Bothriocephalus acheilognathi

Pictures

Picture	Title	Caption	Copyright
Title Scolex Caption Bothriocephalus acheilognathi (Asian fish tapeworm); SEM - lateral view of the scolex. From humpback chub (Gila cypha), Little Colorado River, Grand Canyon, Colorado, USA. Copyright ©Anindo Choudhury	Scolex	Bothriocephalus acheilognathi (Asian fish tapeworm); SEM - lateral view of the scolex. From humpback chub (Gila cypha), Little Colorado River, Grand Canyon, Colorado, USA.	©Anindo Choudhury
Title Scolex Caption Bothriocephalus acheilognathi (Asian fish tapeworm); SEM - dorso-ventral view of the scolex. From non-native common carp (Cyprinus carpio). Litte Colorado River, Grand Canyon, Colorado, USA. Copyright ©Anindo Choudhury	Scolex	Bothriocephalus acheilognathi (Asian fish tapeworm); SEM - dorso-ventral view of the scolex. From non-native common carp (Cyprinus carpio). Litte Colorado River, Grand Canyon, Colorado, USA.	©Anindo Choudhury

Identity

Preferred 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

The 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

• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Platyhelminthes
•             Class: Cestoda
•                 Subclass: Eucestoda
•                     Order: Pseudophyllidea
•                         Family: Bothriocephalidae
•                             Genus: Bothriocephalus
•                                 Species: Bothriocephalus acheilognathi

Notes on Taxonomy and Nomenclature

Bothriocephalus 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

B. 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

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

History of Introduction and Spread

Bauer 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

Risk of Introduction

B. 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

Mature 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).

Habitat List

Climate

Latitude/Altitude Ranges

Means of Movement and Dispersal

B. 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).

Vectors and Intermediate Hosts

Economic Impact

B. 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

Impact 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

Risk and Impact Factors

• 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

Recent 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

Öztürk, 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.

Amin OM, 1978. Intestinal helminths of some Nile fishes near Cairo, Egypt with descriptions of Camallanus kirandensis Baylis, 1928 (Nematoda) and Bothriocephalus aegyptiacus Rysavy and Moravec 1975 (Cestoda). Journal of Parasitology, 64(1):93-101.

Andrews C, Chubb JC, 1974. Helminth parasites from Yorkshire fishes. Bulletin of the European Association of Fish Pathologists, 4(2):22-23.

Andrews C, Chubb JC, Coles T, Dearsley A, 1981. The occurrence of Bothriocephalus acheilognathi Yamaguti, 1934 (B. gowkongensis) (Cestoda: Pseudophyllidea) in the British Isles. Journal of Fish Diseases, 4(1):89-93.

Arai HP, Mudry DR, 1983. Protozoan and metazoan parasites of fishes from the headwaters of the Parsnip and McGregor Rivers, British Columbia: a study of possible parasite transfaunations. Canadian Journal of Fisheries and Aquatic Sciences, 40(10):1676-1684.

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.]

Arthur JR, Lumanlan-Mayo S, 1997. Checklist of the parasites of fishes of the Philippines. FAO Fisheries Technical Paper, No. 369:v + 102 pp. http://www.fao.org/3/contents/28ecae57-3ce8-5e48-8dc1-94a996537271/w6598e00.htm

Aydogdu A, Kostadinova A, Fernandez M, 2003. Variations in the distribution of parasites in the common carp, Cyprinus carpio, from Lake Iznik, Turkey: population dynamics related to season and host size. Helminthologia, 40(1):33-40.

Baer JG, Fain A, 1958. Bothriocephalus (Clestobothrium) kivuensis n. sp., cestode parasite of a barbel of Lake Kivu. (Bothriocephalus (Clestobothrium) kivuensis n.sp. ccstode parasite d'un barbeau du lac Kivu). Annales de la Societe Royale Zoologique de Belgique, 88:287-302.

Bauer ON, Hoffman GL, 1976. Helminth range extension by translocation of fish. Wildlife diseases (Proc. 3rd Internat. Wildlife Dis. Conf., Munich, 1975.) [ed. by Page, L.A.]. New York, USA: Plenum Press, 163-172.

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.]

