Habitat-specific variations in Anguillicola crassus infection in the European eel (Anguilla anguilla) from Lake Shkodra and Karavasta Lagoon, Albania

Abstract

The European eel (Anguilla anguilla) faces numerous threats, both human-induced and ecological, which have led to a decline in its population. Among these threats, the nematode Anguillicola crassus impacts the swim bladder of the European eel, complicating its migration to breeding grounds.The current study compares the biometric parameters and the parasitic infestation situation with A. crassus in two of the most important eel fishing habitats in Albania. The transboundary Lake Shkodra/Skadar (freshwater lake) and Karavasta Lagoon (brackish water lagoon). A total of 297 silver-stage eels were sampled between December 2024 (141 from Lake Shkodra and 156 from Karavasta Lagoon). For each site, biometric data were measured and sagittal otoliths were extracted for age estimation. The prevalence was assessed through macroscopic examination of the swim bladder, while traditional epidemiological metrics such as prevalence, mean intensity, and mean abundance were evaluated. Eels sampled in Lake Shkodra tested positive for A. crassus, with a prevalence rate of 36.9%. Younger individuals and males had the highest prevalence. At older ages, the intensity of the infection decreased. No infected eels were detected among the 156 specimens sampled in the Karavasta Lagoon. These results demonstrate habitat-specific variation in A. crassus infection and suggest environmental effects on parasite prevalence. The lack of infection in the Karavasta Lagoon questions its importance as a refuge for eels. More work is needed to investigate these ecological variations and their long-term effects on eel populations and conservation measures.

Keywords

• European eel
• Anguillicola crassus
• swim bladder

References

1. Abdalhamid AH, Ramadan AA, Mohamed E, Sayed MA, Elawad AN. 2018. Study of some ecological and biological parameters on European eel Anguilla anguilla in Umm Hufayan brackish lagoon, Eastern Libya Mediterranean Sea. Bull Inst Sci Rabat. 40:23-30.
2. Acou A, Laffaille P, Legault A, Feunteun E. 2008. Migration pattern of silver eel (Anguilla anguilla, L.) in an obstructed river system. Ecol Freshw Fish. 17(3):432-442.
3. Arai T. 2014. Do we protect freshwater eels or do we drive them to extinction? SpringerPlus. 3(1):534.
4. Arai T. 2016. Biology and ecology of anguillid eels. CRC Press, Boca Raton, FL, USA.
5. Bagenal TB, Tesch FW. 1978. Age and growth. In: Bagenal T, editor. Methods for Assessment of Fish Production in Fresh Waters. IBP Handbook No. 3, 3rd edn. Blackwell Sci Publ. p. 101-136.
6. Barry J, Newton M, Dodd JA, Evans D, Newton J, Adams CE. 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.
7. Bevacqua D, Melià P, Gatto M, De Leo GA. 2015. A global viability assessment of the European eel. Glob Change Biol. 21(9):3323-3335.
8. Bush AO, Lafferty KD, Lotz JM, Shostak AW. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol. 83:575–583.

