Bothriocephalus acheilognathi infection
Index
- Pictures
- Identity
- Pathogen/s
- Overview
- Host Animals
- Hosts/Species Affected
- Distribution
- Distribution Table
- Pathology
- Diagnosis
- List of Symptoms/Signs
- Disease Course
- Epidemiology
- Impact: Economic
- Impact: Environmental
- Zoonoses and Food Safety
- Disease Treatment
- Prevention and Control
- References
- Principal Source
- Contributors
- Distribution Maps
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Top of pagePreferred Scientific Name
- Bothriocephalus acheilognathi infection
Other Scientific Names
- Schyzocotyle acheilognathi infection
Overview
Top of pageBothriocephalus acheilognathi is a tapeworm that can infect a wide variety of freshwater fish but is primarily reported from cultured and wild carp. It is native to East Asia and over the last few decades has been spread widely throughout the world (to all continents except Antarctica) via human activities including 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 its eggs and spread them through defecation. Moderate to heavy infections can be fatal for fish fingerlings, or adults of small species, and infection with B. acheilognathi can be a problem for aquaculture (both through loss of fish and through disruption to operations and the costs of control); it is also suspected of adversely affecting a number of endangered wild fish species.
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 |
Hosts/Species Affected
Top of pageB. acheilognathi has been reported in over 300 species of fish (Dove et al., 1997; Dove and Fletcher, 2000; Salgado-Maldonado and Pineda-López, 2003; Rojas-Sánchez and García-Prieto, 2008; Bean and Bonner, 2009; Scholz et al., 2012; Kuchta et al., 2018), of which only a selection are recorded in the Hosts table. All freshwater fishes must be considered susceptible, unless shown otherwise. It prefers cyprinid fishes (barbs, carps, minnows, shiners, chub etc.); judging from records, grass carp Ctenopharyngodon idella and common carp Cyprinus carpio are two of its major hosts, although most of the records from common carp appear to be in fish farms (fingerlings of these species are the most severely affected stage, although adults can also be infected). However, it will infect atheriniform species (silversides) and cyprinodontiform species (topminnows, mollies, guppies, and allies). Some cichlids and eleotrids appear to be susceptible in the tropics. Planktivorous fish are particularly susceptible. Perches (Percidae), bass (Centrarchidae), pikes (Esocidae), temperate and tropical catfishes (Siluriformes) and suckers (Catostomidae) seem to be infected only rarely (Hoffman, 1999; Dove and Fletcher, 2000; Rojas-Sanchez and Garcia-Prieto, 2008; Choudhury and Cole, 2012; Scholz et al., 2012).
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 |
|||||||
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 |
|||||||
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 and 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 |
|||||||
Albania | Present | Lake Ohrid | |||||
Austria | Present | Introduced | Carp ponds | ||||
Belarus | Present | ||||||
Bosnia and Herzegovina | Present | Introduced | Carp ponds | ||||
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 |
|||||||
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 |
|||||||
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 |
|||||||
Argentina | Present, Localized | Introduced | |||||
Brazil | Present, Localized | Introduced |
Pathology
Top of pageThe pathology of B. acheilognathi infection has been summarized by Choudhury and Cole (2012) and by Scholz et al. (2012). “It includes inflammation, haemorrhaging, destruction and dysfunction of the intestinal mucosa, necrosis and even perforation (Scott and Grizzle, 1979; Hoole and Nisan, 1994; Schäperclaus, 1991; Sinha and Mehrotra, 1991; Heckmann, 2000). At the cellular level, separation and shedding of microvilli occurred at the interface between the gut and the tapeworm’s bothridia (Hoole and Nisan, 1994). Inflammation is accompanied by migration and infiltration of lymphocytes, macrophages and eosinophils to the infected area and even out of the gut to the parasite surface (Hoole and Nisan, 1994).” (Choudhury and Cole, 2012).
