Anguillicoloides crassus (Moravec 2006), eel swim bladder nematode

• a small, circular mouth opening surrounded by four dorsolateral and ventrolateral cephalic papillae and two small lateral amphids.
• a single row of 22-28 teeth on the front edge of the buccal capsule.
• a muscular esophagus consisting of three lobes extending towards its posterior region and six slightly elevated, rounded lobes that protrude into the buccal cavity.
• a well-developed valvular apparatus of the esophagus.
• three large, oval rectal glands sometimes with a smaller, ventral rectal gland.

Male and female nematodes are sexually dimorphic. Female nematodes are larger and more robust than males (Taraschewski et al. 1987). Also, female nematodes can be distinguished by a cone-shaped vulva and a white uterus with numerous developing eggs that occupies a large portion of the body (Moravec 1994). Males can be identified by the six pairs of caudal papillae (two praeanals, one or two adanals, and two or three postanals) and a visible seminal vesicle (Taraschewski et al. 1987; de Charleroy et al. 1990; Nagasawa et al. 1994).

HABITAT: Since Anguillicola crassus is a parasitic nematode, the habitat of A. crassus is closely tied to its host. The highest rates of A. crassus infections can be found in freshwater and brackish water bodies (de Charleroy et al. 1989.; Kennedy and Fitch 1990; Kirk et al. 2000a; Jakob et al. 2009; Wysujack et al. 2014). A. crassus eggs and early-stage larvae can survive in saltwater for several weeks, but hatching, survival, and infectivity rates are reduced (de Charleroy et al. 1989; Kennedy and Fitch 1990; Kirk et al. 2000a; Wysujack et al. 2014). Later larval stages and adult A. crassus can be protected from seawater by infecting a host, and A. crassus are believed to survive the long migration to the Sargasso Sea in the swim bladder of adult eels (Kirk et al. 2000b). Temperature can also influence A. crassus larvae (Thomas and Ollevier 1993; Ashworth et al. 1996). Colder water temperatures (<10 °C) reduce larval development and adult survival (Knopf et al. 1998; Moser et al. 2001). Optimal hatching temperatures are between 15-30 °C (Thomas and Ollevier 1993). Consequently, areas of warm water around power plants in Europe have acted as havens for A. crassus in several fish hosts (Höglund and Thomas 1992; Emde et al. 2016). Alternatively, warmer temperatures can reduce A. crassus survival by increasing metabolism and depleting energy stores (Thomas and Ollevier 1993). Additionally, A. crassus larvae survival and infectivity is significantly reduced in water with high pH (9.0; Kennedy and Fitch 1990).

FOOD WEB: Anguillicola crassus is a parasite that feeds on the blood of its host (de Charleroy et al. 1990).

LIFE HISTORY: The life cycle of Anguillicola crassus begins within the swim bladder of its host. Females can contain millions of eggs and will release thousands of eggs into the swim bladder (de Charleroy et al. 1990; Kennedy and Fitch 1990). The first-stage (L₁) larvae develop into second-stage (L₂) larvae while still within their egg capsule (de Charleroy et al. 1990). From the swim bladder, the larvae pass out of the eel’s body through the digestive tract via the swim bladder pneumatic duct (de Charleroy et al. 1990; Moravec et al. 1993; Thomas and Ollevier 1993a). Many L₂ larvae hatch shortly after being exposed to freshwater and can survive in the water column for the next several months (Kennedy and Fitch 1990). Larvae are then ingested by an intermediate (obligate) host (de Charleroy et al. 1990; Moravec et al. 1993). Various copepods and ostracods, totaling over 17 species, have been identified as intermediate hosts for European and Japanese eels in experimental and natural conditions (Moravec and Konecny 1994; Moravec et al. 2005). Only copepods within the Acanthocyclops robustus–americanus–vernalis species complex have been found to be a natural intermediate host within the United States so far (Hubbard et al. 2016). The copepod Cyclops strenuus, a nonindigenous species in the Great Lakes, is also a potential intermediate host for A. crassus (Moravec et al. 1993).

