Description
Potentially misidentified species- 5 species of Anguillicoloides are known; A. globiceps and A. crassus are native to eastern Asia, while A. australiensis is native to Australia, A. papernai to southern Africa, and A. novaezelandiae to New Zealand. A. crassus and A. novaezelandiae have both been recorded from Anguilla anguilla the European Eel (in Italy), but A. crassus is much more widespread and is the only species recorded from North America. (Koie 1991; Barse et al. 2001).
Taxonomy
| Kingdom | Phylum | Class | Order | Family | Genus |
|---|---|---|---|---|---|
| Animalia | Nematoda | Secernertea | Dracunculoidea | Anguillicolidae | Anguillicoloides |
Synonyms
Invasion History
Chesapeake Bay Status
| First Record | Population | Range | Introduction | Residency | Source Region | Native Region | Vectors |
|---|---|---|---|---|---|---|---|
| 1997 | Established | Expanding | Introduced | Regular Resident | Eastern Atlantic | Western Pacific | Shipping(Ballast Water),Fisheries(Fisheries Accidental) |
History of Spread
The nematode Anguillicoloides crassus was described from Japan by Kuwuhara et al. (1974), who found it in the swimbladders of the Japanese Eel (Anguilla japonica). It is widespread in Japan and coastal China . A. crassus was first collected in Europe in 1982 in the Weser-Ems region of Germany (Moravec 1992), as a parasite of the European Eel, (Anguilla anguilla). It was probably transported to Europe with commercial shipments of live Anguilla japonica The early stages of this parasite infect copepods and amphipods, which is probably how this parasite entered A. anguilla populations (Koie 1991; Bauer 1991). The spread of A. crassus in Europe was rapid; by 1991 it had been reported from the coast of Sweden, Poland, the British Isles, Spain, Italy, Hungary, and Egypt, in habitats ranging from inland freshwater to fully marine. In many European locations, infection rates approach 100%.(Kennedy and Fitch 1990; Koie 1991; Moravec 1992; Pilcher and Moore 1993). The parasite has been found on the Atlantic Coast of Morocco (Loukili and Belghyti 2007) and in the Indian Ocean on the island of Reunion (Sasal et al. 2008), on the eel A. bicolor (Sasal et al. 2008).
Anguillicoloides crassus was first discovered in North America at an aquaculture facility in south TX , in a batch of elvers (juvenile eels) of unknown origin. To determine whether the parasite had spread outside the facility, wild American Eels (Anguilla rostrata) were sampled in 6 TX rivers, but no parasites were found. However, a sample of 8 eels from Winyah Bay SC contained one infected indivdual (Fries et al. 1996). A survey of eels in the major coastal rivers of NC in 1998-99 found infected eels in all of the 17 rivers sampled, with an overall prevalence of 52% and a mean prevalence of 3.9 worms per eel (Moser et al. 2001).
Chesapeake Bay- In the summer of 1997,Anguillicoloides crassus was found in Anguilla rostrata taken from the Wye, Sassafras, Patuxent Rivers in MD (Barse and Secor 1999). Another survey showed a 90% infection rate for eels from the Potomac River (Anonymous 1998). A more comprehensive survey, in 1998-1999, found that A. crassus was present in eels caught at all Bay stations examined, from the tidal Susquehanna River to the Potomac and Pocomoke Rivers, but absent in eels at Ocean City MD, in Chincoteague Bay (Barse et al. 2001). Prevalence (% of eels infected) and intensity (number of worms per eel) tended to increase up the Bay, from 13% of eels infected, and 2.7 worms per eel in the Pocomoke to 82.4% of eels infected, and 9 worms per eel in the Susquehanna (Barse et al. 2001). In the Sassafras and Wye Rivers, prevalence increased from the spring of 1997, to the spring of 1998, suggesting increasing spread of this parasite (Barse et al. 2001). In a 2007 survey, the mean prevalence of the parasite was 40.1%, but ranged from 17.8% in the James River to 72% in the Sassafras River. This represents an increase a roughly three-fold increase since inital surveys. Eels captured in fall had a decreased prevalence of parasites and swimbladder damage, possibly indicating recovery from parasitism (Fenske et al. 2010).
