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Anguillicoloides
crassus
Taxonomy
(a) European eel Anguilla anguilla, the
final host of A. crassus
(b) eel swim bladder of A. anguilla
showing a typical number of adult blood-
sucking A. crassus, which can cause
heavy infections and might hamper the
5,000 km long catadromous migration to
the Sargasso Sea.
(c) nematodes in swim bladder (opened
up and well supplied with blood)
(d) third-stage larvae of A. crassus,
isolated from a paratenic fish host
• Adult anguillicoloides are all
strictly parasitic to the eel genus
Anguilla.
• A. crassus is known to infect six
of the 15-20 eel species currently
described worldwide.
Diagnosis of Infection
1. moribund behaviour
2. reduced swimming performance
3. abnormal hanging near the surface
4. body emaciation
5. swollen abdomen
6. Anal redness
Life Cycle Of A.crassus
• The adult, ovoviviparous nematodes are
localized exclusively in the swim bladder of its
final host.
• The Stage L1 already developed in uterus.
• Each female lays several hundreds of thousands
embryonated eggs, containing the second larval
stage (L2)
• The L2 larvae leave the eel via the pneumatic
duct.
• Newly hatched second-stage larvae (L2) attach to
the substratum by their caudal extremity.
• After penetrating the intestinal tract of the first
intermediate host, the nematode develops its
third-stage larva (L3) within a few days.
Life Cycle Of
A.crassus
• different species of fishes, mollusks, insects, and
amphibians can be incorporated in the life cycle of A.
crassus as so-called Paratenic Host.
• Smaller eels get infected predominantly by feeding on
parasitized first intermediate (obligate) hosts, e.g.,
crustaceans.
• larger eels mostly prey on infective paratenic (facultative)
hosts, e.g., fish or amphibians.
• The time to metamorphosis into fourth- stage larvae (L4)
is temperature dependent, and may vary from 2-3 weeks
up to 3 months post-infection.
• After an average of 8–10 months, A. crassus reaches
sexual maturity and the life cycle restarts.
Larvae of A.crassus
• A.crassus L2 larvae
• Surrounded by their egg sheath and L1 cuticle.
• Hatching of L2 larvae from egg
• Paracyclops fimbriatus (intermediate host)
infected with larvae which are visible in the
abdomen
• L3 larvae dissected out of the intermediate host
Paracyclops fimbriatus 10 d after infection with
L2 larvae. Moulting has already taken place.
Sections of L3 larvae (1) in the submucosa of the swim bladder of eel Anguilla anguilla where they
pass during their migration to the swim bladder lumen
• The difference between L3 (1) and
L4 (2) larvae is clearly visible.
• The L4 larvae are considerably
larger and are stained darkly
• Nematode moulting from L4 larva to preadult. The L4 cuticle is
still surrounding the parasite and is visible at the head end of
the parasite (1)
X-ray of experimental eels
• X-ray scans were used to measure
the swim-bladder length (SBL)
• determine the actual swim-bladder
status.
• An eel with a large, uninfected
bladder (top),
• An eel with a medium-sized bladder
with visible parasites (middle)
• An eel with a small bladder with
minimal volume (bottom)
• Dissection of the swim-bladder, whole (top) and cut open
(bottom) showing 19 parasites of various sizes.
• Three levels of swim-bladder wall transparency, -thickness and
length showing a large, thin- walled transparent swim-bladder (top),
a medium-sized swim-bladder with a thicker wall (middle) and a
small thick-walled non-transparent swim- bladder (bottom).
Microphotographic sections of eel swimbladders
• Swimbladder of an uninfected eel, showing the
swimbladder lumen (SBL) and the structure of normal
swimbladder wall (SBW), with its four layers: the
innermost mucosa or epithelium (E), the muscularis
mucosa (M), the submucosa (SM), the serosa (S, the
outermost layer), and blood vessels (arrowheads).
• Section of a damaged swimbladder, showing a
migrating third-stage larva (L3 indicated by arrow),
and the considerable thickening and structural
changes in all four layers.