Bean MG, Bonner TH, 2009. Impact of Bothriocephalus acheilognathi (Cestoda: Pseudophyllidea) on Cyprinella lutrensis condition and reproduction. Journal of Freshwater Ecology, 24(3):383-391. http://www.jfreshwaterecol.com/

Bean MG, Bonner TH, 2010. Spatial and temporal distribution of the Asian fish tapeworm Bothriocephalus acheilognathi (Cestoda: Bothriocephalidea) in the Rio Grande (Río Bravo del Norte). Journal of Aquatic Animal Health, 22(3):182-189. http://afsjournals.org/doi/abs/10.1577/H09-019.1

Bean MG, Seríková A, Bonner TH, Scholz T, Huffman DG, 2007. First record of Bothriocephalus acheilognathi in the Rio Grande with comparative analysis of ITS2 and V4-18S rRNA gene sequences. Journal of Aquatic Animal Health, 19(2):71-76.

Bertasso A, Avenant-Oldewage A, 2005. Aspects of the ecology of the Asian tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934 in yellowfish in the Vaal Dam, South Africa. Onderstepoort Journal of Veterinary Research, 72(3):207-217.

Boomker J, Huchzermeyer FW, Naude TW, 1980. Bothriocephalosis in the common carp in the Eastern Transvaal. Journal of the South African Veterinary Association, 51(4):263-264.

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

Borucinska JD, 2008. Diseases caused by Cestoda. In: Fish diseases, Volume 2 [ed. by Eiras, J. C.\Segner, H.\Wahli, T.\Kapoor, B. G.]. Enfield, USA: Science Publishers, Inc., 977-1024.

Bozorgnia A, Youssefi MR, Barzegar M, Hosseinifard SM, Ebrahimpour S, 2012. Biodiversity of parasites of fishes in Gheshlagh (Vahdat) Reservoir, Kurdistan Province, Iran. World Journal of Fish and Marine Sciences, 4(3):249-253. http://idosi.org/wjfms/wjfms4(3)12/6.pdf

Brabec, J., Kuchta, R., Scholz, T., Littlewood, D. T. J., 2016. Paralogues of nuclear ribosomal genes conceal phylogenetic signals within the invasive Asian fish tapeworm lineage: evidence from next generation sequencing data., 46(9), 555-562. http://www.sciencedirect.com/science/journal/00207519 doi: 10.1016/j.ijpara.2016.03.009

Brabec, J., Waeschenbach, A., Scholz, T., Littlewood, D. T. J., Kuchta, R., 2015. Molecular phylogeny of the Bothriocephalidea (Cestoda): molecular data challenge morphological classification., 45(12), 761-771. http://www.sciencedirect.com/science/journal/00207519

Brandt F de W, Van As JG, Schoonbee HJ, Hamilton-Attwell VL, 1981. The occurrence and treatment of bothriocephalosis in the common carp, Cyprinus carpio in fish ponds with notes on its presence in the largemouth yellowfish Barbus kimberleyensis from the Vaal Dam, Transvaal. Water SA, 7(1):34-42.

Britton JR, Pegg J, Williams CF, 2011. Pathological and ecological host consequences of infection by an introduced fish parasite. PLoS ONE, No.October:e26365. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0026365

Brouder MJ, 1999. Relationship between length of roundtail chub and infection intensity of Asian fish tapeworm Bothriocephalus acheilognathi. Journal of Aquatic Animal Health, 11(3):302-304.

Brouder MJ, Hoffnagle TL, 1997. Distribution and prevalence of the Asian fish tapeworm, Bothriocephalus acheilognathi, in the Colorado River and tributaries, Grand Canyon, Arizona, including two new host records. Journal of the Helminthological Society of Washington, 64(2):219-226.

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]

Chaudhary, A., Chiary, H. R., Bindu Sharma, Singh, H. S., 2015. First molecular identification of invasive tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda: Bothriocephalidea) in India., 4(4), 269-276. http://www.reabic.net/journals/bir/2015/4/BIR_2015_Chaudhary_etal.pdf doi: 10.3391/bir.2015.4.4.07

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, Charipar E, Nelson P, Hodgson JR, Bonar S, Cole RA, 2006. Update on the distribution of the invasive Asian fish tapeworm, Bothriocephalus acheilognathi, in the U.S. and Canada. Comparative Parasitology, 73(2):269-273. http://www.bioone.org/perlserv/?request=get-abstract&doi=10.1654%2F4240.1

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.

Choudhury A, Hoffnagle TL, Cole RA, 2004. Parasites of native and nonnative fishes of the Little Colorado River, Grand Canyon, Arizona. Journal of Parasitology, 90(5):1042-1053.

