- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Pathogen Characteristics
- Hosts/Species Affected
- Biology and Ecology
- Notes on Natural Enemies
- Impact Summary
- Economic Impact
- Environmental Impact
- Threatened Species
- Risk and Impact Factors
- Distribution Maps
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PicturesTop of page
IdentityTop of page
Preferred Scientific Name
- Anguillicoloides crassus (Kuwahara, Niimi et Itagaki, 1974)
Other Scientific Names
- Anguillicola crassus Kuwahara, Niimi et Itagaki, 1974
International Common Names
- English: anguillicolosis; swim bladder worm; swimming bladder worm
Local Common Names
- Denmark: svømmeblæreorm
- Germany: Schwimmblasenwurm
- Netherlands: zwemblaasworm
- Poland: angwilikola
- Sweden: simblåsemask
Summary of InvasivenessTop of page
A. crassus is native to eastern Asia where it is a widespread, non-pathogenic parasite of the swimbladder of Anguilla japonica. Introduced to Germany with imported Japanese eels around 1980, it transferred to the European eel Anguilla anguilla and has subsequently spread throughout Europe and northern Africa. Following introduction to America, in less than 20 years it has spread from Texas to Cape Breton in Anguilla rostrata. It has the attributes of an excellent coloniser, including high fecundity, low intermediate host specificity and the ability to use a wide range of freshwater fish as paratenic hosts. These, and the uncontrolled transfers of live eels by man, have facilitated its spread and made it the most invasive helminth known. It can be highly pathogenic to Atlantic eels, damaging swimbladders and able to cause mortalities. It affects eels’ swimming abilities and it is feared that it reduces their ability to migrate to their marine spawning grounds.
Taxonomic TreeTop of page
- Domain: Eukaryota
- Kingdom: Metazoa
- Phylum: Nematoda
- Class: Secernentea
- Subclass: Spiruria
- Order: Camallanida
- Suborder: Camallanina
- Family: Anguillicolidae
- Genus: Anguillicoloides
- Species: Anguillicoloides crassus
Notes on Taxonomy and NomenclatureTop of page
Adults of all five species are parasitic in the swim bladders of eels of the genus Anguilla. The preferred host of each is a species of Pacific eel and their heartland and the original area of their distribution is in Asia and Africa, i.e. in countries bordered by the Pacific and Indian oceans. Thus, Anguillicola globiceps Yamaguti, 1935 is a parasite of Anguillajaponica and its native distribution is in China and Japan. A. crassus is probably widespread throughout China, Japan and Korea and its preferred host there is also Anguilla japonica, but Moravec (2006) believes that it may have been introduced into Japan with imports of eels and that its region of origin is elsewhere in the Pacific. The antipodean species Anguillicoloides australiensis (Johnston and Mawson, 1940) Moravec and Taraschewski, 1988 is restricted to Australia and (probably) New Zealand, and infects the long-finned eels Anguilla reinhardtii and, probably, Anguilla dieffenbachii. The other antipodean species, Anguillicoloides novaezelandiae Moravec and Taraschewski, 1988, is a native of New Zealand but also occurs in Australia, and it infects the short-finned eel Anguilla australis. The remaining species, Anguillicoloides papernai Moravec and Taraschewski, 1988, is a native of South Africa and infects the African long-finned eel Anguilla mossambica. It would seem possible that there may be other species in the genus still to be described which infect other species of Pacific eels, but the parasite fauna of these species is still very poorly known. There are no species of anguillicolid native to the Atlantic eels Anguilla anguilla and Anguilla rostrata.
DistributionTop of page
It would appear that A. crassus was originally restricted to East Asia throughout which it is probably widespread and endemic, especially in China, Japan, Korea and Taiwan (there are not many records of its being definitely identified in China, probably because as a non-pathogenic species it is likely to be considered unimportant, and because of its similarity to Anguillicola globiceps). It is likely that it is present in other countries in this region and it has been reported from Thailand (Moravec, 2006) but there have been very few or no published reports of eel parasites from many parts of Eastern Asia. Its natural range probably coincides with that of its preferred host Anguilla japonica.