Hudson River- A survey by Barse, Baker, and Secor in the Hudson River found A. crassus in eels collected in the upper estuary, at River Kms 210-140, but not in the lower estuary at Km 60 (Haverstraw Bay). Infection rates were 8-20% (Barse and Secor 1999). In later surveys, it was found from the George Washington Bridge to Albany (Morrison et al. 2003) and many tributary streams (Machut and Limburg 2004).
Long Island Sound to the Gulf of Maine- In a field survey in 2005-2006, A. crassus was found to infect American Eels in many rivers from the Pawcatuck on the RI-CT border to the Penobscot River in ME. A single infected eel was found in the St. Johns River, New Brunswick (Aieta and Olivera 2009).
Maritime Atlantic Coast and Gulf of St. Lawrence- Several infected eels were found on the Atlantic Coast of Cape Breton Island, at Sydney and the Mira River 2007, Rockwell et al. 2009), and on the north and west coasts of Cape Breton in 2006 (Aeta and Olivera 2009). One infected eel was found in Silver Lake, Amherst, New Brunswick, draining into the Gulf of St. Lawrence, but none were observed in collections at several sites in the St. Lawrence River (Aeta and Olivera 2009).
Barse and Secor 1999; Barse et al. 2001; Bauer 1991; Fries et al. 1996; Kennedy and Fitch 1990; Koie et al. 1991; Kuwuhara et al. 1974; Moravec 1992; Moser et al. 2001; Pilcher and Moore 1993
Invasion Comments
Probable vectors into Chespeake Bay- Ballast water is considered the likeliest vector for transport of this parasite into the Bay, because of the absence of local eel aquaculture operations (Secor 1998 personal communication). Freshwater cyclopoid copepods, the most frequent intermediate host of Anguillicola crassus (Koie 1991), are frequently seen in samples of ballast water about to be discharged into the Bay.
Ecology
Environmental Tolerances
| For Survival | For Reproduction | |||
|---|---|---|---|---|
| Minimum | Maximum | Minimum | Maximum | |
| Temperature (ºC) | 10.0 | 30.0 | ||
| Salinity (‰) | 0.0 | 35.0 | 0.0 | 15.0 |
| Oxygen | ||||
| pH | 4.2000000000 | 9.2000000000 | ||
| Salinity Range | fresh-eu |
Age and Growth
| Male | Female | |
|---|---|---|
| Minimum Adult Size (mm) | 5.7 | 16.2 |
| Typical Adult Size (mm) | 30.8 | 43.8 |
| Maximum Adult Size (mm) | 55.9 | 71.5 |
| Maximum Longevity (yrs) | ||
| Typical Longevity (yrs |
Reproduction
| Start | Peak | End | |
|---|---|---|---|
| Reproductive Season | |||
| Typical Number of Young Per Reproductive Event |
|||
| Sexuality Mode(s) | |||
| Mode(s) of Asexual Reproduction |
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| Fertilization Type(s) | |||
| More than One Reproduction Event per Year |
|||
| Reproductive Startegy | |||
| Egg/Seed Form |
Impacts
Economic Impacts in Chesapeake Bay
Impacts of Anguillicoloides crassus (Eel Swimbladder Nematode) on Anguilla rostrata (American Eel) populations in the Chesapeake Bay are unknown at present.
Fisheries - Infection rates as high as 90% have been observed in some regions of the Bay (Anonymous 1998). This parasite has caused extensive mortality of cultured Anguilla rostrata (Ooi et al. 1996), and is expected to adversely affect wild populations, particularly in the seaward migration. However, the catadromous life cycle of the eel, and its panmictic spawning makes it difficult to determine the impact of local parasites on Chesapeake Bay Eel fisheries (Barse and Secor 1999).