Diagnosis
Top of pageThere are no certain or exclusive external signs of bothriocephalosis unless worms protrude from the mouth (Han et al., 2010) or from the anus. In most cases, the disease is first suspected from the abdominal distension shown by smaller fish. Diagnosis is by examining faeces and finding eggs and segments, or by examining the gut of the fish. The gastrointestinal tract is either dissected open in a petri dish, or squashed between two glass plates if the gut is relatively thin walled. Either way, the preparation is best examined with a stereo dissecting scope (Choudhury et al., 2004; Scholz et al., 2012). In small fish, the gut can be squashed between two slides and examined with a compound microscope to search for parasites (C. Banner, Oregon State University, Corvallis, Oregon, USA, personal communication, 2015). Dissections are preferred in larger fish because the variable thickness of various regions of the gut, especially the thicker stomach wall, as well the presence of mucus, may interfere with the examinations. The fleshy heart-shaped scolex (when viewed laterally) – unique among Bothriocephalus spp. - along with rounded edges of the segments, and the medial position of the genital pores, allow a tentative first identification. Extracted worms must be fixed in a steaming hot fixative such as buffered 10% hot formalin (3.8% - 4% formaldehyde solution), except for a small piece – not the scolex - that should be stored in 95% or 100% molecular grade ethanol for molecular diagnoses. Fixed worms are stained and processed by standard methods, mounted permanently on slides and examined and identified using a compound microscope and available descriptions (Scholz, 1997). This identification can be supplemented by molecular data (Bean et al., 2007; Choudhury et al., 2013; Salgado-Maldonado et al., 2015). Choudhury and Cole (2012) discuss diagnosis in North America, while Kuchta et al. (2012) provide insight into issues in Africa.
List of Symptoms/Signs
Top of pageSign | Life Stages | Type |
---|---|---|
Finfish / Change in body shape - Body | Aquatic|Fry | Sign |
Finfish / Change in feed-conversion ratio - Miscellaneous | Sign | |
Finfish / Change in length-weight ratio - Body | Aquatic|Fry | Sign |
Finfish / 'Dropsy' - distended abdomen, 'pot belly' appearance - Body | Aquatic|Adult; Aquatic|Fry | Sign |
Finfish / Fish swimming near surface - Behavioural Signs | Aquatic|Fry | Sign |
Finfish / Intestines swelling / oedema - Organs | Sign | |
Finfish / Intestines white-grey patches (haemorrhage / necrosis / tissue damage) - Organs | Sign | |
Finfish / Mortalities -Miscellaneous | Aquatic|Adult; Aquatic|Fry | Sign |
Disease Course
Top of pageThe disease caused by B. acheilognathi is called ‘bothriocephalosis’ and has been reviewed by Hoffman and Schubert (1984), Schäperclaus (1991), Paperna (1991, 1996), Hansen et al. (2006), Borucinska (2008), Choudhury and Cole (2012), and Scholz et al. (2012). The parasite causes a decrease in weight of carp (Bauer et al., 1969; Britton et al., 2011); mortality of young fish caused by moderate to heavy infections 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), as well as in golden shiners (Notemigonus chrysoleucas) and mosquitofish (Gambusia) (Hoffman, 1980; Granath and Esch, 1983b).
Several authors have reviewed the common lesions seen in infections in various species of fish (Scott and Grizzle, 1979; Granath and Esch 1983a; Hoole and Nissan, 1994; Hansen et al., 2006, Han et al., 2010). Stunted growth in infected fish will limit mouth gape size which increases the time the fish relies on zooplankton as prey, thus extending the window of exposure to the infectious larvae (Hansen et al., 2006). As the worms grow, they cause mechanical obstruction and distension of the gut, especially in smaller fish (those which are small when mature, and the young of larger species) in which just a few worms can cause a significant problem. This is accompanied by gut inflammation which can have severe effects. Pathogenic changes are mainly due to the interaction between the worms’ scoleces (attachment organs) and the gut mucosa at the attachment site, but the gut mucosa can also be altered by the rest of the worm’s body (its strobila) in heavy infections, resulting in pressure necrosis and rupture. If left untreated, heavily infected fish suffer distress, which is manifested in altered behaviour and physiological complications that may affect other organs such as the liver. The condition worsens as the disease progresses, and eventually emaciation and pathology lead to death. On the other hand, light chronic infections may not have such a detrimental effect.
Hoffman (1999) suggests that in an aquaculture setting the higher susceptibility of smaller fish to heavy infections may decrease; however there are no data for this decrease in susceptibility in wild populations. Britton et al. (2011) showed that infected fish in experimental settings have a suppressed feeding rate when compared with paired controls of uninfected fish. In wild populations of fish, B. acheilognathi has been implicated in poor body condition (Hoffnagle et al., 2006).
