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Bothriocephalus acheilognathi

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Datasheet

Bothriocephalus acheilognathi

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Summary

  • Last modified
  • 20 November 2019
  • Datasheet Type(s)
  • Invasive Species
  • Natural Enemy
  • Preferred Scientific Name
  • Bothriocephalus acheilognathi
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Metazoa
  •     Phylum: Platyhelminthes
  •       Class: Cestoda
  •         Subclass: Eucestoda
  • 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...

  • Principal Source

  • Draft datasheet under review

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Pictures

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PictureTitleCaptionCopyright
Bothriocephalus acheilognathi (Asian fish tapeworm); SEM - lateral view of the scolex. From humpback chub (Gila cypha), Little Colorado River, Grand Canyon, Colorado, USA.
TitleScolex
CaptionBothriocephalus 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
Bothriocephalus acheilognathi (Asian fish tapeworm); SEM - lateral view of the scolex. From humpback chub (Gila cypha), Little Colorado River, Grand Canyon, Colorado, USA.
ScolexBothriocephalus acheilognathi (Asian fish tapeworm); SEM - lateral view of the scolex. From humpback chub (Gila cypha), Little Colorado River, Grand Canyon, Colorado, USA.©Anindo Choudhury
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.
TitleScolex
CaptionBothriocephalus 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
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.
ScolexBothriocephalus 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

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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

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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

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

Notes on Taxonomy and Nomenclature

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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

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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

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

Last updated: 02 Feb 2021
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

AlgeriaPresent, LocalizedIntroducedLake Oubeira
Congo, Democratic Republic of theAbsent, Unconfirmed presence record(s)Lake Kivu; record is of B. kivuensis, synonymized with B. acheilognathi, but synonymy is questionable (see Choudhury and Cole, 2012)
EgyptAbsent, Unconfirmed presence record(s)Record is of B. aegyptiacus, synonymized with B. acheilognathi, but synonymy should be validated.
EthiopiaPresent
MauritiusPresentIntroducedPaperna reported a personal communication from J.G. Van As, University of the Free State, Bloemfontein, South Africa.
NigeriaPresentIntroducedNiger and Benue River confluence, Lokoja
RwandaAbsent, Unconfirmed presence record(s)Lake Kivu, as B. kivuensis, synonymized with B. acheilognathi, but synonymy requires validation (see Choudhury and Cole, 2012)
South AfricaPresentIntroducedInvasive

Asia

AfghanistanPresentIntroduced
AzerbaijanPresentIntroduced
ChinaPresentPresent based on regional distribution.
-ChongqingPresentNative
-FujianPresentNativeIn grass carp, but not in common carp
-GansuPresentNativeIn grass carp, but not in common carp
-GuangdongPresentNativeOriginally described by Yeh, 1955, as B. gowkongensis
-GuizhouPresentNativeIn common carp and grass carp
-HeilongjiangPresentNativeIn common carp, but not in grass carp
-HubeiPresentNativeLakes in the flood plains of the Yangtze River, in cultrinin cyprinids
-Inner MongoliaPresentNativeDong Lake
-JiangxiPresentNative
-JilinPresentNative
-LiaoningPresentNative
-NingxiaPresentNativeIn common carp, but not in grass carp
-ShanxiPresentNative
-SichuanPresentNative
-XinjiangPresentIntroducedIn common carp, but not in grass carp
-YunnanPresentIntroduced
GeorgiaPresentIntroducedIn closed reservoirs
India
-Jammu and KashmirAbsent, Unconfirmed presence record(s)Reported from hill streams in a native cyprinid. Species identification should be validated
-MeghalayaPresent2016Found in aquacultured grass carp (Ctenopharyngodon idella)
-Uttar PradeshPresentIntroducedReported in 1984 as B. teleostei -- that identification needs to be validated. In 2015 reported again, and identified by molecular methods, from introduced Xiphophorus hellerii.
IranPresentIntroducedInvasive
IraqPresentIntroducedInvasive
IsraelPresentIntroduced
JapanPresentSee Choudhury & Cole (2012) for a discussion of its status as a native or introduced species
KazakhstanPresentIntroducedInvasive
KyrgyzstanPresentIntroduced
MalaysiaPresentIntroduced
MongoliaAbsent, Unconfirmed presence record(s)Dubinina does not specifically mention Mongolia, only the Amur River drainage
PhilippinesPresentIntroduced
South KoreaPresentIntroducedKim et al. (1986) cited in Paperna (1996)
Sri LankaPresentIntroduced
TajikistanPresentIntroduced
TurkeyPresentIntroduced
TurkmenistanPresentIntroduced
UzbekistanPresentIntroduced

