Anguillicola crassus - Swim-bladder nematode

A. crassus is a roundworm native to Southeast Asia ^[2]. This nematode was discovered very late due to the limited impact that this parasite has on its natural host, the Japanese eel Anguilla japonica ^[3]. Because of a lack of juvenile Japanese eels in the early 1970s in Japan, the European eel Anguilla anguilla was introduced there for cultivation ^[4]. Suddenly, the latter eel species started showing all kinds of disease symptoms, which led to the discovery of the massive presence of A. crassus in the fish ^[3]. In 1974, A. crassus was described as a parasitic roundworm that feeds on the blood of the wall of eel’s swim bladders ^[3].

First observation in Belgium

In Belgium, A. crassus was first reported on the 13^th of November 1985, after a sampling of eels released in the Belgian Kleine Nete and Grote Nete. One infected individual was found in a sample of 32 eels. Because the eels originated from the Dutch Lake Grevelingen, this is, strictly speaking, a Dutch observation ^[5]. However, since one of the sampled eels was infected, it is assumed that infected individuals were present among the introduced eels ^[6].

Spreading in Belgium

After the first observation in 1985, the species spread rapidly in Belgium. In the summer of 1986, the parasite already occurred in most rivers around Antwerp and West Flanders ^[7]. In 1987, 34% of the eels in Flemish lakes and rivers were infected with one or more adult A. crassus individuals. Ten years later – in 1995 – this number reached 62.5%; 15 years later 70%. If one also considers the presence of A. crassus larvae in the swim bladder, only one in ten eels is not infected with this parasite ^[6].

Spreading in neighbouring countries

In the spring of 1982, A. crassus was observed for the first time in continental Europe. The roundworm was present in a European eel from the Weser-Ems region in northern Germany ^{[8, 9]}. Shortly after, the parasite rapidly spread across Europe. By 1985, the species was present in Belgium, the Netherlands and France ^[10-12].

Around the 1980s, A. crassus got introduced to Europe via the import of infected eels ^[16] from East Asia, presumably Taiwan ^[4]. These eels were subsequently transported to Europe for consumption ^[16]. Eels for consumption are usually sold alive. The transport water – containing the parasite’s larvae – may end up in rivers. Initially, the parasite could spread via uncontrolled eel introductions. Later, via natural dispersal mechanisms ^[7]. In the end, it was the import of these infected European eels from the Netherlands – to supplement the eel stocks in the Belgian rivers – that introduced A. crassus to Belgian waters ^[7].

Before A. crassus’ arrival to Europe, the European eel had no parasites inside its swim bladder. So, the introduced parasite had the advantage since there was no competition and could spread quickly ^[17].

Once the larvae of this parasite are released into the water, they attach themselves with their tail to the bottom. Once settled, they make twisting movements to get quickly noticed and consumed by their intermediate hosts ^{[14, 18, 19]}. This roundworm infects various species of copepods in Europe. In addition, several other intermediate hosts – via predation of the copepods – may also get infected. These extra hosts are not essential for A. crassus to complete its life cycle. These additional hosts include small fish, snails, amphibians and insects. They enable the larvae to survive longer without losing their infection capability ^[17]. The eel – the final host – can become infected by feeding on the intermediate hosts ^[18]. In the swim bladder of the eels, the larvae become sexually mature ^[18]. Without the eel as a host, the swim-bladder nematode cannot complete its life cycle ^[17].  

The presence of a broad range of micro- (e.g. viruses, bacteria, fungi, protozoa) and macro-parasites (e.g. Platyhelminthes, arthropods, Myxosporea) have a positive effect on the invasive potential of A. crassus in the final host. This is because a physical reaction against infections triggers an antagonistic process, whereby a reaction against, for example, micro-parasites gives the macro-parasites a greater chance of successfully infecting the eel ^[20].

A. crassus can tolerate a wide range of temperatures and salinities. The larvae can survive for several months in low temperatures down to 5°C, even though the species prefers warmer waters. Additionally, this nematode can survive in fresh, brackish and salt water ^{[14, 19]}.