Distribution TableTop of page
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.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|China||Present||Present based on regional distribution.|
|-Fujian||Present||Native||Nagasawa et al., 1994||In culture|
|-Hubei||Present||Native||Nagasawa et al., 1994||In culture|
|Japan||Present||Present based on regional distribution.|
|-Hokkaido||Widespread||Native||Nagasawa et al., 1994||Especially in culture|
|-Honshu||Widespread||Native||Nagasawa et al., 1994||Culture in wild|
|Korea, Republic of||Present||Native||Kim et al., 1989||Reported from culture|
|Taiwan||Widespread||Native||Münderle et al., 2006||Wild and in culture|
|Turkey||Present||Introduced||Invasive||Genç et al., 2005||In several rivers|
|Egypt||Present||Introduced||Invasive||Mohamed and Nouh, 2004|
|Morocco||Localised||Introduced||Invasive||Loukilli and Belghyti, 2007||Known since 1999|
|Réunion||Localised||Introduced||Invasive||Sasal et al., 2008||Reported from African eel species, and believed to have been introduced by man|
|Tunisia||Localised||Introduced||Invasive||Maamouri et al., 1999||In one lake system, but extending range|
|Canada||Present||Present based on regional distribution.|
|-New Brunswick||Widespread||Introduced||Invasive||Aieta and Oliveira, 2009|
|-Newfoundland and Labrador||Widespread||Introduced||Invasive||Aieta and Oliveira, 2009|
|-Nova Scotia||Widespread||Introduced||Invasive||Aieta and Oliveira, 2009|
|-Prince Edward Island||Widespread||Introduced||Invasive||Aieta and Oliveira, 2009|
|USA||Present||Present based on regional distribution.|
|-Maine||Widespread||Introduced||Invasive||Aieta and Oliveira, 2009|
|-Maryland||Widespread||Introduced||Invasive||Barse et al., 2001|
|-Massachusetts||Widespread||Introduced||Invasive||Aieta and Oliveira, 2009|
|-New York||Localised||Introduced||Invasive||Machut and Limburg, 2007||In Hudson River watershed|
|-North Carolina||Present||Introduced||Invasive||Moser et al., 2001|
|-Rhode Island||Present||Introduced||Invasive||Aieta and Oliveira, 2009|
|-South Carolina||Localised||Introduced||Invasive||Fries et al., 1996|
|-Texas||Present||Introduced||circa 1995||Invasive||Johnson et al., 1995||First record in N. America|
|Austria||Localised||Introduced||Invasive||Schabuss et al., 2005||Foci in stocked lakes|
|Belgium||Widespread||Introduced||Invasive||Schabuss et al., 1997||First records 1980s|
|Czech Republic||Widespread||Introduced||Invasive||Baruš et al., 1999a||Introduced with eel stocking|
|Denmark||Widespread||Introduced||Invasive||Køie, 1991||Introduced with eel stocking|
|Estonia||Present||Introduced||Invasive||Höglund and Thomas, 1992|
|France||Widespread||Introduced||Invasive||Dupont and Petter, 1988||Early introduction into south|
|Germany||Widespread||Introduced||Invasive||Sures et al., 1999a; Neumann, 1985; Hartmann, 1987; Würtz et al., 1998||First record from Europe in Weser-Ems in 1982. Now in all major rivers.|
|Hungary||Localised||Introduced||Invasive||Molnár, 1994||Usually in stocked lakes, especially Lake Balaton|
|Ireland||Widespread||Introduced||Invasive||Evans and Matthews, 1999; Evans et al., 2001||First report 1998, but now spreading rapidly. Introduced with eel trade|
|Italy||Widespread||Introduced||Invasive||Canestri-Trotti, 1987; Koops and Hartmann, 1989||Introduced with eels imported from France. Mainly in eel culture|
|Netherlands||Widespread||Introduced||Invasive||Borgsteede et al., 1999||First reported soon after arrival in Europe|
|Norway||Localised||Introduced||Invasive||Mellergaard, 1988||Slower colonisation near limit of the species range|
|Portugal||Widespread||Introduced||Invasive||Maíllo et al., 2005||Often in coastal lagoons|
|Russian Federation||Present||Present based on regional distribution.|
|-Central Russia||Localised||Introduced||Invasive||Rodjuk and Shelenkova, 2006||Mainly around Kaliningrad and Baltic Sea|
|Slovakia||Localised||Introduced||Invasive||Moravec, 2006||In River Danube system|
|Spain||Localised||Introduced||Invasive||Aguilar et al., 2005||Localisation may reflect areas of study|
|Sweden||Localised||Introduced||Invasive||Hellstrom et al., 1988; Höglund and Thomas, 1992||Initially only in thermal effluents but now spreading more widely in south.|
|UK||Widespread||Introduced||Invasive||Kennedy and Fitch, 1990; Lyndon and Pieters, 2005||Introduced with eel trade in south and east in 1987. Now widespread all over including Scotland.|
History of Introduction and SpreadTop of page
A. crassus is the most efficient invasive helminth known (Nagasawa et al., 1994) but its rapid spread throughout the distribution range of the two species of Atlantic eel has been facilitated by, and is due in no small measure to, the uncontrolled inter-continental transfer of live eels. Its spread has, in fact, been so rapid that it has exceeded the rate at which it can be documented and any published account is invariably out of date. References cited in the table therefore tend to report the early stages of invasion as it is not possible to keep pace with the parasite’s subsequent spread throughout a country. It is already widespread throughout Europe (Ashworth and Blanc, 1997; Kirk, 2003; Moravec, 1992, 2006) and it can be predicted that its distribution range in Atlantic eels will become congruent with that of the eels themselves.