Choudhury A, Zheng Shuai, Pérez-Ponce de León G, Martínez-Aquino A, Brosseau C, Gale E, 2013. The invasive Asian fish tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934, in the Chagres River/Panama Canal drainage, Panama. BioInvasions Records, 2(2):99-104. http://www.reabic.net/journals/bir/2013/2/BIR_2013_2_Choudhury_etal.pdf

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.

Clarkson RW, Robinson AT, Hoffnagle L, 1997. Asian tapeworm (Bothriocephalus acheilognathi) in native fishes from the Little Colorado River, Grand Canyon, Arizona. Great Basin Naturalist, 57(1):66-69.

Davydov ON, 1978. Growth, development and fecundity of Bothriocephalus gowkongensis (Jen, 1955), a parasite of cyprinid fish. Gidrobiologicheskii Zhurnal, 14(4):70-77. [English translation: 1979, Hydrobiological Journal, 14(4):60–66]

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, Choudhury A, 1995. Cestoidea (Phylum Platyhelminthes). In: Fish diseases and disorders. Volume 1: protozoan and metazoan infections. [ed. by P. T. K. Woo]. CAB International, Wallingford., UK 391-414.

Dick TA, Gallagher C, Watkinson D, Franzin W, 2007. Red River Delta Fish Parasite Results. 20 + 29 pp.. http://hdl.handle.net/1993/30095

Djikanovic, V., Paunovic, M., Nikolic, V., Simonovic, P., Cakic, P., 2012. Parasitofauna of freshwater fishes in the Serbian open waters: a checklist of parasites of freshwater fishes in Serbian open waters., 22(1), 297-324. http://www.springerlink.com/link.asp?id=100215 doi: 10.1007/s11160-011-9226-6

Dove ADM, Cribb TH, Mockler SP, Lintermans M, 1997. The Asian fish tapeworm, Bothriocephalus acheilognathi, in Australian freshwater fishes. Marine and Freshwater Research, 48(2):181-183.

Dove ADM, Fletcher AS, 2000. The distribution of the introduced tapeworm Bothriocephalus acheilognathi in Australian freshwater fishes. Journal of Helminthology, 74(2):121-127.

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.

Edwards DJ, Hine PM, 1974. Introduction, preliminary handling, and diseases of grass carp in New Zealand. New Zealand Journal of Marine and Freshwater Research, 8(3):441-454.

Emde, S., Kochmann, J., Kuhn, T., Dörge, D. D., Plath, M., Miesen, F. W., Klimpel, S., 2016. Cooling water of power plant creates "hot spots" for tropical fishes and parasites., 115(1), 85-98. http://link.springer.com/article/10.1007%2Fs00436-015-4724-4 doi: 10.1007/s00436-015-4724-4

Evans BB, Lester RJG, 2001. Parasites of ornamental fish imported into Australia. Bulletin of the European Association of Fish Pathologists, 21(2):51-55.

Eyo JE, Iyaji FO, 2014. Parasites of Clarotes laticeps (Ruppell, 1832 Siluriformes, Bagridae) at Rivers Niger-Benue confluence, Lokoja, Nigeria. Journal of Fisheries and Aquatic Science, 9(3):125-133. http://scialert.net/abstract/?doi=jfas.2014.125.133

Faina F, Par O, 1977. Rinsing of the digestive tract of live carp as a diagnostic method for Bothriocephalus infections. (Vyuziti pruplachu zazivadel zivych kapru k diagnostice botriocefalozy.) Buletin - Vyzkumny Ustav Fybarsky a Hydrobiologicky Vodnany CSSR, No.2:15-21.

Fernando CH, Furtado JI, 1963. A study of some helminth parasites of freshwater fishes in Ceylon. Zeitschrift fur Parasitenkunde, 23(2):141-163.

Fernando CH, Furtado JI, 1964. Helminth parasites of some Malayan freshwater fishes. Bulletin of the National Museum Singapore, 32:45-71.

Font WF, 1997. Distribution of helminth parasites of native and introduced stream fishes in Hawaii. Bishop Museum Occasional Papers, No. 49:56-62.

Font WF, Tate DC, 1994. Helminth parasites of native Hawaiian freshwater fishes: an example of extreme ecological isolation. Journal of Parasitology, 80(5):682-688.