After they leave their host’s body (the eels), A. crassus larvae attach themselves to the bottom, which limits their spread by the currents. Migration of the intermediate hosts plays a major role in this roundworm’s dispersal. In the end, the final host – the European eel – migrates from lakes and rivers to the sea, bridging long distances that allow A. crassus to quickly expand its habitat ^{[13, 17]}.

Humans are one of the major factors responsible for the spread of the parasitic roundworm. Lakes and rivers get frequently stocked with eels from other areas for fishing, and, in addition, cultivated eels get transported between farms ^[17]. The trade of living eels for consumption also plays an important role in this parasite spread: the transport water – that can be infected with A. crassus larvae – may end up in rivers ^[21]. Transport of infected intermediate hosts with the ballast water of ships may also affect the species’ distribution ^[14].

As mentioned earlier, the larvae of this parasite can survive in both high and low water temperatures and salinities. This means that the species thrives in a wide range of environmental conditions and adapts easily to new environments. Ideal conditions for the accelerated completion of the life cycle are high temperatures and low salt concentrations ^{[13, 19]}.

The European eel – as well as the American eel – experiences strong disturbance from infection by A. crassus ^[22-26]. This is in contrast to the Japanese eel (the original host), which appears to be adapted to the occurrence of these parasites in its swim bladder ^[17].

In the case of the European eel, the wall of its swim bladder becomes thicker and its volume smaller in response to the infection. These changes may cause problems during the migration of the eels from fresh to salt water ^[27]. To reproduce, the eels migrate from the rivers towards the Sargasso Sea (NW Atlantic Ocean). Marine and freshwater have different densities. The swim bladder ensures that eels (and many other fishes) can keep their body at the desired depth without having to use energy by swimming. Vertical migrations are complicated by a smaller and dysfunctional swim bladder ^[28]. Higher energy consumption can lead to insufficient energy reserves for the maturation of the sex glands and reproduction. Additionally, an infected swim bladder results in a slower swimming speed. Before the eel begins its journey to the Sargasso Sea, it experiences a metamorphosis ^{[29, 30]}. The eel turns silver and undergoes other functional adaptations to survive the higher pressure in the ocean. The infection by A. crassus can speed up this transformation, which leads to a less silver colouration. In turn, this can lead to a reduced capacity to migrate over long distances and reproduce ^[29]. A. crassus is also responsible for a reduced immune response that can result in a higher sensitivity to other pathogenic diseases ^[31].

Since 2000, only glass eels (juvenile eels with a translucent appearance) get released in Flanders – on the recommendation of the Flemish High Council for River Fishing. (Sub)adult eels are no longer released to reduce the risk of further spreading of A. crassus and other diseases. However, this measure proved to be of little use because glass eels are also vulnerable to the parasite, and the nematode already occurred throughout Belgium since 2000. Furthermore, the swim-bladder nematode can naturally expand its habitat ^[6].

In cultivation environments, infected eels are more sensitive to stress ^[32], have a decreased appetite and suffer from weight loss ^[10]. During hot summers, this can lead to mass extinctions of eels in small farms. Additionally, higher water temperatures are ideal for A. crassus, which can spread even more rapidly ^[17]. The most effective treatment against this parasite in farms is using an antibiotic, namely L-levamisole, which has a paralyzing effect on the nematodes. However, in North America, this antibiotic is no longer available, which means that alternatives have to be explored. A 2012 study suggested using Benzoic acid (Emamectin benzoate) as an alternative to L-levamisole for the treatment of the American eel ^[33].

Furthermore, attempts are being made to maintain the population of intermediate hosts – the copepods – and the accumulated organic matter in the farms at a low level. This would reduce the chances of survival of A. crassus. The use of chemical products such as diflubenzuron (DFB) is not recommended. This treatment must be repeated weekly to be effective and is not environmentally friendly ^[34].

The rate of infection among European eels currently appears to be stabilising. Eels with a thickened swim bladder wall are less susceptible to new infections. Encapsulated larvae are also increasingly found in the swim bladder; these develop less quickly into adult nematodes ^{[6, 7]}.

Adult A. crassus only appear in the swim bladder of eels and are removed – along with the swim bladder – when cleaning the eel. Therefore, there are no expected adverse effects for humans when consuming eels or eel-derived products ^[10].