Europe

AlbaniaPresentLake Ohrid
AustriaPresentIntroducedCarp ponds
BelarusPresent
Bosnia and HerzegovinaPresentIntroducedCarp ponds
BulgariaPresentIntroduced
CroatiaPresentIntroducedKezic et al. (1975) cited in Hoffman (1999)
CzechoslovakiaPresent
FrancePresentIntroduced
GermanyPresentIntroducedInvasive
HungaryPresentDescribed as B. phoxini, in Phoxinus phoxinus
ItalyPresentIntroducedInvasive
LatviaPresentIntroducedCarp ponds. Vismanis and Jurkane (1967) cited in Kirjušina and Vismanis (2007)
North MacedoniaPresentIntroducedLake Ohrid
PolandPresentIntroduced
RomaniaPresentIntroduced
RussiaPresentPresent based on regional distribution.
-Central RussiaPresentIntroducedInvasiveMainly in aquaculture facilities
-Eastern SiberiaPresentNativeAmur River drainage
-Russian Far EastPresentNativeAmur River drainage
-Southern RussiaPresentIntroducedInvasiveMainly in aquaculture facilities
-Western SiberiaPresentIntroducedInvasiveMainly in aquaculture facilities
UkrainePresentIntroduced
United KingdomPresentIntroduced

North America

CanadaPresentPresent based on regional distribution.
-British ColumbiaAbsent, Invalid presence record(s)Specimens reported by Arai and Mudry (1983) were misidentified
-ManitobaPresentIntroducedLake 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)
-OntarioPresent, LocalizedIntroducedDetroit 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.
HondurasPresentIntroduced
MexicoPresent, WidespreadIntroducedInvasiveWidespread
PanamaPresentIntroduced
Puerto RicoPresentIntroduced
United StatesPresentPresent based on regional distribution.
-ArizonaPresent, WidespreadIntroducedInvasive
-ArkansasPresentIntroducedIn a hatchery
-CaliforniaPresentIntroduced1980Southern California
-ColoradoPresentIntroduced
-FloridaPresentIntroduced
-HawaiiPresentIntroduced
-IndianaPresentIntroduced
-KansasPresentIntroduced
-KentuckyPresentIntroduced
-LouisianaPresentIntroducedIn mosquitofish, Gambusia; Original citation: W. Font, Southeastern Louisiana University, Hammond, Louisiana, USA, personal communication, 2015
-MichiganPresentIntroducedIn wild in Detroit River, Lake Huron and Lake St. Clair; likely present in Lake Erie. Widespread in mostly wild-caught baitfish in retail stores.
-NebraskaPresentIntroduced
-NevadaPresentIntroduced1987Muddy River, Virgin River, bait shops
-New HampshireAbsent, Unconfirmed presence record(s)
-New MexicoAbsent, Unconfirmed presence record(s)Pecos River
-New YorkPresentIntroduced
-North CarolinaPresentIntroducedInvasiveIn a reservoir
-TexasPresentIntroducedInvasiveRio Grande/Río Bravo del Norte, Pecos River
-UtahPresentIntroducedVirgin River
-WisconsinPresentIntroducedLand-o-Lakes lakes

Oceania

AustraliaPresentIntroducedInvasive
-New South WalesPresentIntroduced
-VictoriaPresentIntroduced
New ZealandAbsent, Intercepted onlyArrived with grass carp imports from Hong Kong but intercepted during quarantine.

South America

ArgentinaPresent, LocalizedIntroduced
BrazilPresent, LocalizedIntroduced

History of Introduction and Spread

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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

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Australia Europe 1960s Hitchhiker (pathway cause) Yes No Harris (2013) Boolarra strain of common carp may be main cause of spread -- deliberate introduction of carp
Panama USA 1960s Hitchhiker (pathway cause) Yes No Choudhury et al. (2013) Probably imported with grass carp imported for control of aquatic vegetation. Documented
Romania Russian Federation 1950s Hitchhiker (pathway cause) No No Radulescu and Georgescu (1962) Probably transported with fish imported for aquaculture
UK Europe 1972-1973 Hitchhiker (pathway cause) No No Andrews et al. (1981) With fish imported for aquaculture. Europe stated as a “likely” source for one hatchery
Ukraine Russian Federation 1950s Hitchhiker (pathway cause) No No Bykhovskaya-Pavlovskaya et al. (1962) With fish imported for aquaculture. Documented
USA Malaysia 1960s Hitchhiker (pathway cause) Yes No Choudhury and Cole (2012); Hoffman and Schubert (1984) With fish imported for aquaculture; original shipments documented

Risk of Introduction

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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

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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

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CategorySub-CategoryHabitatPresenceStatus
Freshwater

Host Animals

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Animal nameContextLife stageSystem
Aristichthys nobilis (bighead carp)Aquatic: AdultEnclosed systems/Ponds
Carassius auratus auratus (goldfish)
Ctenopharyngodon idella (grass carp)Domesticated host; Wild hostAquatic: Adult|Aquatic/FryEnclosed systems/Ponds; Enclosed systems/Tanks
Cyprinus carpio (common carp)Domesticated host; Wild hostAquatic: Adult|Aquatic/FryEnclosed systems/Ponds; Enclosed systems/Tanks
Gambusia affinis (western mosquitofish)Wild hostAquatic: Adult
Gila bicolor mohavensis (Mohave tui chub)
Gila cyphaWild hostAquatic: Adult
Gila elegansExperimental settingsAquatic: AdultEnclosed systems/Freshwater recirculating systems
Gila robusta (roundtail chub)
Hypophthalmichthys molitrix (silver carp)Aquatic: FryEnclosed systems/Ponds
Notropis topeka
Plagopterus argentissimus (woundfin)Wild hostAquatic: Adult
Profundulus hildebrandi