Fuller PL, Nico LG, Williams JD, 1999. Nonindigenous fishes introduced into inland waters of the United States. Bethesda, Maryland, USA: American Fisheries Society. [American Fisheries Society, Special Publication 27]

Granath WO Jr, Esch GW, 1983. Seasonal dynamics of Bothriocephalus acheilognathi in ambient and thermally altered areas of a North Carolina cooling reservoir. Proceedings of the Helminthological Society of Washington, 50(2):205-218.

Granath WO Jr, Esch GW, 1983. Survivorship and parasite-induced host mortality among mosquitofish in a predator-free, North-Carolina cooling reservoir. American Midland Naturalist, 110(2):314-323.

Granath WO Jr, Esch GW, 1983. Temperature and other factors that regulate the composition and infrapopulation densities of Bothriocephalus acheilognathi (Cestoda) in Gambusia affinis (Pisces). Journal of Parasitology, 69(6):1116-1124.

Han JeeEun, Shin SangPhil, Kim JiHyung, Choresca CH Jr, Jun JinWoo, Gomez DK, Park SeChang, 2010. Mortality of cultured koi Cyprinus carpio in Korea caused by Bothriocephalus acheilognathi. African Journal of Microbiology Research, 4(7):543-546. http://www.academicjournals.org/ajmr/PDF/Pdf2010/4Apr/Han%20et%20al.pdf

Hansen SP, Choudhury A, Cole RA, 2007. Evidence of experimental postcyclic transmission of Bothriocephalus acheilognathi in bonytail chub (Gila elegans). Journal of Parasitology, 93(1):202-204.

Hansen SP, Choudhury A, Heisey DM, Ahumada JA, Hoffnagle TL, Cole RA, 2006. Experimental infection of the endangered bonytail chub (Gila elegans) with the Asian fish tapeworm (Bothriocephalus acheilognathi): impacts on survival, growth, and condition. Canadian Journal of Zoology, 84(10):1383-1394. http://cjz.nrc.ca

Hanzelová V, Zitnan R, 1986. Embryogenesis and development of Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda) in the intermediate host under experimental conditions. Helminthologia, 23(3):145-155.

Harris JH, 2013. Fishes from elsewhere. In: Ecology of Australian Freshwater Fishes [ed. by Humphries, P. \Walker, K.]., Australia: CSIRO Publishing, 259-280.

Heckmann R, 2009. The fate of an endangered fish species (Plagopterus argentissimus) due to an invasive fish introduction (Cyprinella lutrensis) infected with Asian tapeworm (Bothriocephalus argentissimus): recovery methods. Proceedings of Parasitology, No.47:43-52.

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.

Heckmann RA, Deacon JE, Greger PD, 1986. Parasites of the woundfin minnow, Plagopterus argentissimus, and other endemic fishes from the Virgin River, Utah. Great Basin Naturalist, 46(4):662-676.

Heckmann RA, Greger PD, Deacon JE, 1987. New host records for the Asian fish tapeworm, Bothriocephalus acheilognathi, in endangered fish species from the Virgin River, Utah, Nevada, and Arizona. Journal of Parasitology, 73(1):226-227.

Heckmann RA, Greger PD, Furtek RC, 1993. The Asian fish tapeworm, Bothriocephalus acheilognathi in fishes from Nevada. Journal of the Helminthological Society of Washington, 60(1):127-128.

Hoffman GL, 1976. The Asian tapeworm, Bothriocephalus gowkongensis, in the United States, and research needs in fish parasitology. In: Proceedings of the 1976 Fish Farming Conference and Annual Convention of the Catfish Farmers of Texas, Texas Agricultural and Mechanical University, College Station, Texas, USA. pp. 84-90.

Hoffman GL, 1980. Asian tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934, in North America. Fisch und Umwelt, 8(Special):69-75.

Hoffman GL, 1999. Parasites of North American freshwater fishes, Second Edition. Ithaca, New York, USA: Cornell University Press.

Hoffman GL, Schubert G, 1984. Some parasites of exotic fishes. In: Distribution, biology and management of exotic fishes [ed. by Courtenay, W.R., Jr.\Stauffer, J.R.]. Baltimore, USA & London, UK: Johns Hopkins University Press, 233-261.

Hoffnagle TL, Choudhury A, Cole RA, 2006. Parasitism and body condition in humpback chub from the Colorado and Little Colorado rivers, Grand Canyon, Arizona. Journal of Aquatic Animal Health, 18(3):184-193.

Hoole D, Nisan H, 1994. Ultrastructural studies on the intestinal response of carp, Cyprinus carpio L. to the pseudophyllidean tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934. Journal of Fish Diseases, 17(6):623-629.