Mating of A. crassus occurs within the swim bladder. The female can lay up to 500,000 eggs. Once the larvae have hatched, they move to the open water via a connecting tube between the swim bladder and the intestine. The larvae attach themselves to the bottom and get eaten by the parasite’s intermediate host (copepods). Subsequently, the eel gets infected via consumption of this intermediate host or another organism that has previously fed on the copepods (e.g. fish, snails, amphibians or insects). After consumption by the eel, the parasites move through the intestinal wall into the swim bladder. The infection of the eel’s swim bladder is essential for A. crassus to complete its life cycle ^{[18, 34]}.

A. crassus individuals are dark brown due to the blood they consume. They have a round head and a pointed tail. They roll themselves up into two or three coils. When looking at a swim bladder of an infected eel, the parasites are noticeable as dark nodes ^[10]. The male nematode is 3.5 centimetres long, while the female individuals can be on average twice as long (7 centimetres). The different sexes also have different widths: a male individual is about 2 millimetres wide, the female measures around 5 millimetres ^{[3, 10]}.

A. crassus individuals have a lifespan of 8 to 10 months and occur in fresh, brackish and salt water. However, the survival rate of the larvae is lower in seawater than in water with a lower salinity ^[13].

[1]          World Register of Marine Species (WoRMS) (2024). Anguillicola crassus Kuwahara, Niimi & Itagaki, 1974 [https://www.marinespecies.org/aphia.php?p=taxdetails&id=122885] (2024-10-18).

[2]          Didziulis, V. (2006). NOBANIS – Invasive Alien Species Fact Sheet – Anguillicola crassus. NOBANIS - North European and Baltic Network on Invasive Alien Species: [s.l.]. 9 pp. [http://www.vliz.be/en/imis?module=ref&refid=209254]

[3]          Kuwahara, A.; Niimi, A.; Itagaki, H. (1974). Studies of a nematode parasitic in the air bladder of the eel: 1. Description of Anguillicola crassus n. sp. (Philometridae, Anguillicolidae). Jap. J. Parasit. 23(5): 275-279. [http://www.vliz.be/en/imis?module=ref&refid=123781]

[4]          Køie, M. (1991). Swimbladder nematodes (Anguillicola spp.) and gill monogeneans (Pseudodactylogyrus spp.) parasitic on the european eel (Anguilla anguilla). J. Cons. - Cons. Int. Explor. Mer 47(3): 391-398. [http://www.vliz.be/en/imis?module=ref&refid=135845]

[5]          Belpaire, C.; De Charleroy, D. (Ed.) (1985). Onderzoek naar de gezondheidstoestand van vissen bestemd voor uitzetting. Laboratorium voor Ekologie en Faunabeheer: Leuven. 32 pp. [http://www.vliz.be/en/imis?module=ref&refid=195126]

[6]          Audenaert, V.; Huyse, T.; Goemans, G.; Belpaire, C.; Volckaert, F.A.M. (2003). Spatio-temporal dynamics of the parasitic nematode Anguillicola crassus in Flanders, Belgium. Dis. Aquat. Org. 56(3): 223-233. [http://www.vliz.be/en/imis?module=ref&refid=67870]

[7]          Belpaire, C.; De Charleroy, D.; Thomas, K.; Van Damme, P.; Ollevier, F. (1989). Effects of eel restocking on the distribution of the swimbladder nematode Anguillicola crassus in Flanders, Belgium. J. Appl. Ichthyol./Z. Angew. Ichthyol. 5(3): 151-153. [www.vliz.be/en/imis?module=ref&refid=123657]

[8]          Neumann, W. (1985). Schwimmblasenparasit Anguillicola bei Aalen. Fisch.Teichwirt 11: 322-322. [http://www.vliz.be/en/imis?module=ref&refid=206432]

[9]          Peters, G.; Hartmann, F. (1986). Anguillicola, a parasitic nematode of the swim bladder spreading among eel populations in Europe. Dis. Aquat. Org. 1: 229-230. [http://www.vliz.be/en/imis?module=ref&refid=125981]