Histopathological changes in the swimbladder wall of the European
eel
CS = cutting surface,
E = epithelium
Mm = muscularis
mucosae Sm =
submucosa
S = serosa
• Swimbladder wall of an uninfected
swimbladder
• The smooth surface shows only
elevations of the blood vessel
• Swimbladder wall of an infected,
thickened swimbladder.
• The epithelium is characterized by
heavy folds
• blood vessels can only be seen at the
cutting line.
• All layers show thickening.
• Epithelium of an uninfected swimbladder;
• higher magnification reveals short
microvilli on top of the epithelium and
makes cell borders visible.
• Epithelium of an infected swimbladder;
• in thickened swim bladders the surface
shows folds and the cells have a bubble
shaped surface
Blh - basal labyrinth,
Bla = basal lamina,
C = collagen fibres,
Ca = capillary,
F = fibroblast,
Jc - junctional complex,
M = macrophage
Opened swimbladders with different damage degrees
Swimbladders along with the liver (L), gallbladder (GB) and intestine
(I)
(a) Healthy swimbladder showing adult worms inside, and visible
pneumatic duct (PO)
(b) degraded swimbladder showing overall shrinkage, and no worms
inside the few lumen remaining.
• In Germany, eel populations are infected already
from 65% to 90% with A. crassus (Deutscher
Bundestag 2004)
Protective/Control Strategies
• 24 h water bath with Levamisole at 2 mg/l was the most effective procedure. However, larval stages L3 and
L4 in the wall of the swim bladder are not affected by any medication
• Trichlorfon and Diflubenzuron proved to be effective in single-dose application at concentrations (e.g. 0.01-
0.02 mg/l) which are not dangerous to eels
• There is no available vaccine against A. crassus on the market
Bernies, D., Brinker, A., & Daugschies, A. (2011). An invasion record for the swimbladder nematode Anguillicoloides crassus in European eel Anguilla anguilla in a deep cold-
monomictic lake, from invasion to steady state. Journal of Fish Biology, 79(3), 726–746. https://doi.org/10.1111/j.1095-8649.2011.03054.x
De Charleroy, D., Grisez, L., Thomas, K., Belpaire, C., & Ollevier, F. (1990). The life cycle of Anguillicola crassus. Diseases of Aquatic Organisms, 8(May 2014), 77–84.
https://doi.org/10.3354/dao008077
Dissertations, T., & Theses, M. P. (2017). W&M ScholarWorks W&M ScholarWorks Impact of the Parasitic Nematode Anguillicoloides Crassus on Impact of the Parasitic
Nematode Anguillicoloides Crassus on American Eels (Anguilla Rostrata) in Chesapeake Bay American Eels (Anguilla Rostrata) in Chesapeake.
https://doi.org/10.21220/V5HB27
Emde, S., & Klimpel, S. (2016). Encyclopedia of Parasitology. Encyclopedia of Parasitology. https://doi.org/10.1007/978-3-642-27769-6
Innal, D., Ozmen, O., & Genc, E. (2019). Infection of European Eel, Anguilla anguilla with the Nematode Anguillicoloides crassus from Some Estuarine Systems in Turkey. Turkish
Journal of Fisheries and Aquatic Sciences, 19(11), 899–905. https://doi.org/{10.4194/1303-2712-v19_11_01}
Kirk, R. S. (2003). The impact of Anguillicola crassus on European eels. Fisheries Management and Ecology, 10(6), 385–394. https://doi.org/10.1111/j.1365-2400.2003.00355.x
Knopf, K., Madriles Helm, A., Lucius, R., Bleiss, W., & Taraschewski, H. (2008). Migratory response of European eel (Anguilla anguilla) phagocytes to the eel swimbladder
nematode Anguillicola crassus. Parasitology Research, 102(6), 1311–1316. https://doi.org/10.1007/s00436-008-0910-y
Molnar, K. (1994). Formation of parasitic nodules in the swimbladder and intestinal walls of the eel Anguilla anguilla due to infections with larval stages of Anguillicola crassus.