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.

Kirjusina M, Vismanis K, 2007. Checklist of the parasites of fishes of Latvia. FAO Fisheries Technical Paper, No.369/3:vi + 106 pp.

Kiskaroly M, 1977. Study of the parasite fauna of freshwater fishes from fish ponds of Bosnia and Herzegovina. I - Cyprinid fish ponds. B. Cestodes 1 (systematics and morphology). (Istrazivanje parazitofaune riba iz slatkovodnih ribnjaka BiH. I - Ciprinidni ribnjaci. B. Cestodi 1 (sistematika i morfologija).) Veterinaria, Yugoslavia, 26(4):477-483.

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.]

Kline SJ, Archdeacon TP, Bonar SA, 2009. Effects of praziquantel on eggs of the Asian tapeworm Bothriocephalus acheilognathi. North American Journal of Aquaculture, 71(4):380-383. http://afsjournals.org/doi/abs/10.1577/A08-038.1

Koehle JJ, Adelman IR, 2007. The effects of temperature, dissolved oxygen, and Asian tapeworm infection on growth and survival of the Topeka shiner. Transactions of the American Fisheries Society, 136(6):1607-1613. http://www.tandfonline.com/doi/full/10.1577/T07-033.1

Koehn JD, 2004. Carp (Cyprinus carpio) as a powerful invader in Australian waterways. Freshwater Biology, 49(7):882-894.

Korting W, 1974. Bothriocephalosis of the carp. Veterinary Medical Review, No.2:165-171.

Korting W, 1975. Larval development of Bothriocephalus sp. (Cestoda: Pseudophyllidea) from carp (Cyprinus carpio L.) in Germany. Journal of Fish Biology, 7(6):727-733.

Košuthová, L., Šmiga, L., Oros, M., Barcák, D., Košuth, P., 2015. The pathogenic Asian fish tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda) in the Red discus (Symphysodon discus)., 52(3), 287-292. http://www.degruyter.com/view/j/helmin

Kuchta R, Burianová A, Jirku M, Chambrier A de, Oros M, Brabec J, Scholz T, 2012. Bothriocephalidean tapeworms (Cestoda) of freshwater fish in Africa, including erection of Kirstenella n. gen. and description of Tetracampos martinae n. sp. Zootaxa, 3309:1-35. http://www.mapress.com/zootaxa/2012/f/zt03309p035.pdf

Kuchta R, Scholz T, 2007. Diversity and distribution of fish tapeworms of the 'Bothriocephalldea' (Eucestoda). Parassitologia, 49:21-38.

Kuchta, R., Choudhury, A., Scholz, T., 2018. Asian fish tapeworm: the most successful invasive parasite in freshwaters., 34(6), 511-523. http://www.sciencedirect.com/science/journal/14714922 doi: 10.1016/j.pt.2018.03.001

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.

Luo HY, Nie P, Zhang YA, Wang GT, Yao WJ, 2002. Molecular variation of Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda: Pseudophyllidea) in different fish host species based on ITS rDNA sequences. Systematic Parasitology, 52(3):159-166.

Luo HY, Nie P, Zhang YA, Yao WJ, Wang GT, 2003. Genetic differentiation in populations of the cestode Bothriocephalus acheilognathi (Cestoda, Pseudophyllidea) as revealed by eight microsatellite markers. Parasitology, 126(5):493-501.

Lusk S, Lusková V, Hanel L, 2010. Alien fish species in the Czech Republic and their impact on the native fish fauna. Folia Zoologica, 59(1):57-72.

Maitland PS, Campbell RN, 1992. Freshwater fishes of the British Isles. HarperCollins Publishers, London, UK. 368 pp.

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.

Marcogliese DJ, 2008. First report of the Asian fish tapeworm in the Great Lakes. Journal of Great Lakes Research, 34(3):566-569. http://www.iaglr.org/jglr/db/view_contents.php?pub_id=2661&mode=view&table=yes&topic_id=&mode=toc&volume=34&issue=3

Marcogliese DJ, Esch GW, 1989. Alterations in seasonal dynamics of Bothriocephalus acheilognathi in a North Carolina cooling reservoir over a seven-year period. Journal of Parasitology, 75(3):378-382.

Marcogliese DJ, Esch GW, 1989. Experimental and natural infection of planktonic and benthic copepods by the Asian tapeworm, Bothriocephalus acheilognathi. Proceedings of the Helminthological Society of Washington, 56(2):151-155.