9. Cakić PD, Stojanovski S, Kulišić Z, Hristovski N, Lenhardt MB. 2002. Occurrence of Anguillicola crassus, ematoda: Dracunculoidea, in eels of lake Ohrid, Macedonia. Acta Vet. 52(2-3):163-168.
10. Dekker W. 2004. Slipping through our hands—population dynamics of the European eel. PhD thesis, University of Amsterdam. 186 pp. http://www.diadfish.org/doc/these_2004/dekker_thesis_eel.pdf
11. Dekker W, Beaulaton L. 2016. Climbing back up what slippery slope? Dynamics of the European eel stock and its management in historical perspective. ICES J Mar Sci. 73(1):5-13.
12. Dekker W. 2003. Status of the European eel stock and fisheries. In: Eel biology. Tokyo: Springer Japan. p. 237–254.
13. Drouineau H, Durif C, Castonguay M, Mateo M, Rochard E, Verreault G, Lambert P. 2018. Freshwater eels: A symbol of the effects of global change. Fish Fish. 19(5):903-930.
14. Durif C, Guibert A, Elie P. 2009. Morphological discrimination of the silvering stages of the European eel. Am Fish Soc Symp. 58:103-111.
15. Fazio G, Sasal P, Lecomte-Finiger R, Da Silva C, Fumet B, Moné H. 2008. Macroparasite communities in European eels, Anguilla anguilla, from French Mediterranean lagoons, with special reference to the invasive species Anguillicola crassus and Pseudodactylogyrus spp. Knowl Manag Aquat Ecosyst. 390-391:06.
16. Geeraerts C, Belpaire C. 2010. The effects of contaminants in European eel: a review. Ecotoxicology. 19(2):239-266.
17. Giari L, Castaldelli G, Gavioli A, Lanzoni M, Fano EA. 2021. Long-term ecological analysis of Anguillicola crassus occurrence and impact on the European eel population in a Mediterranean lagoon (North Italy). Estuar Coast Shelf Sci. 249:107117.
18. Glamuzina L, Pećarević M, Dobroslavić T, Tomšić S, Glamuzina B. 2022. The study of European eel, Anguilla anguilla in the River Neretva estuary (Eastern Adriatic Sea, Croatia) using traditional fishery gear. Acta Adriat. 63(1):35-44.
19. Hart TJ. 1948. The distribution and biology of hake. Biol Rev. 23(1):62-80.
20. Hartmann F. 1994. Untersuchungen zur Biologie, Epidemiologie und Schadwirkung von Anguillicola crassus Kuwahara, Niimi and ltagahi 1974 (Nematoda), einem blutsaugenden Parasiten in der Schwimmblase des Europaischen Aals (Anguilla anguilla). Shaker Verlag, Aachen. p.1-139.
21. ICES. 2009. Workshop on Age Reading of European and American Eel (WKAREA), 20–24 April 2009, Bordeaux, France. ICES CM 2009/ACOM: 48. 66 pp.
22. Imsland AK, Folkvord A, Grung GL, Stefansson SO, Taranger GL. 1997. Sexual dimorphism in growth and maturation of turbot, Scophthalmus maximus (Rafinesque, 1810). Aquac Res. 28(2):101-114.
23. Jakob E, Hanel R, Klimpel S, Zumholz K. 2009. Salinity dependence of parasite infestation in the European eel Anguilla anguilla in northern Germany. ICES J Mar Sci. 66:358–366.
24. Kirk RS. 2003. The impact of Anguillicola crassus on European eels. Fish Manag Ecol. 10(6):385–394.
25. Kirk RS, Kennedy CR, Lewis JW. 2000a. Effect of salinity on hatching, survival and infectivity of Anguillicola crassus (Nematoda: Dracunculoidea) larvae. Dis Aquat Org. 40:211–218.
26. Kirk RS, Lewis JW, Kennedy CR. 2000b. Survival and transmission of Anguillicola crassus Kuwahara, Niimi and Itagaki, 1974 (Nematoda) in seawater eels. Parasitol. 120:289–295. doi:10.1017/S0031182099005399
27. Knopf K. 2006. The swimbladder nematode Anguillicola crassus in the European eel Anguilla anguilla and the Japanese eel Anguilla japonica: differences in susceptibility and immunity between a recently colonised host and the original host. J Helminthol. 80(2):129-136.
28. Koto R, Hoxha L, Bani A. 2022. Analysis of water quality, heavy metals and nutrient of Karavasta lagoon using GIS assessment of ecological risk. J Hyg Eng Des. 41:[page numbers missing].
29. Kuwahara A, Niimi A, Itagaki H. 1974. Studies on a nematode parasitic in the air bladder of the eel. I. Description of Anguillicola crassa n. sp. (Philometridea, Anguillicolidae). Jpn J Parasitol. 23(5):275-279.
30. Lefebvre F, Contournet P, Crivelli AJ. 2007. Interaction between the severity of the infection by the nematode Anguillicola crassus and the tolerance to hypoxia in the European eel Anguilla anguilla. Acta Parasitol. 52(2):171-175.
31. Loukili A, Belghyti D. 2007. The dynamics of the nematode Anguillicola crassus, Kuvahara 1974 in eel Anguilla anguilla (L. 1758) in the Sebou estuary (Morocco). Parasitol Res. 100:683–686.