Epidemiology
Top of pageB. acheilognathi typically has two hosts in its life cycle. As an adult, it lives in the gut of its fish host where it reproduces sexually and releases its eggs. The eggs pass out with the faeces into the water, where a ciliated larva, the coracidium, develops and eventually hatches out. Development is temperature dependent; at 28-30°C, larvae develop and hatch after a day, whereas at 14-15°C, it takes 10-28 days for development and hatching (Hoffman, 1980; Granath and Esch, 1983c; Paperna, 1996). Eggs do not develop below 12°C (Paperna, 1996). The hatched coracidium larva swims around, using its stored energy reserves, until it is eaten by a copepod (Marcogliese and Esch, 1989b; Paperna, 1996). Numerous species of cyclopoid copepods are suitable intermediate hosts (see Vectors and Intermediate Hosts table in the Bothriocephalus acheilognathi datasheet)). Coracidia survive longer (5-6 days) at lower temperatures (15-16°C -- Hanzelova and Zitnan, 1986), but may become sluggish (Granath and Esch, 1983c). Once consumed by a copepod, the larva burrows through the gut into the body cavity where it develops into a larval stage called a procercoid. Copepods may have several procercoids at the same time. In a week or so at 20°C, the procercoid develops a tiny rounded tail called a ‘cercomer’ and is now ready to infect a fish host. Small fish are more likely to become infected because of the higher proportion of zooplankton, and therefore of infected copepods, in their diet. When susceptible fish hosts ingest infected copepods, the procercoid larvae emerge from the copepod body and occupy the folds of the gut mucosa where they begin developing into typical, segmented, ‘strobilate’ tapeworms. In north-temperate regions, recruitment of larval worms into fish typically occurs in the autumn (fall) and worms produce eggs by the following spring. This seasonality may not be pronounced in the tropics. Strobilation – producing segments - is also temperature dependent. In a study in common carp (Cyprinus carpio), 89% of the worms became segmented in 16-20 days at 25°C, while 80% remained unsegmented 4 months later at 15°C (Oskinis, 1994). In barbs (also members of the Cyprinidae), maturation takes 1.5 -2 months at 15-22°C (Davydov 1978), while temperatures below 15°C hinder development (6-8 months). In grass carp (Ctenopharyngodon idella), worms mature in about three weeks at 28-29°C (Liao and Shih, 1956). Granath and Esch (1983c) found that worms in mosquitofish (Gambusia affinis) did not mature at 20°C. Such differences may be due to parasite strain/population differences along with differences in host physiology.
Hansen et al. (2007) showed, using different size classes of bonytail chub (Gila elegans) in experimental infections, that larger, suitable, predatory fish hosts can acquire and accumulate infections by consuming smaller infected fish.
Impact: Economic
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.
Impact: Environmental
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.
Zoonoses and Food Safety
Top of pageYera et al. (2013) report eggs of B. acheilognathi in the faeces of a patient presenting with stomach pains. The eggs were identified by molecular sequencing and the infection was reported as accidental and was the result of the tapeworm passing through the intestine after an infected fish was consumed. Apart from that, this parasite has never been described from mammals.
Disease Treatment
Top of pageVarious herbal extracts, such as from Cucurbita (gourds) and Areca (areca nut), were successfully used to treat Asian fish tapeworm infections before the advent of modern anthelminthics (Liao and Shih, 1956; Nie and Pan, 1985). Scholz et al. (2012) also mention horseradish (Armoracia rusticana) leaves and conifer needles.
Such herbal extracts were replaced by niclosamide-based drugs (see Dick and Choudhury, 1995, and table), which were quite successful. Molnár (1970) reported that niclosamide was effective in clearing Asian tapeworm infections in aquaria and experimental ponds when added to feed at doses between 0.1 and 20 g/kg body weight of fish. Par et al (1977) successfully used a dose of 1 g/kg body weight of fish. Zitnan et al. (1981) used ‘Taenifugin Carp’, a granulated medicated feed containing 0.7% niclosamide salt, and reported that administering this feed at 2% of body weight of fish (=0.14 g niclosamide/kg body weight of fish) was effective in clearing tapeworm infections. However, niclosamide was reported to be highly toxic to fish when administered in water (Molnár, 1970).
Praziquantel, which is administered either by water bath or in food, seems to be the current drug of choice. Time and dosage are important; Ward (2007) was able to clear infections in bonytail chub (Gila elegans) exposed to a dose of 1.5 mg/l for 24 hours. Mitchell and Darwish (2009) found that fish density during treatment also affected efficacy; grass carp (Ctenopharyngodon idella) immersed for 24 hrs at a density of 60 g/l, and 0.75 mg/l of praziquantel or higher, were cleared of the tapeworm. Their study showed that dosage must be adjusted to fish densities for effective treatment. Drug delivery must also take into account potential harm to fish at higher dosages (Mitchell and Hobbs, 2007).
Prevention and Control
Top of pageImmunization and Vaccines
There is currently no effective fish vaccine against B. acheilognathi.