Diseases of Aquatic Organisms, 20(3), 163–170. https://doi.org/10.3354/dao020163
Palstra, A. P., Heppener, D. F. M., van Ginneken, V. J. T., Székely, C., & van den Thillart, G. E. E. J. M. (2007). Swimming performance of silver eels is severely impaired by the
swim-bladder parasite Anguillicola crassus. Journal of Experimental Marine Biology and Ecology, 352(1), 244–256. https://doi.org/10.1016/j.jembe.2007.08.003
Popielarczyk, R., Robak, S., & Siwicki, K. A. (2012). Infection of European eel,Anguilla anguilla (L.), with the nematode Anguillicoloides crassus (Kuwahara, Niimi et Itagaki, 1974)
in Polish waters. Polish Journal of Veterinary Sciences, 15(2), 253–257. https://doi.org/10.2478/V10181-011-0142-4
Thomas, K., & Ollevier, F. (1992). Paratenic hosts of the swimbladder nematode Anguillicola crassus. Diseases of Aquatic Organisms, 13(3), 165–174.
https://doi.org/10.3354/dao013165
Woo, P. T. K., & Buchmann, K. (2011). Fish parasites: Pathobiology and protection. Fish Parasites: Pathobiology and Protection, (December 2011), 1–383.
https://doi.org/10.1079/9781845938062.0000
Würtz, J., & Taraschewski, H. (2000). Histopathological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus.
Diseases of Aquatic Organisms, 39(2), 121–134. https://doi.org/10.3354/dao039121
(Bernies, Brinker, & Daugschies, 2011; De Charleroy, Grisez, Thomas, Belpaire, & Ollevier, 1990; Dissertations & Theses, 2017; Emde & Klimpel, 2016; Innal, Ozmen, & Genc,
2019; Kirk, 2003; Knopf, Madriles Helm, Lucius, Bleiss, & Taraschewski, 2008; Molnar, 1994; Palstra, Heppener, van Ginneken, Székely, & van den Thillart, 2007; Popielarczyk,
Robak, & Siwicki, 2012; Thomas & Ollevier, 1992; Woo & Buchmann, 2011; Würtz & Taraschewski, 2000)
Ref.
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Anguillicoloides crassus

  • 3. (a) European eel Anguilla anguilla, the final host of A. crassus (b) eel swim bladder of A. anguilla showing a typical number of adult blood- sucking A. crassus, which can cause heavy infections and might hamper the 5,000 km long catadromous migration to the Sargasso Sea. (c) nematodes in swim bladder (opened up and well supplied with blood) (d) third-stage larvae of A. crassus, isolated from a paratenic fish host
  • 4. • Adult anguillicoloides are all strictly parasitic to the eel genus Anguilla. • A. crassus is known to infect six of the 15-20 eel species currently described worldwide.
  • 5. Diagnosis of Infection 1. moribund behaviour 2. reduced swimming performance 3. abnormal hanging near the surface 4. body emaciation 5. swollen abdomen 6. Anal redness
  • 6. Life Cycle Of A.crassus • The adult, ovoviviparous nematodes are localized exclusively in the swim bladder of its final host. • The Stage L1 already developed in uterus. • Each female lays several hundreds of thousands embryonated eggs, containing the second larval stage (L2) • The L2 larvae leave the eel via the pneumatic duct. • Newly hatched second-stage larvae (L2) attach to the substratum by their caudal extremity. • After penetrating the intestinal tract of the first intermediate host, the nematode develops its third-stage larva (L3) within a few days.
  • 7. Life Cycle Of A.crassus • different species of fishes, mollusks, insects, and amphibians can be incorporated in the life cycle of A. crassus as so-called Paratenic Host. • Smaller eels get infected predominantly by feeding on parasitized first intermediate (obligate) hosts, e.g., crustaceans. • larger eels mostly prey on infective paratenic (facultative) hosts, e.g., fish or amphibians. • The time to metamorphosis into fourth- stage larvae (L4) is temperature dependent, and may vary from 2-3 weeks up to 3 months post-infection. • After an average of 8–10 months, A. crassus reaches sexual maturity and the life cycle restarts.