Climate

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ClimateStatusDescriptionRemark
A - Tropical/Megathermal climate Tolerated Average temp. of coolest month > 18°C, > 1500mm precipitation annually
Af - Tropical rainforest climate Tolerated > 60mm precipitation per month
Am - Tropical monsoon climate Tolerated Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25]))
As - Tropical savanna climate with dry summer Tolerated < 60mm precipitation driest month (in summer) and < (100 - [total annual precipitation{mm}/25])
Aw - Tropical wet and dry savanna climate Tolerated < 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25])
B - Dry (arid and semi-arid) Tolerated < 860mm precipitation annually
BS - Steppe climate Tolerated > 430mm and < 860mm annual precipitation
BW - Desert climate Tolerated < 430mm annual precipitation
C - Temperate/Mesothermal climate Preferred Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C
Cf - Warm temperate climate, wet all year Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year
Cs - Warm temperate climate with dry summer Preferred Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter Preferred Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)
D - Continental/Microthermal climate Tolerated Continental/Microthermal climate (Average temp. of coldest month < 0°C, mean warmest month > 10°C)
Df - Continental climate, wet all year Tolerated Continental climate, wet all year (Warm average temp. > 10°C, coldest month < 0°C, wet all year)
Ds - Continental climate with dry summer Tolerated Continental climate with dry summer (Warm average temp. > 10°C, coldest month < 0°C, dry summers)
Dw - Continental climate with dry winter Tolerated Continental climate with dry winter (Warm average temp. > 10°C, coldest month < 0°C, dry winters)

Latitude/Altitude Ranges

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Latitude North (°N)Latitude South (°S)Altitude Lower (m)Altitude Upper (m)
50 30

Rainfall Regime

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Bimodal
Summer
Uniform
Winter

Means of Movement and Dispersal

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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

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CauseNotesLong DistanceLocalReferences
HitchhikerMoved worldwide in host fish, especially carp for aquaculture Yes Yes Bauer and Hoffman (1976); Choudhury and Cole (2012); Scholz et al. (2012)

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Aquaculture stockRearing of grass carp and common carp brood stock, fingerlings etc. Yes Bauer and Hoffman (1976)
BaitBait fish transfers spread the parasite into the U.S. southwest Yes Yes Heckmann et al. (1993); Scholz et al. (2012); Boonthai et al. (2017)
Host and vector organismsFish act as final hosts, copepod crustaceans as intermediate hosts; piscivorous birds can carry eggs Yes Yes Bauer and Hoffman (1976); Choudhury and Cole (2012); Prigli (1975); Scholz et al. (2012)
Pets and aquarium speciesAquarium fishes such as koi and goldfish Yes Yes Scholz et al. (2012)
Plants or parts of plantsInfected copepods may attach to aquatic vegetation. Yes Yes
WaterWater may contain propagative stages such as eggs, and copepods infected with parasite larvae Yes Yes

Economic Impact

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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

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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

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Threatened SpeciesConservation StatusWhere ThreatenedMechanismReferencesNotes
Gila bicolor mohavensis (Mohave tui chub)USA ESA listing as endangered speciesUSAParasitism (incl. parasitoid)Archdeacon et al. (2008)
Gila cyphaEN (IUCN red list: Endangered)USAParasitism (incl. parasitoid)Choudhury and Cole (2012); Hoffnagle et al. (2006); Stone et al. (2007)
Gila elegansCR (IUCN red list: Critically endangered)USAParasitism (incl. parasitoid)Hansen et al. (2006)
Gila robusta (roundtail chub)NT (IUCN red list: Near threatened)USA; Arizona; California; NevadaParasitism (incl. parasitoid)Brouder (1999); US Fish and Wildlife Service (2013)
Notropis topekaUSA ESA listing as endangered speciesUSAParasitism (incl. parasitoid)Koehle and Adelman (2007)
Plagopterus argentissimus (woundfin)EN (IUCN red list: Endangered); USA ESA listing as endangered speciesUSAParasitism (incl. parasitoid)Heckmann (2000); Heckmann (2009)
Profundulus hildebrandiEN (IUCN red list: Endangered)MexicoParasitism (incl. parasitoid)Velázquez-Velázquez et al. (2011)

Risk and Impact Factors

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Invasiveness
  • 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
Impact outcomes
  • 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
Impact mechanisms
  • Parasitism (incl. parasitoid)
Likelihood of entry/control
  • 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

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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

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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.

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