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|Germany||circa 1982||Aquaculture (pathway cause)||Yes||Koops and Hartmann (1989); Neumann (1985)||First introduction in Europe, to Bremerhaven probably from Taiwan, imported with live eels|
|Italy||France||Aquaculture (pathway cause)||Introduced with eel imports|
|Texas||Asia||Aquaculture (pathway cause)||Yes||Wielgoss et al. (2008)||From Asia, probably Japan, to Texas, N. America|
|UK||1987||Aquaculture (pathway cause)||Introduced with eel imports|
Risk of IntroductionTop of page
Although movements of eels for purposes of stocking and farming have played a major role in the rapid and widespread dissemination of A. crassus (Kennedy and Fitch, 1990; Belpaire et al., 1989) it is important to appreciate that A. crassus itself possesses many of the attributes of a successful coloniser (Kennedy and Fitch, 1990). These include: 1) a high reproductive potential, 2) a relatively simple life cycle with a low degree of specificity towards its intermediate host, including estuarine species of copepod, 3) the ability to use a wide range of fish species as paratenic hosts, 4) free living L2 larvae capable of surviving and remaining infective for long periods in freshwater of a range of salinities and in sea water, 5) the capability of infecting eels of all sizes, 6) the ability to survive for long periods in eels living in sea water, and 7) escaping the restrictions of a narrow specificity to its definitive host by using a species of fish that is itself widespread in distribution and capable of surviving a wide range of habitat and environmental conditions. It also occupies the swimbladder of an eel, a habitat in which there is no competitor. Every eel within the temperature and pH range of A. crassus is thus potentially at risk of infection. A combination of the colonisation abilities of the parasite, the natural movements of eels themselves and transfers of eels by man have enabled A. crassus to colonise Europe, North America and North Africa within 25 years: this is an extraordinary achievement.
Pathogen CharacteristicsTop of page
A. crassus is, like all anguillicolids, parasitic as an adult in the lumen of the swimbladder of its eel host. Eels acquire infections by ingestion of an infected copepod, the intermediate host, or by ingestion of an infected fish, a paratenic host. In either case, the L3 larvae migrate to the swimbladder wall of the eel, where they moult to the L4 stage and eventually move into the lumen of the swimbladder and develop into adults. The adult is a large nematode with a stout body tapering at each end. It is a blood feeder with a well-developed buccal capsule, a row of circumoral teeth and a muscular oesophagus. The presence of blood and the breakdown products of blood in the intestine give the whole nematode a dark, almost black, appearance. The sexes are separate. The body wall and other organs are typical of nematodes in general. Males range in length from about 6-23 mm and in width from 0.3 to 1.8 mm, whilst females range from 13-45 mm in length and from 1.2 – 5.0 mm in width. Females in particular appear very robust. They are ovoviviparous: the uterus occupies most of the space of the body and contains eggs which in turn contain developing embryos and fully formed larvae (L2). A single female may contain up to 500,000 eggs (Kennedy and Fitch, 1990). The eggs may hatch inside the female to release the larvae, or may be shed from the female and hatch in the pneumatic duct so that the larvae pass out to the exterior with the eel faeces. Females die in the swim bladder, which then contains live worms of each sex as well as disintegrating parasite tissues and numerous eggs. The presence of adult parasites, both living and dead, brings about characteristic changes in the thickness of the swimbladder wall and affects the gas content and functioning of the swimbladder.