Once ingested by the intermediate host, the larval A. crassus will travel through the digestive tract wall using a larval cephalic tooth and penetrate the haemocoel in several hours (de Charleroy et al. 1990; Morevec et al. 1993). The A. crassus larvae will molt into the third-stage (L₃) inside its new host within 10-12 days (de Charleroy 1989; de Charleroy et al. 1990; Moravec et al. 1993). The L₃ larvae remain alive in its intermediate or paratenic host and can infect all life-stages of its definitive host, eels in the genus Anguilla (de Charleroy et al. 1990, Nimeth et al. 2000). Alternatively, A. crassus can also incorporate paratenic (facultative) hosts should another fish species consume the intermediate host (de Charleroy et al. 1990). At least 30 different fish species along with several amphibian, snail, and insect species that can act as paratenic hosts in Europe (Thomas and Ollevier 1992; Szekely 1994; Moravec and Konecny 1994; Moravec 1996, Szekely 1996; Moravec and Skorikova 1998; Emde and Klimpel 2015). Several European fish (common carp Cyprinus carpio, three-spined stickleback Gasterosteus aculeatus, ruffe Gymnocephalus cernua, rudd Scardinius erythrophthalmus, trench Tinca tinca, round goby Neogobius melanstomus) that A. crassus can infect are nonindingenous to the Great Lakes Basin (de Charleroy et al. 1990; Haenan and van Banning 1990; Szekely 1994; Emde et al. 2014). In the United States, A. crassus L₃ larvae have also been confirmed in several fish species that inhabit in the Great Lakes, such as brown bullhead (Ameriurus nebulosus), pumpkinseed (Lepomis gibbosus), and bluegill (Lepomis macrochirus) (El-Shehabi et al. 2018). After ingestion by the paratenic host, the L₃ larvae  penetrates the fish body cavity where the larvae can survive for around two months (Moravec and Konecny 1994). Certain paratenic hosts, such as cyprinid species, reduce the capability of A. crassus to infect new hosts by encapsulating the larvae as part of an immune response (Moravec and Konecny 1994; Szekely 1996). In other paratenic hosts, such as Perciformes, A. crassus L₃ larvae can develop into a fourth-stage (L₄) larvae (Moravec 1996).

Larger (>50 cm) eels primarily consume fish, and so copepods are not the main food source for older eels (Thomas and Ollevier 1992). As a consequence of this flexible life cycle, smaller, younger eels are typically infected by consuming intermediate hosts while larger, older eels are usually infected by consuming paratenic hosts (Barry et al. 2017). Once the host is consumed by an eel, the A. crassus quickly migrates through the intestinal wall and body cavity of the eel to the swim bladder usually within 17 hours (Haenen et al. 1989; Haenan and van Banning 1990). The L₃ larvae remain in the submucosa of the swim bladder before molting into L₄ larvae (Haenen and de Charleroy 1990). Over the next few months, A. crassus larvae will continue to feed, molt again, and become sexually mature (de Charleroy et al. 1990; Haenen and de Charleroy 1990). Adult nematodes will move into the swim bladder lumen and breed (de Charleroy et al. 1990; Haenen and de Charleroy 1990).

The native eel host, Japanese eels (Anguilla japonica), have higher recovery rates and lower levels of damage after Anguillicola crassus infractions (Keppel et al. 2014). Japanese eels are able to encapsulate Anguillicola crassus larvae, which reduces larvae survival (Knopf and Mahnke 2004). Novel eel hosts, like European eels (Anguilla anguilla) and American eels (Anguilla rostrata), do not seem to have these immune defenses against Anguillicola crassus (Keppel et al. 2014). There is also evidence that American eels might be more susceptible to Anguillicola crassus than European eels (Marohn et al. 2014).

Currie et al. 2020

In Europe, A. crassus is considered an invasive species given its harmful effects on European eels (Anguilla anguilla) and rapid spread outside its native range (Lefebvre et al. 2012). However, there is no data demonstrating that A. crassus is negatively impacting American eels or the St. Lawrence River American eel populations and ecosystem (Pratt et al. 2018). Given the parasite's capability for harm, A. crassus should be considered a potentially invasive species.

Summary of species impacts derived from literature review. Click on an icon to find out more...

Environmental	Socioeconomic

The life cycle of A. crassus involves an intermediate host and/or a paratenic host (Thomas and Ollevier 1992; Moravec and Konecny 1994; Szekely 1994; Moravec 1996; Szekely 1996; Moravec and Skorikova 1998). Eels are infected once they eat the intermediate or paratenic hosts (Barry et al. 2017). A. crassus might increase predation risk for other infected fish species serving as paratenic hosts (Wlsaow et al. 1998; Sjöberg et al. 2009).

Anguillicola crassus has a low socioeconomic impact in the Great Lakes.
European eel farms have seen die-offs, appetite loss, physical deformities, and reduced growth rates from Anguillicola crassus infections, which can reduce economic output (van Banning and Haenan 1990; Køie 1991). Also, European eel catch size has decreased by 75%, and A. crassus is believed to have contributed to this decline (Emde and Klimpel 2015).  However, Great Lakes American eel fisheries were already in serious decline prior to the introduction of this parasite to Lake Ontario.

Anguillicola crassus has a low beneficial impact in the Great Lakes.
There is a potential for Anguillicola crassus to negatively impact the overall health and reproductive success of nonindigenous American eel populations in the upper Great Lakes.

While A. crassus was first described in Japan and East Asia is generally considered its native range, there is not enough data to conclude that A. crassus was not introduced earlier to aquaculture in Japan (Lefebvre 2012). Answering questions about the natural history of A. crassus could help manage the parasitic invader’s spread.

More research is necessary to find the intermediate and paratenic hosts used by A. crasssus and frequently infect American eels (Pratt et al. 2019).