English version published in 1973 by Israel Program for Scientific Translations, Jerusalem, Israel; 220 pp.]
Boonthai T, Herbst SJ, Whelan G, Deuren MG van, Loch TP, Faisal M, 2017. The Asian fish tapeworm Schyzocotyle acheilognathi is widespread in baitfish retail stores in Michigan, USA, 618(22 December 2017). https://parasitesandvectors.biomedcentral.com/articles/10.1186/s13071-017-2541-6
Buckner RL, Denner MW, Brooks DR, Buckner SC, 1985. Parasitic endohelminths from fishes of southern Indiana. Proceedings of the Indiana Academy of Science, 94:615-620.
Bunkley-Williams L, Williams EH, 1994. Parasites of Puerto Rican freshwater sport fishes. San Juan and Mayaguez, Puerto Rico: Department of Natural and Environmental Resources and Department of Marine Sciences, University of Puerto Rico, 164 pp. http://www.uprm.edu/biology/cjs/epub5/book.pdf
Buza L, Molnár K, Szakolczai J, 1970. [English title not available]. (Bothriocephalus acheilognathi elofor dulasa magyarorszagon.) Holaszat, 16:42-43.
Bykhovskaya-Pavlovskaya IE, et al. , 1962. Key to parasites of freshwater fish of the USSR. USSR: Zoological Institute Academy of Science USSR. [English version published in 1964 by NTIS, U.S. Department of Commerce, Springfield, Virginia, USA, no. TT76-58184]
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Choudhury A, Cole RA, 2012. Bothriocephalus acheilognathi Yamaguti (Asian tapeworm). In: A handbook of global freshwater invasive species [ed. by Francis, R. A.]. Oxford, UK: Earthscan, 385-400.
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Denis A, Gabron C, Lambert A, 1983. Presence in France of two parasites of east Asian origin: Diplozoon nipponicum Goto 1891 and Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda) in Cyprinus carpio (Teleostei, Cyprinidae). (Presence en France de deux parasites d'origine Est-asiatique: Diplozoon nipponicum Goto 1891 et Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda) chez Cyprinus carpio (Teleostei, Cyprinidae).) Bulletin Français de la Pêche et de la Pisciculture, 289:128-134. http://dx.doi.org/10.1051/kmae:1983012
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Fernando CH, Furtado JI, 1964. Helminth parasites of some Malayan freshwater fishes. Bulletin of the National Museum Singapore, 32:45-71.
Harris JH, 2013. Fishes from elsewhere. In: Ecology of Australian Freshwater Fishes [ed. by Humphries, P. \Walker, K.]., Australia: CSIRO Publishing, 259-280.
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Hoffman GL, 1999. Parasites of North American freshwater fishes, Second Edition. Ithaca, New York, USA: Cornell University Press.
Kezic N, Fijan N, Kajgana L, 1975. Bothriocephalosis of carp in S.R. Croatia. (Botriocefaloza sarana u SR Hrvatskoj.) Veterinarski Arhiv, 45:289-291.
Khalifa KA, 1986. Cestoda of freshwater farmed fishes in Iraq. Journal of Wildlife Diseases, 22(2):278.
Kim YG, Kim JY, Chun SK, 1986. Life History of Bothriocephalus opsariichthydis Yamaguti (Cestoda; Pseudophyllida) parasitized on Israel carp Cyprinus carpio (Linne). First intermediate host and developing procercoid. Bulletin of Fisheries Science Institute Kunsan, Fisheries Journal Collection, 1:1-10.
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Korting W, 1974. Bothriocephalosis of the carp. Veterinary Medical Review, No.2:165-171.
Kuchta R, Scholz T, 2007. Diversity and distribution of fish tapeworms of the 'Bothriocephalldea' (Eucestoda). Parassitologia, 49:21-38.
Kuperman BI, Matey VE, Warburton ML, Fisher RN, 2002. Introduced parasites of freshwater fish in Southern California. In: Proceedings of the Tenth International Congress of Parasitology, Vancouver, Canada, 4-9 August, 2002. Bologna, Italy: Medimond.
Kurashvili BE, 1990. Bothriocephalosis and lernaeosis in fish in closed water reservoirs of Georgia, USSR. Soobshcheniya Akademii Nauk Gruzinskoi SSR, 138:417-420.