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.

Méndez O, Salgado-Maldonado G, Caspeta-Mandujano JM, Cabañas-Carranza G, 2010. Helminth parasites of some freshwater fishes from Baja California Sur, Mexico. Zootaxa, 2327:44-50. http://www.mapress.com/zootaxa/2010/f/z02327p050f.pdf

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.

Mitchell A, Darwish A, 2009. Efficacy of 6-, 12-, and 24-h praziquantel bath treatments against Asian tapeworms Bothriocephalus acheilognathi in grass carp. North American Journal of Aquaculture, 71(1):30-34. http://afsjournals.org/doi/abs/10.1577/A07-091.1

Mitchell AJ, Hobbs MS, 2007. The acute toxicity of praziquantel to grass carp and golden shiners. North American Journal of Aquaculture, 69(3):203-206.

Mokhayer B, 1976. Fish disease in Iran. Rivista Italiana di Piscicoltura e Ittiopathologia, 11:123-128.

Molnár K, 1968. Bothriocephalus phoxini sp.n. (Cestoda, Pseudophyllidea) from Phoxinus phoxinus L. Folia Parasitologica, 15(1):83-86.

Molnár K, 1970. An attempt to treat fish bothriocephalosis with Devermin. Toxicity for the host and anti-parasitic effect. Acta vet. hung, 20(3):325-331.

Molnar K, Murai E, 1973. Morphological studies on Bothriocephalus gowkongensis Yeh, 1955 and B. phoxini Molnar, 1968 (Cestoda, Pseudophyllidea). Parasitologia Hungarica, 6(6):99-108.

Moravec F, Amin A, 1978. Some helminth parasites, excluding Monogenea, from fishes of Afghanistan. Acta Scientiarum Naturalium Academiae Scientiarum Bohemoslovacae, Brno, 12(6):1-45.

Muzzall, P. M., Thomas, M. V., Whelan, G., 2016. Occurrence of the Asian fish tapeworm, Bothriocephalus acheilognathi, in Notropis spp. (Cyprinidae) in Saginaw Bay and Port Sanilac, Lake Huron, and Lake St. Clair, Michigan, U.S.A., 83(1), 124-129. http://www.bioone.org/loi/copa doi: 10.1654/1525-2647-83.1.124

Nakajima K, Egusa S, 1974. Bothriocephalus opsariichthydis Yamaguti (Cestoda: Pseudophyllidea) found in the gut of cultured carp, Cyprinus carpio (Linne) - I. Morphology and taxonomy. Fish Pathology, 9(1):31-39.

Nedeva I, Mutafova T, 1988. On the morphology of Botrhiocephalus acheilognathi Yamaguti, 1934 (Bothriocephalidae). Khelmintologiya, 26:39-46.

Nedeva, I., 1988. On the biology of Bothriocephalus acheilognathi Yamaguti, 1934 (Bothriocephalidae)., (No. 26), 32-38.

Nie D-S, Pan J-P, 1985. Diseases of grass carp (Ctenopharyngodon idellus Valenciennes, 1844) in China, a review from 1953 to 1983. Fish Pathology, 20(2/3):323-330.

Nie P, Wang GT, Yao WJ, Zhang YA, Gao Q, 2000. Occurrence of Bothriocephalus acheilognathi in cyprinid fish from three lakes in the flood plain of the Yangtze River, China. Diseases of Aquatic Organisms, 41(1):81-82.

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.

Panczyk J, Zelazny J, 1974. Khawia sinensis and Bothriocephalus gowkongensis infections in carp - new parasitic diseases found in Poland. (Kawoiza i botriocefaloza karpi - nowe choroby pasozytnicze stwierdzone w Polsce.) Gospodarka Rybna, 26(6):10-13.

Paperna I, 1991. Disease caused by parasites in the aquaculture of warm water fish. Annual Review of Fish Diseases, 1991:155-194.

Paperna I, 1996. Parasites, infections and diseases of fishes in Africa: an update. CIFA Technical Paper, No. 31:230 pp. http://www.fao.org/docrep/008/v9551e/v9551e00.htm

Par O, Parova J, 1976. The tapeworm Bothriocephalus gowkongensis Yeh, 1955 in fish ponds in the Vodnany District. (Tasemnice Bothriocephalus gowkongensis Yeh, 1955 v rybnicich na Vodnansku.) Buletin - Vyzkumny Ustav Rybarsky a Hydrobiologicky Vodnany CSSR, No.2:34-42.