[10]        Van Banning, P.; Heermans, W.; Van Willigen, J.A. (1985). Anguillicola crassa, een nieuwe aalparasiet in de Nederlandse wateren. Visserij ('s-Gravenhage) 38(6-7): 237-240. [http://www.vliz.be/en/imis?module=ref&refid=123622]

[11]        Dupont, F.; Petter, A.J. (1988). Anguillicola, une épizootie plurispécifique en Europe: apparition de Anguillicola crassa (Nematoda, Anguillicolidae) chez l’anguille européenne Anguilla anguilla en Camargue, Sud de la France. Bull. Fr. Pêche Piscic. 308: 38-41. [http://www.vliz.be/en/imis?module=ref&refid=125091]

[12]        Lefebvre, F.S.; Crivelli, A.J. (2004). Anguillicolosis: dynamics of the infection over two decades. Dis. Aquat. Org. 62(3): 227-232. [http://www.vliz.be/en/imis?module=ref&refid=125989]

[13]        Kennedy, C.R.; Fitch, D.J. (1990). Colonization, larval survival and epidemiology of the nematode Anguillicola crassus, parasitic in the eel in Britain. J. Fish Biol. 36: 117-131. [http://www.vliz.be/en/imis?module=ref&refid=123776]

[14]        DAISIE (Delivering Alien Invasive Species Inventories for Europe) (2009). Handbook of alien species in Europe. Invading Nature - Springer Series in Invasion Ecology, 3. Springer: Dordrecht, The Netherlands. ISBN 978-1-4020-8279-5. xxviii, 399 pp. [http://www.vliz.be/en/imis?module=ref&refid=134923]

[15]        Koyuncu, E.; Kaya, D.; Özer, S.; Bariş, M.; Genc, E. (2017). Infection status of Anguillicoloides crassus in wild European eels (Anguilla anguilla) from four rivers of the northeast Mediterranean Region, Turkey. Acta Biologica Turcica = Türk Bioloji Dergisi 30(4): 152-156. [http://www.vliz.be/nl/catalogus?module=ref&refid=312294]

[16]        Höglund, J.; Thomas, K. (1992). The black goby Gobius niger as a potential paratenic host for the parasitic nematode Anguillicola crassus in a thermal effluent of the Baltic. Dis. Aquat. Org. 13(3): 175-180. [http://www.vliz.be/en/imis?module=ref&refid=135885]

[17]        Kennedy, C.R. (2007). The pathogenic helminth parasites of eels. J. Fish Dis. 30(6): 319-334. [http://www.vliz.be/en/imis?module=ref&refid=125671]

[18]        De Charleroy, D.; Grisez, L.; Thomas, K.; Belpaire, C.; Ollevier, F. (1990). The life cycle of Anguillicola crassus. Dis. Aquat. Org. 8: 77-84. [http://www.vliz.be/en/imis?module=ref&refid=3074]

[19]        Thomas, K.; Ollevier, F. (1993). Hatching, survival, activity and penetration efficiency of second-stage larvae of Anguillicola crassus (Nematoda). Parasitology 107: 211-217. [http://www.vliz.be/en/imis?module=ref&refid=2788]

[20]        Martínez-Carrasco, C.; Serrano, E.; Ruiz de Ybáñez, R.; Peñalver, J.; García, J.A.; A., G.-A.; Morand, S.; Muñoz, P. (2011). The European eel—the swim bladder–nematode system provides a new view of the invasion paradox. Parasitol Res. 108(6): 1501-1506. [http://www.vliz.be/nl/catalogus?module=ref&refid=296681]

[21]        Belpaire, C. (2011). Persoonlijke mededeling

[22]        Barry, J.; McLeish, J.; Dodd, J.A.; Turnbull, J.F.; Boylan, P.; Adams, C.E. (2014). Introduced parasite Anguillicola crassus infection significantly impedes swim bladder function in the European eel Anguilla anguilla (L.). J. Fish Dis. 37(10): 921-924. [http://www.vliz.be/nl/catalogus?module=ref&refid=312295]

[23]        Barry, J.; Newton, M.; Dodd, J.A.; Evans, D.; Newton, J.; Adams, C.E. (2017). The effect of foraging and ontogeny on the prevalence and intensity of the invasive parasite Anguillicola crassus in the European eel Anguilla anguilla. J. Fish Dis. 40(9): 1213-1222. [http://www.vliz.be/nl/catalogus?module=ref&refid=312296]