Hosts/Species AffectedTop of page
As far as is known, all individuals of Anguilla anguilla are equally at risk of infection by A. crassus: small individuals by eating infected copepods and large individuals by eating infected fish. There is no resistance to re-infection (Haenen et al., 1996) and antibodies produced against the parasite have no protective function (Knopf and Lucius, 2008). Once A. crassus has entered a lake or eel farm, its prevalence often rises to 100%, and transmission rates and infection levels may be very high when eel densities are themselves high as in eel farms or shallow lakes (Molnár et al., 1994; Baruš et al. 1999a). Stress in individual eel hosts may predispose them to disease (Gollock et al., 2005a).
Biology and EcologyTop of page
The genetics of this species have been intensively studied, for more details see Heitlinger et al. (2009).
ClimateTop of page
|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||Tolerated||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|Cw - Warm temperate climate with dry winter||Tolerated||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)|
Notes on Natural EnemiesTop of page
There are no known natural enemies of A. crassus as such. There will always be some mortality of L2s through being eaten by copepods that are not suitable intermediate hosts and of L3s in paratenic hosts being eaten by fish other than eels or by birds, but there is no known predator or hyperparasite of adult parasites.
Impact SummaryTop of page
|Fisheries / aquaculture||Negative|
Economic ImpactTop of page
In the cases of the eel mortalities attributed to A. crassus in European lakes, the only figures available relate to mortalities. Thus, Molnár et al. (1991, 1994) state that in 1991, 200 tonnes of eels died in Lake Balaton, and in 1992 40 tonnes. Baruš et al. (1999a) similarly quote a figure 3.5 tonnes of eels killed in the Vranov Dam in 1994, but no financial values have been attached to these losses. It must be presumed that there was a severe economic loss to professional eel fishermen as a consequence of the mortalities but no figures are available to support this presumption.
Environmental ImpactTop of page
Impact on biodiversity
The effects of A. crassus on wild eel populations are more difficult to study than those on captive ones, but experiments suggest that infected eels are more likely to die in adverse conditions (Didziulis, 2006). Mass mortalities have been reported among wild eels, but only when there have been particular combinations of unfavourable circumstances (for more details, see datasheet on Anguillicolosis). Concern has been expressed that severe damage to the swimbladder may reduce the ability of eels to migrate to their spawning grounds in the Sargasso Sea, which could have a severe impact on the future of the population (Didziulis, 2006). Such a decline could have significant effects on ecosystem community structure.
Threatened SpeciesTop of page
Risk and Impact FactorsTop of page Invasiveness
- Proved invasive outside its native range
- Has a broad native range
- Abundant in its native range
- Highly adaptable to different environments
- Fast growing
- Has high reproductive potential
- Has propagules that can remain viable for more than one year
- Host damage
- Negatively impacts aquaculture/fisheries
- Parasitism (incl. parasitoid)
- Highly likely to be transported internationally accidentally
- Highly likely to be transported internationally illegally
- Difficult to identify/detect as a commodity contaminant
- Difficult to identify/detect in the field
- Difficult/costly to control
ReferencesTop of page
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Ashworth ST, 1994. Possible regulation in the Anguillicola crassus host-parasite system. In: Parasitic diseases of fish [ed. by Pike, A. W.\Lewis, J. W.]. Tresaith, Dyfed, UK: Samara Publishing, 141-150.
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Kennedy CR; Fitch DJ, 1990. Colonisation, larval survival and epidemiology of the nematode Anguillicola crassus, parasitic in the eel Anguilla anguilla, in Britain. Journal of Fish Biology, 36:117-131.
Knopf K, 2006. The swimbladder nematode Anguillicola crassus in the European eel Anguilla anguilla and the Japanese eels Anguilla japonica: differences in susceptibility and immunity between a recently colonised host and the original host. Journal of Helminthology, 80(2):129-136.
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Kuwahara A; Niimi A; Itagaki A, 1974. Studies on a nematode parasitic in the air bladder of the eel I. Descriprion of Anguillicola crassus n.sp. (Philometridea, Anguillicolidae. Japanese Journal of Parasitology, 23(5):275-279.
Køie M, 1991. Swimbladder nematodes (Anguillicola spp.) and gill monogeneans (Pseudodactylogyrus spp.) parasitic on the European eel (Anguilla anguilla). Journal de la Conseil International pour Exploration de la Mer, 47:391-398.
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OrganizationsTop of page
Denmark: North European and Baltic Network on Invasive Alien Species (NOBANIS), Web-based service, firstname.lastname@example.org, http://www.nobanis.org/
ContributorsTop of page
04/10/09 Original text by:
Clive Kennedy, University of Exeter, School of Biosciences, Geoffrey Pope Building, Stocker Road, Exeter, EX4 4QD, UK
Distribution MapsTop of page
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