Management Strategies in Aquaculture
(reviewed by Choudhury and Cole, 2012)
Infected fish should not be allowed into aquaculture facilities. Imported fish and new shipments should be quarantined and examined carefully for B. acheilognathi and other parasites and pathogens. ‘Disease free’ certification should include this species. Aquaculture operations may wish to deworm fish before introducing them to their aquaculture facilities. However, praziquantel-treated fish cannot be sold as food in the USA. Praziquantel will not kill the eggs or free coracidia swimming larvae (Kline et al., 2009). Copepod densities can be controlled in small indoor facilities, but probably not in outdoor ponds. Stocking of fish and movement between hatcheries should be done carefully. Bauer et al. (1969) noted success in treating the pond sediment after fish have been harvested. Drying the pond in the spring or freezing to a depth of 5-10 cm was recommended. Chemical treatment of drained ponds with chloride of lime (0.5-0.6 ton /hectare) in autumn decreased transmission. Chlorination (50 p.p.m bleaching powder -- Liao and Shih, 1956) or a combination of chlorination and freezing is even more efficacious (Bauer et al., 1969).
Management Strategies in the Wild
(reviewed by Choudhury and Cole, 2012)
Eradicating a parasite like B. acheilognathi in open systems such as interconnected lakes and streams is improbable. In systems where the parasite depends on the continued presence of an introduced host, as in Australia, eradicating that host (common carp, Cyprinus carpio) may eliminate the parasite. However, given the abundance of carp in eastern Australia, this seems unlikely to be feasible. Ward (2007) discussed a strategy for systematically deworming humpback chub (Gila cypha) from the Little Colorado River in the U.S. southwest, a river that is isolated by seasonally dry upstream regions and the cold Colorado River downstream. The abundance of the tapeworm from the Little Colorado River appears to have declined following this strategy.
References
Top of pageÖztürk, T., Özer, A., 2014. Comparative invasive Asian tapeworm Bothriocephalus acheilognathi on the lower Kizilirmak delta fishes Journal of Academic Documents for Fisheries and Aquaculture, 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]
Chauhan RS, Malhotra SK, 1986. Population biology of the pseudophyllidean cestode Bothriocephalus teleostei (Malhotra, 1984) in the Indian Hill-Stream teleosts. I. Influence of season and temperature. Boletín Chileno de Parasitología, 41(3-4):51-61.
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.
Chubb JC, 1981. The Chinese tapeworm Bothriocephalus acheilognathi Yamaguti, 1934 (synonym B. gowkongensis Yeh, 1955) in Britain. In: Proceedings of the 2nd British Freshwater Fisheries Conference, University of Liverpool, Liverpool, UK. 40-51.
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
Dick TA, Gallagher C, Watkinson D, Franzin W, 2007. Red River Delta Fish Parasite Results. 20 + 29 pp.. http://hdl.handle.net/1993/30095
Dubinina MN, 1987. Class Cestoda Rudolphi, 1808. In: Key to the Parasites of Freshwater Fish of the USSR, 2nd edition, Vol 3 [ed. by Bauer, O. N.]. Leningrad, USSR: Nauka, 5-76.
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.
Heckmann RA, 2000. Asian Tapeworm, Bothriocephalus acheilognathi (Yamaguti, 1934) a recent cestode introduction into the western United States of America: control methods and effect on endangered fish populations. Proceedings of Parasitology, 29:1-24.
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.
Kline J, Archdeacon T, Iles AC, Bonar SA, 2007. Factors influencing distribution of introduced Asian Tapeworm and effects on selected southwestern fishes (Yaqui topminnow and Yaqui chub). Arizona, USA: Arizona Cooperative Fish and Wildlife Research Unit, 55 pp. [Arizona Cooperative Fish and Wildlife Research Unit Fisheries Research Report 01-07.]
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.
Pool DW, Chubb JC, 1985. A critical scanning electron microsope study of the scolex of Botrhiocephalus acheilognathi Yamaguti, 1934 with a review of the taxonomic history of the genus Bothriocephalus parasitizing cyprinid fishes. Systematic Parasitology, 7(3):199-211.
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). First intermediate host and developing procercoid. 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. Cestodos de Peces I. Bothriocephalus (Clestobothrium) acheilognathi (Cestoda: Bothriocephalidae). (Cestodes of fishes I. Bothriocephalus (Clestobothrium) acheilognathi (Cestoda: Bothriocephalidae). In: Anales de Instituto Biologia de Universidad Nacional Autónoma de México, Seria Zoología, 51 69-84.
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)). 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 S O, 1971. Parasites of fish of Uzbekistan. 532pp.
Otte E, Pfeiffer H, Supperer R, 1972. Mass occurrence of Bothriocephalus acheilognathi in pond carps. (Massenauftreten von Bothriocephalus acheilognathi in Teichkarpfen). In: Wiener Tierärztliche Monatsschrift, 59 174-175.
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 fish in the Angeles National Forest. In: Final Report, Prepared for U.S. Forest Service, San Diego, California, USA: Geological Survey, Western Ecological Research Center.
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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