  • 8. Larvae of A.crassus • A.crassus L2 larvae • Surrounded by their egg sheath and L1 cuticle. • Hatching of L2 larvae from egg
  • 9. • Paracyclops fimbriatus (intermediate host) infected with larvae which are visible in the abdomen • L3 larvae dissected out of the intermediate host Paracyclops fimbriatus 10 d after infection with L2 larvae. Moulting has already taken place.
  • 10. Sections of L3 larvae (1) in the submucosa of the swim bladder of eel Anguilla anguilla where they pass during their migration to the swim bladder lumen
  • 11. • The difference between L3 (1) and L4 (2) larvae is clearly visible. • The L4 larvae are considerably larger and are stained darkly • Nematode moulting from L4 larva to preadult. The L4 cuticle is still surrounding the parasite and is visible at the head end of the parasite (1)
  • 12. X-ray of experimental eels • X-ray scans were used to measure the swim-bladder length (SBL) • determine the actual swim-bladder status. • An eel with a large, uninfected bladder (top), • An eel with a medium-sized bladder with visible parasites (middle) • An eel with a small bladder with minimal volume (bottom)
  • 13. • Dissection of the swim-bladder, whole (top) and cut open (bottom) showing 19 parasites of various sizes. • Three levels of swim-bladder wall transparency, -thickness and length showing a large, thin- walled transparent swim-bladder (top), a medium-sized swim-bladder with a thicker wall (middle) and a small thick-walled non-transparent swim- bladder (bottom).
  • 14. Microphotographic sections of eel swimbladders • Swimbladder of an uninfected eel, showing the swimbladder lumen (SBL) and the structure of normal swimbladder wall (SBW), with its four layers: the innermost mucosa or epithelium (E), the muscularis mucosa (M), the submucosa (SM), the serosa (S, the outermost layer), and blood vessels (arrowheads). • Section of a damaged swimbladder, showing a migrating third-stage larva (L3 indicated by arrow), and the considerable thickening and structural changes in all four layers.
  • 15. Histopathological changes in the swimbladder wall of the European eel CS = cutting surface, E = epithelium Mm = muscularis mucosae Sm = submucosa S = serosa • Swimbladder wall of an uninfected swimbladder • The smooth surface shows only elevations of the blood vessel • Swimbladder wall of an infected, thickened swimbladder. • The epithelium is characterized by heavy folds • blood vessels can only be seen at the cutting line. • All layers show thickening.
  • 16. • Epithelium of an uninfected swimbladder; • higher magnification reveals short microvilli on top of the epithelium and makes cell borders visible. • Epithelium of an infected swimbladder; • in thickened swim bladders the surface shows folds and the cells have a bubble shaped surface
  • 17. Blh - basal labyrinth, Bla = basal lamina, C = collagen fibres, Ca = capillary, F = fibroblast, Jc - junctional complex, M = macrophage
  • 18. Opened swimbladders with different damage degrees
  • 19. Swimbladders along with the liver (L), gallbladder (GB) and intestine (I) (a) Healthy swimbladder showing adult worms inside, and visible pneumatic duct (PO) (b) degraded swimbladder showing overall shrinkage, and no worms inside the few lumen remaining.
  • 20. • In Germany, eel populations are infected already from 65% to 90% with A. crassus (Deutscher Bundestag 2004)
  • 21. Protective/Control Strategies • 24 h water bath with Levamisole at 2 mg/l was the most effective procedure. However, larval stages L3 and L4 in the wall of the swim bladder are not affected by any medication • Trichlorfon and Diflubenzuron proved to be effective in single-dose application at concentrations (e.g. 0.01- 0.02 mg/l) which are not dangerous to eels • There is no available vaccine against A. crassus on the market
  • 22.