[24]        Jakob, E.; Walter, T.; Hanel, R. (2016). A checklist of the protozoan and metazoan parasites of European eel (Anguilla anguilla): checklist of Anguilla anguilla parasites. J. Appl. Ichthyol. 32(4): 757-804. [http://www.vliz.be/nl/catalogus?module=ref&refid=312297]

[25]        Schneebauer, G.; Hanel, R.; Pelster, B. (2016). Anguillicola crassus impairs the silvering-related enhancements of the ROS defense capacity in swimbladder tissue of the European eel (Anguilla anguilla). J. Comp. Physiol. (B Biochem. Syst. Environ. Physiol.) 186(7): 867-877. [http://www.vliz.be/nl/catalogus?module=ref&refid=312298]

[26]        Weclawski, U.; Heitlinger, E.G.; Baust, T.; Klar, B.; Petney, T.; Han, Y.S.; Taraschewski, H. (2013). Evolutionary divergence of the swim bladder nematode Anguillicola crassus after colonization of a novel host, Anguilla anguilla. BMC Evol. Biol. 13(1): 78. [http://www.vliz.be/nl/catalogus?module=ref&refid=312299]

[27]        Kelly, C.E.; Kennedy, C.R.; Brown, J.A. (2000). Physiological status of wild European eels (Anguilla anguilla) infected with the parasitic nematode, Anguillicola crassus. Parasitology 120(2): 195-202. [http://www.vliz.be/en/imis?module=ref&refid=123778]

[28]        Wysujack, K.; Dorow, M.; Ubl, C. (2014). The infection of the European eel with the parasitic nematode Anguillicoloides crassus in inland and coastal waters of northern Germany. J. Coast. Conserv. 18(2): 121-130. [http://www.vliz.be/nl/catalogus?module=ref&refid=296683]

[29]        Fazio, G.; Sasal, P.; Mouahid, G.; Lecomte-Finiger, R.; Moné, H. (2012). Swim bladder nematodes (Anguillicoloides crassus) disturb silvering in European eels (Anguilla anguilla). J. Parasitol. 98(4): 695-705. [http://www.vliz.be/nl/catalogus?module=ref&refid=296684]

[30]        van Ginneken, V.; Ballieux, B.; Willemze, R.; Coldenhoff, K.; Lenjes, E.; Antonissen, E.; Haenen, O.; Van Den Thillart, G. (2005). Hematology patterns of migrating European eels and the role of EVEX virus. Comp. Biochem. Physiol., Part C Pharmacol. Toxicol. Endocrinol. 140(1): 97-102. [http://www.vliz.be/nl/catalogus?module=ref&refid=99667]

[31]        Terech-Majewska, E.; Schulz, P.; Siwicki, A.K. (2015). Experimental immunology influence of nematode Anguillicoloides crassus infestation on the cellular and humoral innate immunity in European eel (Anguilla anguilla L.). Central European Journal of Immunology 40(2): 127-131. [http://www.vliz.be/nl/catalogus?module=ref&refid=312300]

[32]        Dekker, W.; Van Willigen, J.A. (1988). Abundance of Anguillicola crassa in Dutch outdoor waters and the reaction of its host Anguilla anguilla. CM Documents - ICES. C.M. 1988(M:13). ICES: Copenhagen. 1-6 pp. [http://www.vliz.be/en/imis?module=ref&refid=31465]

[33]        Larrat, S.; Marvin, J.; Lair, S. (2012). Safety and efficacy of emamectin benzoate to treat Anguillicoloides crassus (Kuwahara, Niimi & Itagaki) infections in American eels, Anguilla rostrata (Lesueur). J. Fish Dis. 35(6): 497-470. [http://www.vliz.be/nl/catalogus?module=ref&refid=296685]

[34]        Kamstra, A. (1990). Anguillicola in Dutch Eelfarms: current state. Int. Revue ges. Hydrobiol. 75(6): 897-874. [http://www.vliz.be/en/imis?module=ref&refid=123821]