Par O, Parova J, Prouza A, 1977. Mansonil - an effective anthelmintic for the treatment of Bothriocephalus infections in carp. Buletin VURH (Vyzkumny Ustav Rybarsky a Hydrobiologicky) Vodnany, CSSR, No. 1:17-25.

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.

Petkov P, 1972. Occurrence of Bothriocephalus gowkongensis in carp bred in artificial water-reservoirs in the Pleven district. Veterinarnomeditsinski Nauki, 9(9):75-78.

Pool DW, 1987. A note on the synonomy of Bothriocephalus acheilognathi Yamaguti, 1934, B. aegyptiacus Rysavý and Moravec, 1975 and B. kivuensis Baer and Fain, 1958. Parasitology Research, 73(2):146-150.

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.

Prigli M, 1975. The role of aquatic birds in spreading Bothriocephalus gowkongensis Yeh, 1955 (Cestoda). (Uber die Rolle der Wasservogel bei der Verbreitung des Bothriocephalus gowkongensis Yeh, 1955 (Cestoda).) Parasitologia Hungarica, 8:61-62.

Pullen RR, Bouska WW, Campbell SW, Paukert CP, 2009. Bothriocephalus acheilognathi and other intestinal helminths of Cyprinella lutrensis in Deep Creek, Kansas. Journal of Parasitology, 95(5):1224-1226. http://www.journalofparasitology.org/perlserv/?request=get-abstract&doi=10.1645%2FGE-1891.1

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.

Rego AA, Chubb JC, Pavanelli GC, 1999. Cestodes in South American freshwater teleost fishes: keys to genera and brief description of species. Revista Brasileira de Zoologia, 16(2):299-367.

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.

Riggs MR, Esch GW, 1987. The suprapopulation dynamics of Bothriocephalus acheilognathi in a North Carolina reservoir: abundance, dispersion, and prevalence. Journal of Parasitology, 73(5):877-892.

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.

Scholz T, Cave D di, 1992. Bothriocephalus acheilognathi (Cestoda: Pseudophyllidea) parasite of freshwater fish in Italy. Parassitologia (Roma), 34(1/2/3):155-158.

Scholz T, Kuchta R, Williams C, 2012. Bothriocephalus acheilognathi. In: Fish parasites: pathobiology and protection [ed. by Woo, P. T. K.\Buchmann, K.]. Wallingford, UK: CABI, 282-297. http://www.cabi.org/cabebooks/ebook/20113395272

Schäperclaus W, 1991. Fish Diseases vol. 2, 5th edition. New Delhi, India: Amerind Publishing.

Scott AL, Grizzle JM, 1979. Pathology of cyprinid fishes caused by Bothriocephalus gowkongensis Yeh, 1955 (Cestoda: Pseudophyllidea). Journal of Fish Diseases, 2(1):69-73.

Sinha AK, Mehrotra PN, 1991. Pathogenicity of Bothriocephalus acheilognathi (Yamaguti) in the intestine of Xiphophorus helleri (Heckel). Rivista di Parassitologia, 8(2):181-185.

Stadtlander, T., Weyl, O. L. F., Booth, A. J., 2011. New distribution record for the Asian tapeworm Bothriocephalus acheilognathi Yamaguti, 1934 in the Eastern Cape province, South Africa., 36(3), 339-343. http://www.tandfonline.com/loi/taas20 doi: 10.2989/16085914.2011.636914

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.

Stone DM, Haverbeke DR van, Ward DL, Hunt TA, 2007. Dispersal of nonnative fishes and parasites in the intermittent Little Colorado River, Arizona. Southwestern Naturalist, 52(1):130-137. http://www.bioone.org/perlserv/?request=get-abstract&doi=10.1894%2F0038-4909%282007%2952%5B130%3ADONFAP%5D2.0.CO%3B2

Tekin-Özan S, Kir I, Barlas M, 2008. Helminth parasites of common carp (Cyprinus carpio L., 1758) in Bey?ehir Lake and population dynamics related to month and host size. Turkish Journal of Fisheries and Aquatic Sciences, 8(2):201-205.