Li, W. X., Zhang, D., Boyce, K., Xi, B. W., Zou, H., Wu, S. G., Li, M., Wang, G. T., 2017. The complete mitochondrial DNA of three monozoic tapeworms in the Caryophyllidea: a mitogenomic perspective on the phylogeny of eucestodes, 10(314), (27 June 2017). https://parasitesandvectors.biomedcentral.com/articles/10.1186/s13071-017-2245-y doi: 10.1186/s13071-017-2245-y
Liao H, Shih L, 1956. On the biology and control of Bothriocephalus gowkongensis Yeh, a tapeworm parasitic in the young grass carp (Ctenpharyngodon idellus C. & V.). Acta Hydrobiologica Sinica, 2:129-185.
Liao XH, 2002. Population dynamics of Bothriocephalus acheilognathi (Eucestoda: Bothriocephalidae) in juvenile grass carp Ctenopharyngodon idellus in pond culture in South China. Acta Zoologica Sinica, 48(2):154-166.
Liao XH, 2007. Diversity of the Asiatic tapeworm Bothriocephalus acheilognathi parasitizing common carp and grass carp in China. Acta Zoologica Sinica, 53(3):470-480.
López-Jiménez S, 1981. Cestodos de Peces I. Bothriocephalus (Clestobothrium) acheilognathi (Cestoda: Bothriocephalidae). (Cestodes of fishes I. Bothriocephalus (Clestobothrium) acheilognathi (Cestoda: Bothriocephalidae).) Anales de Instituto Biologia de Universidad Nacional Autónoma de México, Seria Zoología, 51:69-84.
Malevitskaya MA, 1958. The introduction of a parasite with a complex life cycle, Bothriocephalus gowkongensis Yeh, 1955, during acclimatization of fish from the Amur River. Doklady Akademii Nauk SSSR, 123(3): 961-964.
Malhotra SK, 1984. Cestode fauna of hill-stream fishes in Garhwal Himalayas, India. II. Bothriocephalus teleostei n. sp. from Barilius bola and Schizothorax richardsonii. Boletín Chileno de Parasitología, 39(1-2):6-9.
Matey, V. E., Ervin, E. L., Hover, T. E., 2015. Asian Fish Tapeworm (Bothriocephalus acheilognathi) Infecting a Wild Population of Convict Cichlid (Archocentrus nigrofasciatus) in Southwestern California, 114(2), 89-97. http://scholar.oxy.edu/scas/vol114/iss2/3
Meddour A, 1988. Parasites of freshwater fishes from Lake Oubeira, Algeria. PhD Dissertation. Liverpool, UK: University of Liverpool.
Mhaisen FT, Khamees NR, Ali AH, 2013. Checklists of cestodes of freshwater and marine fishes of Basrah Province, Iraq. Basrah Journal of Agricultural Science, 26(Special Issue 1):79-98.
Minervini R, Lombardi F, Cave D di, 1985. [English title not available]. (L'introduzione di Bothriocephalus acheilognathi Yamaguti 1934, in Italia: osservazioni su popolazioni naturali e di allevamento di carpa (Cyprinus carpio).) Rivista Italiana di piscicoltura e ittiopatologia, 20:27-32.
Mokhayer B, 1976. Fish disease in Iran. Rivista Italiana di Piscicoltura e Ittiopathologia, 11:123-128.
Nedeva I, Mutafova T, 1988. On the morphology of Botrhiocephalus acheilognathi Yamaguti, 1934 (Bothriocephalidae). Khelmintologiya, 26:39-46.
Oškinis V, 1994. Temperature and development of Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda) in laboratory conditions. Ekologija, 4:40-42.
Osmanov SO, 1971. Parasites of fishes of Uzbekistan. Tashkent, USSR: Izdatelstvo EAN Uzbekskoj SSR, 532 pp.
Otte E, Pfeiffer H, Supperer R, 1972. Mass occurrence of Bothriocephalus acheilognathi in pond carps. (Massenauftreten von Bothriocephalus acheilognathi in Teichkarpfen.) Wiener Tierärztliche Monatsschrift, 59:174-175.
Paperna I, 1991. Disease caused by parasites in the aquaculture of warm water fish. Annual Review of Fish Diseases, 1991:155-194.
Pérez-Ponce de Leon G, Rosas-Valdez R, Mendoza-Garfias B, Aguilar-Aguilar R, Falcón-Ordaz J, Garrido-Olvera L, Pérez-Rodriguez R, 2009. Survey of the endohelminth parasites of freshwater fishes in the upper Mezquital River Basin, Durango State, Mexico. Zootaxa, 2164:1-20.
