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.

Diseases Table

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).

Host Animals

Climate

Latitude/Altitude Ranges

Rainfall Regime

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).

Pathway Causes

Pathway Vectors

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.

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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