References- Anonymous 1998; Barse and Secor 1999; Ooi et al. 1996
Economic Impacts Outside of Chesapeake Bay
Fisheries - Anguillicoloides crassus appears to have relatively little impact on its native host, Anguilla japonica (Japanese Eel) , but its introduction to Europe has had severe effects (mortality, decreased growth, reduced swimming speed) on the culture of A. anguilla (European Eels ), raised in ponds from wild-caught elvers (juveniles), and on wild eels as well (Van Banning and Haenan 1990; Koie 1991). Effects on recruitment and population dynamics of wild eels are likely but difficult to determine.
In North America, infected wild A. rostrata (American Eels) are so far known from SC, Chesapeake Bay, and the Hudson River estuary. (Barse and Secor 1998). In addition, high rates of infection and mortality were seen in an inland eel culture facility in TX in 1995 (Fries et al. 1996). Anguillicoloides crassus is expected to have serious impacts on American Eel populations, but these will be difficult to separate from pollution, habitat destruction, and other human-caused environmental changes.
References- Barse and Secor 1998; Fries et al. 1996; Koie 1991; Van Banning and Haenan 1990
Ecological Impacts on Chesapeake Native Species
Anguillicoloides crassus (Eel Swimbladder Nematode) was discovered in the Chesapeake Bay in 1997. The extent of impacts of A. crassus on American Eel (Anguilla rostrata) populations in the Chesapeake Bay are unknown at present.
Parasitism- Infection rates as high as 90% have been observed in some regions of the Bay (Anonymous 1998). This parasite has caused extensive mortality of cultured Anguilla rostrata (Ooi et al. 1996), and is expected to adversely affect wild populations, particularly in seaward migration. However, the catadromous life cycle of the eel, and its panmictic spawning makes it difficult to determine the impact of local parasites on Chesapeake Bay Eel populations (Barse and Secor 1999).
Impacts of Anguillicoloides crassus infection have been most throughly studied in Anguilla anguilla(European Eel) After ingestion of an infected copepod or a paratenic host fish, nematodes move from the digestive tract into the swimbladder, and develop in the swimbladder wall. Mature nematodes move into the swimbladder lumen. Anguillicoloides infection may result in inflammation and connective tissue formation in the swimbladder wall, causing decreased swimbladder function. Infection rates rates were highest in cultured A. anguilla, but significant infection and swimbladder damage was seen in wild eels as well (van Banning and Haenen 1980). Effects of infection were especially severe on elvers (juvenile eels). In heavily infected eels, severe hemorrhaging and secondary bacterial infection resulted in high rates of mortality. Similar effects were seen in farmed Anguilla rostrata, in Taiwan. Aberrant migration of the developing juvenile nematodes, and possibly the lack of an immune response in Anguilla anguilla and Anguilla rostrata seems to contribute to high mortality, which is not seen when A. crassus infects Japanese Eels (A. japonica) (Ooi et al. 1996).
In Anguilla anguilla, high rates of infection of wild fish resulted in a slight decrease in length-weight ratios (Barus and Prokes 1996), decreased oxygen content in swimbladder gas (Wurtz et al. 1996), and decreased swimming speed (Sprengel and Luchetenberg 1991). Such effects, likely to also occur in the Anguilla rostrata, are likely to adversely affect the seaward migration of mature (silver) Anguilla rostrata to their oceanic spawning grounds. However, since the migration route and spawning grounds are imperfectly known, effects of this parasite cannot be separated quantitatively from other human-induced and natural environmental changes.
History References- Anonymous 1998; Barse and Secor 1999; Barus and Prokes 1996; Ooi et al. 1996; Sprengel and Luchetenberg 1991; van Banning and Haenen 1980; Wurtz et al. 1996
Ecological Impacts on Other Chesapeake Non-Native Species
Impacts of Anguillicoloides crassuson exotic biota in the Chesapeake Bay are unknown.