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Radulescu I, Georgescu R, 1962. Contributions to the knowledge of the parasitofauna of the species Ctenopharyngodon idella in the first year of acclimatization in the Popular Republic of Romania. (Contributii la cunoasterea parasitofaunei specie Ctenopharyngodon idella in primul an de aclimatizare in P.R. Romîna.) Buletinul Institutului de Cercetari si Proiectari Pisciole, 21:85-91.
Raissy M, Ansari M, 2012. Parasites of Some Freshwater Fish from Armand River, Chaharmahal va Bakhtyari Province, Iran. Iranian Journal of Parasitology, 7(1):73-79.
Retief NR, Avenant-Oldewage A, Preez HH du, 2007. Ecological aspects of the occurrence of Asian tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934 infection in the largemouth yellowfish, Labeobarbus kimberleyensis (Gilchrist and Thompson, 1913) in the Vaal Dam, South Africa. Physics and Chemistry of the Earth, 32(15-18):1384-1390.
Rogers W, 1976. Grass carp hosts Asian tapeworm. Sports Fishing Institute Bulletin, 276:2-3.
Rojas-Sánchez A, García-Prieto L, 2008. Current distribution of the cestode Bothriocephalus acheilognathi in Mexico. (Distribución actual del céstodo Bothriocephalus acheilognathi en México.) In: Memorias XXV Simposio sobre Fauna Silvestre., Mexico: Universidad Nacional Autónoma de México, 89 -93.
Rysavy B, Moravec F, 1973. Bothriocephalus aegyptiacus sp. n. (Cestoda: Pseudophyllidea) from Barbus bynni, and its life cycle. Vestnik Ceskoslovenske Spolecnosti Zoologicke, 39:68-75.
Salgado-Maldonado G, Matamoros WA, Krieser BR, Caspeta-Mandujano JM, Mendoza-Franco EF, 2015. First record of the invasive Asian fish tapeworm Bothriocephalus acheilognathi in Honduras, Central America. Parasite, 22(5):1-6.
Salgado-Maldonado G, Pineda-López R, 2003. The Asian fish tapeworm Bothriocephalus acheilognathi: a potential threat to native freshwater fish species in Mexico. Biological Invasions, 5(3):261-268.
Scholz T, 1997. A revision of the species Bothriocephalus Rudolphi, 1808 (Cestoda: Pseudophyllidea) parasitic in American freshwater fishes. Systematic Parasitology, 36:85-107.
Scholz T, 1999. Parasites in cultured and feral fish. Veterinary Parasitology, 84(3/4):317-335.
Schäperclaus W, 1991. Fish Diseases vol. 2, 5th edition. New Delhi, India: Amerind Publishing.
Sinha AK, Mehrotra PN, 1991. Pathogenicity of Bothriocephalus acheilognathi (Yamaguti) in the intestine of Xiphophorus helleri (Heckel). Rivista di Parassitologia, 8(2):181-185.
Stojanovski S, Velkova-Jordanovska L, Blažekovic-Dimovska D, Smiljkov S, Rusinek O, 2013. Parasite fauna of Chondrosoma nasus (Linnaeus, 1758) (Teleostei: Cyprinidae) from Lake Ohrid (Macedonia). Natura Montenegrina, Podgorica, 12(3-4):753-760.
US Fish and Wildlife Service, 2015. National Wild Fish Health Survey. Washington, DC, USA: US Fish and Wildlife Service. http://www.fws.gov/wildfishsurvey/
Velasquez CC, 1982. Cestodes of freshwater fishes from the Philippines. In: Molecular and Biochemical Parasitology, Supplement [Abstracts: 5th International Congress of Parasitology, Toronto, Canada, 7-14 August, 1982], p.311.
Vismanis KO, Jurkane E, 1967. The agent of bothriocephalosis and its control. Trudy BaltNIIRKh, 2:167-170.
Warburton M, Kuperman B, Matey V, Fisher R, 2002. Parasite analysis of native and non-native fish in the Angeles National Forest. San Diego, California, USA: U.S. Geological Survey, Western Ecological Research Center, unpaginated. [2001 Final Report, Prepared for U.S. Forest Service, Angeles National Forest.]
Ward DL, 2005. Collection of Asian tapeworm (Bothriocephalus acheilognathi) from the Yampa river, Colorado. Western North American Naturalist, 65(3):403-404.