  • 23. Bernies, D., Brinker, A., & Daugschies, A. (2011). An invasion record for the swimbladder nematode Anguillicoloides crassus in European eel Anguilla anguilla in a deep cold- monomictic lake, from invasion to steady state. Journal of Fish Biology, 79(3), 726–746. https://doi.org/10.1111/j.1095-8649.2011.03054.x De Charleroy, D., Grisez, L., Thomas, K., Belpaire, C., & Ollevier, F. (1990). The life cycle of Anguillicola crassus. Diseases of Aquatic Organisms, 8(May 2014), 77–84. https://doi.org/10.3354/dao008077 Dissertations, T., & Theses, M. P. (2017). W&M ScholarWorks W&M ScholarWorks Impact of the Parasitic Nematode Anguillicoloides Crassus on Impact of the Parasitic Nematode Anguillicoloides Crassus on American Eels (Anguilla Rostrata) in Chesapeake Bay American Eels (Anguilla Rostrata) in Chesapeake. https://doi.org/10.21220/V5HB27 Emde, S., & Klimpel, S. (2016). Encyclopedia of Parasitology. Encyclopedia of Parasitology. https://doi.org/10.1007/978-3-642-27769-6 Innal, D., Ozmen, O., & Genc, E. (2019). Infection of European Eel, Anguilla anguilla with the Nematode Anguillicoloides crassus from Some Estuarine Systems in Turkey. Turkish Journal of Fisheries and Aquatic Sciences, 19(11), 899–905. https://doi.org/{10.4194/1303-2712-v19_11_01} Kirk, R. S. (2003). The impact of Anguillicola crassus on European eels. Fisheries Management and Ecology, 10(6), 385–394. https://doi.org/10.1111/j.1365-2400.2003.00355.x Knopf, K., Madriles Helm, A., Lucius, R., Bleiss, W., & Taraschewski, H. (2008). Migratory response of European eel (Anguilla anguilla) phagocytes to the eel swimbladder nematode Anguillicola crassus. Parasitology Research, 102(6), 1311–1316. https://doi.org/10.1007/s00436-008-0910-y Molnar, K. (1994). Formation of parasitic nodules in the swimbladder and intestinal walls of the eel Anguilla anguilla due to infections with larval stages of Anguillicola crassus. Diseases of Aquatic Organisms, 20(3), 163–170. https://doi.org/10.3354/dao020163 Palstra, A. P., Heppener, D. F. M., van Ginneken, V. J. T., Székely, C., & van den Thillart, G. E. E. J. M. (2007). Swimming performance of silver eels is severely impaired by the swim-bladder parasite Anguillicola crassus. Journal of Experimental Marine Biology and Ecology, 352(1), 244–256. https://doi.org/10.1016/j.jembe.2007.08.003 Popielarczyk, R., Robak, S., & Siwicki, K. A. (2012). Infection of European eel,Anguilla anguilla (L.), with the nematode Anguillicoloides crassus (Kuwahara, Niimi et Itagaki, 1974) in Polish waters. Polish Journal of Veterinary Sciences, 15(2), 253–257. https://doi.org/10.2478/V10181-011-0142-4 Thomas, K., & Ollevier, F. (1992). Paratenic hosts of the swimbladder nematode Anguillicola crassus. Diseases of Aquatic Organisms, 13(3), 165–174. https://doi.org/10.3354/dao013165 Woo, P. T. K., & Buchmann, K. (2011). Fish parasites: Pathobiology and protection. Fish Parasites: Pathobiology and Protection, (December 2011), 1–383. https://doi.org/10.1079/9781845938062.0000 Würtz, J., & Taraschewski, H. (2000). Histopathological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus. Diseases of Aquatic Organisms, 39(2), 121–134. https://doi.org/10.3354/dao039121 (Bernies, Brinker, & Daugschies, 2011; De Charleroy, Grisez, Thomas, Belpaire, & Ollevier, 1990; Dissertations & Theses, 2017; Emde & Klimpel, 2016; Innal, Ozmen, & Genc, 2019; Kirk, 2003; Knopf, Madriles Helm, Lucius, Bleiss, & Taraschewski, 2008; Molnar, 1994; Palstra, Heppener, van Ginneken, Székely, & van den Thillart, 2007; Popielarczyk, Robak, & Siwicki, 2012; Thomas & Ollevier, 1992; Woo & Buchmann, 2011; Würtz & Taraschewski, 2000) Ref.