References
Aieta, Amy E.; Oliveira, Kenneth (2009) Distribution, prevalence, and intensity of the swim bladder parasite Anguillicola crassus in New England and eastern Canada, Diseases of Aquatic Organisms 84: 229-235Anonymous (1998) Foreign worms taking bite out of eels in Chesapeake., Bay Journal 8: 3
Barse, Ann M.; McGuire, Scott A.; Vinores, Melissa A.; Eierman, Laura E.; Weeder, Julia A. (2001) The swimbladder nematode Anguillicola crassus in American Eels (Anguilla rostrata) from middle and upper regions of Chesapeake Bay, Journal of Parasitology 87: 1366-1370
Barse, Ann M.; Secor, David H. (1999) An exotic nematode parasite of the American Eel., Fisheries 24: 6-10
Barus, Vlastimil; Prokes, Miroslav (1996) Length-weight relations of uninfected and infected eels (Anguilla anguilla) by Anguillicola crassus (Nematoda)., Folia Zoologica 45: 183-189
De Charleroy, D.; Grisez, L.; Thomas, K.; Belpaire, C.; Ollevier, F. (1990) Life cycle of Anguillicola crassus, Diseases of Aquatic Organisms 8: 77-84
Fenske, Karl H.; Secor, David H; Wilber, Michael J.. (2010) Demographics and parasitism of American Eels in the Chesapeake Bay, USA, Transactions of the American Fisheries Society 139: 1699-1710
Fries, Loraine T.; Williams, D. Jody (1996) Occurrence of Anguillicola crassus, an exotic parasite swim bladder nematode of eels, in the southeastern United States, Transactions of the American Fisheries Society 125: 794-797
Kennedy, C. R.; Fitch, D. J. (1990) Colonization, larval survival, and epidemiology of the nematode Anguillicola crassus, parasitic in the eel, Anguilla anguilla, in Britain, Journal of Fish Biology 36: 117-131
Koie, Marianne (1991) Swimbladder nematodes (Anguillicola spp.) and gill monogeneans (Pseudodactylogyrus spp.) parasitic on the Anguilla anguilla (European eel), Journal de Conseil Internationale d' Exploration de la Mer 47: 391-398
Lefebvre, François; Wielgoss, Sébastien; Nagasawa, Kazuya; Moravec, František (2012) On the origin of Anguillicoloides crassus, the invasive nematode of anguillid eels, Aquatic Invasions 7: in press
Machut, L. S.; Limburg, K. E. (2008) Anguillicola crassus infection in Anguilla rostrata from small tributaries of the Hudson River, New York, USA, Diseases of Aquatic Organisms 79: 37-45
Ooi, Hong-Kean; Wang, Way-Shyan; Chang, Hong-You; Wu, Chwen-Heng; Lin, Cheng-Chung; Hsieh, Meng-Tong (1996) Epizootic of anguillicolosis in cultured American eels in Taiwan, Journal of Aquatic Animal Health 8: 163-166
Sasal, Pierre; Tarazchewski, Horst; Valade, Pierre; Grondin, Henri; Wilegloss, Sebastien; Moravek, Frantisek (2008) Parasitic communities in the eels of the island of Reunion: a lesson in parasitic introduction., Senekenbergiana 102: 1343-1350
Sprengel, G.; Luchtenberg, H. (1991) Infection by endoparasites reduces maximum swimming speed of European smelt Osmerus eperlanus and European eel Anguilla anguilla, Diseases of Aquatic Organisms 11: 31-35
van Banning, P.; Haenen, O. L. M. (1990) Effects of the swimbladder nematode Angiullicola crassus in wild and farmed eel, Anguilla anguilla, , San Diego. Pp. 317-330
Wurtz, Charles B.; Roback, Selwyn S. (1955) Invertebrate fauna of some Gulf coast rivers, Proceedings of the Academy of Natural Sciences of Philadelphia 107: 167-206