Ward DL, 2007. Removal and quantification of Asian tapeworm from humpback chub using Praziquantel. North American Journal of Aquaculture, 69(3):207-210.
Xi BW, Wang GT, Xie J, 2011. Occurrence of Bothriocephalus acheilognathi (Cestoda, Bothriocephalidea) in grass carp Ctenopharyngodon idella in the Changjian River Drainage. Chinese Journal of Oceanology and Limnology, 29(3):564-566.
Yeh IS, 1955. On a tapeworm Bothriocephalus gowkongensis n. sp. (Cestoda: Bothriocephalidae) from freshwater fish in China. Acta Zoologica Sinica, 7:69-74.
Žitnan R, 1973. [English title not available]. (Helminty rýb Dobšinskej (Hnileckej) priehrady a ich epizootologický význam.) Biolgické Práce, 19(6):1-97.
Öztürk T, Ahmet O, 2014. Comparative Invasive Asian Tapeworm Bothriocephalus acheilognathi Infections on the Lower Kizilirmak Delta Fishes. Journal of Academic Documents for Fisheries and Aquaculture, 1:1-7.
Distribution References
Akhter S, Fayaz A, Chishti MZ, Tariq KA, 2008. Seasonal dynamics of Bothiocephalus [Bothriocephalus] acheilognathi in Schizothorax spp. and cyprinid spp. from the Kashmir Valley. In: Indian Journal of Applied and Pure Biology, 23 (1) 67-72.
Buckner RL, Denner MW, Brooks DR, Buckner SC, 1985. Parasitic endohelminths from fishes of southern Indiana. [Proceedings of the Indiana Academy of Science], 94 615-620.
Bunkley-Williams L, Williams EH, 1994. Parasites of Puerto Rican freshwater sport fishes., San Juan and Mayaguez, Puerto Rico: Department of Natural and Environmental Resources and Department of Marine Sciences, University of Puerto Rico. 164 pp. http://www.uprm.edu/biology/cjs/epub5/book.pdf
Buza L, Molnár K, Szakolczai J, 1970. [English title not available]. (Bothriocephalus acheilognathi elofor dulasa magyarorszagon). In: Holaszat, 16 42-43.
CABI, Undated. Compendium record. Wallingford, UK: CABI
CABI, Undated a. CABI Compendium: Status inferred from regional distribution. Wallingford, UK: CABI
CABI, Undated b. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI
Choudhury A, Cole RA, 2012. Bothriocephalus acheilognathi Yamaguti (Asian tapeworm). In: A handbook of global freshwater invasive species, [ed. by Francis RA]. Oxford, UK: Earthscan. 385-400.
Denis A, Gabron C, Lambert A, 1983. Presence in France of two parasites of east Asian origin: Diplozoon nipponicum Goto 1891 and Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda) in Cyprinus carpio (Teleostei, Cyprinidae). (Presence en France de deux parasites d'origine Est-asiatique: Diplozoon nipponicum Goto 1891 et Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda) chez Cyprinus carpio (Teleostei, Cyprinidae)). In: Bulletin Français de la Pêche et de la Pisciculture, 289 128-134. http://dx.doi.org/10.1051/kmae:1983012
Dubinina MN, 1987. Class Cestoda Rudolphi, 1808. In: Key to the Parasites of Freshwater Fish of the USSR, 3 (2nd) [ed. by Bauer ON]. Leningrad, Nauka. 5-76.
Fernando CH, Furtado JI, 1964. Helminth parasites of some Malayan freshwater fishes. In: Bulletin of the National Museum Singapore, 32 45-71.
Hoffman GL, 1999. Parasites of North American freshwater fishes, Second Edition., Ithaca, New York, USA: Cornell University Press.
Kezic N, Fijan N, Kajgana L, 1975. Bothriocephalosis of carp in S.R. Croatia. (Botriocefaloza sarana u SR Hrvatskoj). In: Veterinarski Arhiv, 45 289-291.
Khalifa KA, 1986. Cestoda of freshwater farmed fishes in Iraq. In: Journal of Wildlife Diseases, 22 (2) 278.
Kim YG, Kim JY, Chun SK, 1986. Life History of Bothriocephalus opsariichthydis Yamaguti (Cestoda; Pseudophyllida) parasitized on Israel carp Cyprinus carpio (Linne). In: Bulletin of Fisheries Science Institute Kunsan, Fisheries Journal Collection, 1 1-10.