32. Macnamara R, Koutrakis ET, Sapounidis A, Lachouvaris D, Arapoglou F, Panora D, McCarthy KT. 2014. Reproductive potential of silver European eels (Anguilla anguilla) migrating from Vistonis Lake (northern Aegean Sea, Greece). Mediterr Mar Sci. [pages missing].
33. MARD URDHËR. Nr. 536. 2019. Për Miratimin e Planit të Menaxhimit të Ngjalës Evropiane (Anguilla anguilla) në Shqipëri për Periudhën 2019-2024.
34. Molnár K, Székely C, Baska F. 1993. Pathological and histopathological studies of the swim bladder of eels Anguilla anguilla infected by Anguillicola crassus. Dis Aquat Org. 15(1):41–50.
35. Moravec F. 2004. Nematodes of freshwater fishes of the Neotropical region. Academia. Moriarty C. 1973. A technique for examining eel otoliths. J Fish Biol. 5(2):183–184.
36. Mrdak D, Petrovic D, Katnic A, Erceg M. 2011. Integrated study to support the designation of the transboundary Lake Skadar/Shkodra as biosphere reserve in the frame of the project “Supporting the proposed Transboundary Biosphere Reserve of Lake Skadar/Shkodra area through a participatory approach”. Univ Montenegro, Fac Sci Math, Podgorica. p.9.
37. Paggi L, Orecchia P, Minervini R, Mattiucci S. 1982. Appearance of Anguillicola australiensis Johnston and Mawson, 1940 (Dracuncoloidea: Anguillicolidae) in Anguilla anguilla of Lake Bracciano. Parassitologia. 24(2-3):139-144.
38. Palstra AP, Heppener DFM, van Ginneken VJT, Székely C, van den Thillart GEEJM. 2007. Swimming performance of silver eels is severely impaired by the swim‐bladder parasite Anguillicola crassus. J Exp Mar Biol Ecol. 352(1):244–256. doi:10.1016/j.jembe.2007.08.003
39. Palstra AP, van den Thillart GEEJM. 2010. Swimming physiology of European silver eels (Anguilla anguilla L.): energetic costs and effects on sexual maturation and reproduction. Fish Physiol Biochem. 36(3):297–322. doi:10.1007/s10695-010-9397-4
40. Pelster B. 2015. Swimbladder function and the spawning migration of the European eel Anguilla anguilla. Front Physiol. 5:486. doi:10.3389/fphys.2014.00486
41. Pešić V, Karaman GS, Kostianoy AG, Vukašinović-Pešić V. 2018. The Skadar/Shkodra Lake Environment. p.25. Pike C, Crook V, Gollock M. 2023. Anguilla anguilla (Europe assessment). The IUCN Red List of Threatened Species.
42. Here are your references, formatted according to your provided model: QGIS Development Team. 2025. QGIS Geographic Information System (Version 3.42). Open Source Geospatial Foundation. https://www.qgis.org
43. R Core Team. 2023. R: A Language and Environment for Statistical Computing. Version 4.3.1. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
44. Ragias V, Kalfa A. 1997. Occurrence of the parasitic nematode Anguillicola crassus, Kuwahara, in natural and farmed population of the eel Anguilla anguilla in northern Greece.
45. Kantzoura V, Sapounidis A, Kouam MK, Kolygas MN, Krey G, Koutrakis E. 2021. Anguillicola (Anguillicoides) crassus: Morphometric characteristics and pathogenicity in eels (Anguilla anguilla) in Greece. Vet Parasitol Reg Stud Rep. 25:100586.
46. Simon J. 2015. Age and growth of European eels (Anguilla anguilla) in the Elbe River system in Germany. Fish Res. 164:278-285.
47. Simon J, Fladung E, Arlt E, Witkowski J, Hennicke M, Weichler F. 2023. Wissenschaftliche Vorbereitung, Begleitung und Bewertung von Aalbesatzmaßnahmen im Brandenburger Einzugsgebiet der Elbe und Weiterentwicklung der Managementpläne. Projektabschlussbericht im Auftrag des Landesamtes für Ländliche Entwicklung, Landwirtschaft und Flurneuordnung, Referat L4, Tierzucht und Fischerei, Frankfurt/Oder, 138 S.
48. Sonne C, Peng WX, Alstrup AK, Lam SS. 2021. European eel population at risk of collapse. Science. 372(6548):1271.
49. Székely C, Palstra A, Molnár K, van den Thillart G. 2009. Impact of the Swim‐Bladder Parasite on the Health and Performance of European Eels. In: van den Thillart G, Dufour S, Rankin JC, editors. Spawning Migration of the European Eel. Fish and Fisheries Series, Vol. 30. Springer. [chapter]. doi:10.1007/978-1-4020-9095-0_9
50. Taraschewski H. 2006. Hosts and parasites as aliens. J Helminthol. 80(2):99–128.
51. Tesch FW. 2003. The eel. Blackwell Science. 408 pp.
52. Tesch FW, White RJ. 2003. The eel. Vol. 15. Oxford: Blackwell Science.
53. Vøllestad LA, Jonsson B, Hvidsten NA, Næsje TF, Haraldstad Ø, Ruud-Hansen J. 1986. Environmental factors regulating the seaward migration of European silver eels (Anguilla anguilla). Can J Fish Aquat Sci. 43(10):1909-1916.
54. Würtz J, Taraschewski H, Pelster B. 1996. Changes in gas composition in the swim bladder caused by the nematode Anguillicola crassus. Dis Aquat Org. 27(2):121–128.