Thapa, S., Das, S. K., 2016. Occurrence of Asian tapeworm Bothriocephalus acheilognathi (Yamaguti, 1934) in aquaculture systems of North East Hill region of India., 86(11), 1343-1345. http://www.icar.org.in

Urazbaev AN, Kurbanova AI, 2006. Parasitofauna of fish of the far east complex established in reservoirs of the southern Aral Sea. Vestnik Zoologii, 40(6):535-540, 572. www.v-zool.kiev.ua

US Fish and Wildlife Service, 2013. In: U.S. Fish and Wildlife Service species assessment and listing priority assignment form: Gila robusta. US Fish and Wildlife Service, 79 pp.. http://ecos.fws.gov/docs/candidate/assessments/2013/r2/E02Z_V01.pdf

US Fish and Wildlife Service, 2015. National Wild Fish Health Survey. Washington, DC, USA: US Fish and Wildlife Service. http://www.fws.gov/wildfishsurvey/

Van As JG, Basson L, 1984. Checklist of freshwater fish parasites from southern Africa. South African Journal of Wildlife Research, 14(2):49-61.

Van As JG, Schoonbee HJ, Brandt F de W, 1981. Further records of the occurrence of Bothriocephalus (Cestoda: Pseudophyllidea) in the Transvaal. South African Journal of Science, 77(8):343.

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.

Velázquez-Velázquez E, González-Solís D, Salgado-Maldonado G, 2011. Bothriocephalus acheilognathi (Cestoda) in the endangered fish Profundulus hildebrandi (Cyprinodontiformes), Mexico. Revista de Biología Tropical, 59(3):1099-1104. http://www.scielo.sa.cr/scielo.php?script=sci_arttext&pid=S0034-77442011000300012&lng=en&nrm=iso&tlng=en

Velázquez-Velázquez, E., Mendez-Gómez, B., Salgado-Maldonado, G., Matamoros, W., 2015. The invasive tapeworm Bothriocephalus acheilognathi Yamaguti, 1934 in the endangered killifish Profundulus candalarius Hubbs, 1924 in Chiapas, Mexico., 4(4), 265-268. http://www.reabic.net/journals/bir/2015/4/BIR_2015_VelazquezVelazquez_etal.pdf doi: 10.3391/bir.2015.4.4.06

Vincent AG, Font WF, 2003. Host specificity and population structure of two exotic helminths, Camallanus cotti (Nematoda) and Bothriocephalus acheilognathi (Cestoda), parasitizing exotic fishes in Waianu Stream, O'ahu, Hawai'i. Journal of Parasitology, 89(3):540-544.

Vismanis KO, Jurkane E, 1967. The agent of bothriocephalosis and its control. Trudy BaltNIIRKh, 2:167-170.

Waicheim A, Blasetti G, Cordero P, Rauque C, Viozzi G, 2014. Macroparasites of the invasive fish, Cyprinus carpio, in Patagonia, Argentina. Comparative Parasitology, 81(2):270-275. http://www.bioone.org/doi/abs/10.1654/1525-2647-81.2.270

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.

Yamaguti S, 1934. Studies on the helminth fauna of Japan. Part 4. Cestodes of fishes. Japanese Journal of Zoology, 6(1):1-112.

Yeh IS, 1955. On a tapeworm Bothriocephalus gowkongensis n. sp. (Cestoda: Bothriocephalidae) from freshwater fish in China. Acta Zoologica Sinica, 7:69-74.

Yera H, Kuchta R, Brabec J, Peyron F, Dupouy-Camet J, 2013. First identification of eggs of the Asian fish tapeworm Bothriocephalus acheilognathi (Cestoda: Bothriocephalidea) in human stool. Parasitology International, 62(3):268-271. http://www.sciencedirect.com/science/journal/13835769

Zekarias T, Yimer E, 2007. Study on parasites of fish at Lake Awassa, Ethiopia. Bulletin of Animal Health and Production in Africa, 55(3):149-155. http://www.ajol.info/journal_index.php?jid=227&tran=0&ab=bahpa

Žitnan R, 1973. [English title not available]. (Helminty rýb Dobšinskej (Hnileckej) priehrady a ich epizootologický význam.) Biolgické Práce, 19(6):1-97.

Zitnan R, Hanzelova V, Prihoda J, Kostan B, 1981. Evaluation of the efficacy of Taenifugin carp in the treatment of Bothriocephalus infections in carp at low water temperature. Biologizace e Chemizace Zivocisne vyroby, Veterinaria, 17(23)(5):471-477.

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.

Principal Source

Draft datasheet under review

Contributors

18/05/2015 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.

Distribution Maps