Korting W, 1974. Bothriocephalosis of the carp. Veterinary Medical Review. 165-171.
Kurashvili BE, 1990. Bothriocephalosis and lernaeosis in fish in closed water reservoirs of Georgia, USSR. In: Soobshcheniya Akademii Nauk Gruzinskoi SSR, 138 417-420.
Liao H, Shih L, 1956. On the biology and control of Bothriocephalus gowkongensis Yeh, a tapeworm parasitic in the young grass carp (Ctenpharyngodon idellus C. & V.). In: Acta Hydrobiologica Sinica, 2 129-185.
López-Jiménez S, 1981. Cestodes of fishes I. Bothriocephalus (Clestobothrium) acheilognathi (Cestoda: Bothriocephalidae). (Cestodos de Peces I. Bothriocephalus (Clestobothrium) acheilognathi (Cestoda: Bothriocephalidae)). In: Anales de Instituto Biologia de Universidad Nacional Autónoma de México, Seria Zoología, 51 69-84.
Meddour A, 1988. Parasites of freshwater fishes from Lake Oubeira, Algeria. In: PhD Dissertation, Liverpool, UK: University of Liverpool.
Minervini R, Lombardi F, Cave D di, 1985. (L'introduzione di Bothriocephalus acheilognathi Yamaguti 1934, in Italia: osservazioni su popolazioni naturali e di allevamento di carpa (Cyprinus carpio).)). In: Rivista Italiana di piscicoltura e ittiopatologia, 20 27-32.
Mokhayer B, 1976. Fish disease in Iran. In: Rivista Italiana di Piscicoltura e Ittiopathologia, 11 123-128.
Osmanov SO, 1971. Parasites of fishes of Uzbekistan., Tashkent, USSR: Izdatelstvo EAN Uzbekskoj SSR. 532 pp.
Paperna I, 1996. CIFA Technical Paper, 230 pp. http://www.fao.org/docrep/008/v9551e/v9551e00.htm
Radulescu I, Georgescu R, 1962. Contributions to the knowledge of the parasitofauna of the species Ctenopharyngodon idella in the first year of acclimatization in the Popular Republic of Romania. (Contributii la cunoasterea parasitofaunei specie Ctenopharyngodon idella in primul an de aclimatizare in P.R. Romîna). In: Buletinul Institutului de Cercetari si Proiectari Pisciole, 21 85-91.
Rogers W, 1976. Grass carp hosts Asian tapeworm. In: Sports Fishing Institute Bulletin, 276 2-3.
Salgado-Maldonado G, Matamoros WA, Krieser BR, Caspeta-Mandujano JM, Mendoza-Franco EF, 2015. First record of the invasive Asian fish tapeworm Bothriocephalus acheilognathi in Honduras, Central America. In: Parasite, 22 (5) 1-6.
Stojanovski S, Velkova-Jordanovska L, Blazekovic-Dimovska D, Smiljkov S, Rusinek O, 2013. Parasite fauna of Chondrosoma nasus (Linnaeus, 1758) (Teleostei: Cyprinidae) from Lake Ohrid (Macedonia). In: Natura Montenegrina, Podgorica, 12 (3-4) 753-760.
Velasquez CC, 1982. Cestodes of freshwater fishes from the Philippines. In: Molecular and Biochemical Parasitology, Supplement [Abstracts: 5th International Congress of Parasitology, Toronto, Canada, 7-14 August, 1982], 311.
Vismanis KO, Jurkane E, 1967. The agent of bothriocephalosis and its control. In: Trudy BaltNIIRKh, 2 167-170.
Warburton M, Kuperman B, Matey V, Fisher R, 2002. Parasite analysis of native and non-native ?sh inthe Angeles National Forest. 2001 Final Report., San Diego, USA: U.S. Forest Service.
Xi BW, Wang GT, Xie J, 2011. Occurrence of Bothriocephalus acheilognathi (Cestoda, Bothriocephalidea) in grass carp Ctenopharyngodon idella in the Changjian River Drainage. In: Chinese Journal of Oceanology and Limnology, 29 (3) 564-566.
Contributors
Top of page18/05/2015 Original text by:
Rebecca A. Cole, US Geological Survey, National Wildlife Health Center, Madison, Wisconsin, U.S.A.
Anindo Choudhury, Division of Natural Sciences, St. Norbert College, De Pere, Wisconsin, U.S.A.
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