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The European Eel Anguilla anguilla (Anguillidae) Invasion by the Allochthone Nematode Anguillicoloïdes crassus in Southern Mediterranean

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Abstract

For the first time, the spreading of a fearsome non-native parasite nematode Anguillicoloïdes crassus is studied in European Eel Anguilla anguilla in 4 different coastal ecosystems throughout 12 years. We found that the parasite become more abundant with time in each study site; only 4.8% of eels inhabited brackish water (Mellah Lagoon) are infected while—over the third of fish are infected in the other waterbodies parasite nematode is presented in fish of all ages as well as of both sex; however infected specimens are less common among juveniles and males Based on the evaluation of the swimbladder degenerative index, we found that swimbladder is damaged in more than a half of fish captured in freshwater, however the opposite situation is observed in the brackish water.There is a significant difference in age, length, weight and condition between infected and uninfected fish.

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REFERENCES

  1. Belpaire, C., Pujolar, J.M., Geeraerts, C. and Maes, G.E., Contaminants in eels and their role in the collapse of the eel stocks, in Biology and Ecology of Anguillid Eels, Arai, T., Ed., Florida: Boca Raton, 2016.

  2. Boon, J.H., Cannaerts, V.M.H., Augustijn, H., et al., The effect of different infection levels with infective larvae of Anguillicola crassus on haematological parameters of European eel (Anguilla anguilla), Aquaculture, 1990, vol. 87, pp. 243−253. https://doi.org/10.1016/0044-8486(90)

    Article  Google Scholar 

  3. Bornarel, V., Lambert, P, Briand, C., et al., Modelling the recruitment of European eel (Anguilla anguilla) throughout its European range, ICES J. Mar. Sci., 2017, vol. 75, pp. 541−552. https://doi.org/10.1093/icesjms/fsx180.90062-R

    Article  Google Scholar 

  4. Boudjadi, Z., Tahri, M., Djebari, N., et al., Etude de l’infestation des anguilles (Anguilla anguilla) par le nématode (Anguillicola crassus) dans l’estuaire du Mafrag (Algérie), Mésogée, 2009, vol. 65, pp. 5966.

    Google Scholar 

  5. Bush, A.O., Lafferty, K.D., Lotz, J.M. and Shostak, A.W., Parasitology meets ecology on its own terms: Margolis et al. revisited, J. Parasitol., 1997, vol. 83, pp. 575−583.

    Article  CAS  PubMed  Google Scholar 

  6. Byer, J.D., Lebeuf, M., Trottier, S., et al., Trends of persistent organic pollutants in American eel (Anguilla rostrata) from eastern Lake Ontario, Canada, and their potential effects on recruitment, Sci. Total Environ., 2015, vol. 529, pp. 231−242. https://doi.org/10.1016/j.scitotenv.2015.05.054

    Article  CAS  PubMed  Google Scholar 

  7. Castonguay, M., Hodson, P.V., Moriarty, C., et al., Is there a role of ocean environment in American and European eel decline? Fish Oceanogr., 1994a, vol. 3, pp. 197−203.

    Article  Google Scholar 

  8. Castonguay, M., Hodson, P.V., Couillard, C.M., et al., Why is recruitment of the American eel, Anguilla rostrata, declining in the St. Lawrence River and Gulf?, Can. J. Fish Aquat. Sci., 1994b, vol. 51, pp. 479−488.

    Article  Google Scholar 

  9. Dekker, W., Status of the European eel stock and fisheries, in Eel Biology, Aida, K., Eds., Tokyo: Springer-Verlag, 2003. https://doi.org/10.1007/978-4-431-65907-5_17

    Book  Google Scholar 

  10. Dekker, W. and Casselman, J.M., The Québec Declaration of Concern about eel declines−11 years later: Are eels climbing back up the slippery slope?, Fisheries, 2014, vol. 39, pp. 613−614. https://doi.org/10.1080/03632415.2014.979342

    Article  Google Scholar 

  11. Dekker, W., Casselman, J.M., Cairns, D.K., et al., Québec Declaration of Concern: Worldwide decline of eel resources necessitates immediate action, Fisheries, 2003, vol. 28, no. 12, pp. 28−30. https://edepot.wur.nl/40989

    Google Scholar 

  12. Dhaouadi, R., Sghaier, A., Aloui, N., et al., Etude de l’infestation de l’anguille européenne, Anguilla anguilla, par le nématode Anguillicoloides crassus dans la lagune de Ghar El Melh (Nord de la Tunisie), Mar. Life, 2014, vol. 18, pp. 17−24.

    Google Scholar 

  13. Diekmann, M., Simon, J. and Salva, J., On the actual recruitment of European eel (Anguilla anguilla) in the River Ems, Germany, Fish. Manag. Ecol., 2019, vol. 26, pp. 20−30. https://doi.org/10.1111/fme.12314

    Article  Google Scholar 

  14. Drouineau, H., Durif, C., Castonguay, M., et al., Freshwater eels: A symbol of the effects of global change, Fish Fish., 2018, vol. 19, pp. 903−930. https://doi.org/10.1111/faf.12300

    Article  Google Scholar 

  15. EELREP, Estimation of the reproduction capacity of European eel, Final report, EU contract Q5RS-2001–01836, Leiden : Leiden Univ., 2005. http://www.fishbiology.net/eelrepsum.html

  16. Fazio, G., Moné, H., Da Silva, C., et al., Changes in gene expression in European eels (Anguilla anguilla) induced by infection with swim bladder nematodes (Anguillicola crassus), J. Parasitol., 2009, vol. 95, pp. 808−816. https://doi.org/10.1645/GE-1705.1

    Article  CAS  PubMed  Google Scholar 

  17. Feunteun, E., Management and restoration of European eel population (Anguilla anguilla): An impossible bargain, Ecol. Eng., 2002, vol. 18, pp. 575−591. https://doi.org/10.1016/S0925-8574(02)00021-6

    Article  Google Scholar 

  18. Fèvre, E.M., Bronsvoort, B.M.D.C., Hamilton, K.A. and Cleaveland, S., Animal movements and the spread of infectious diseases, Trends Microbiol., 2006, vol. 14, pp. 125−131. https://doi.org/10.1016/j.tim.2006.01.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Fries, L.T., Williams, D.J. and Johnson, S.K., Occurrence of Anguillicola crassus, an exotic parasitic swim bladder nematode of eels, in the Southeastern United States, Trans. Amer. Fish. Soc., 1996, vol. 125, pp. 794−797. https://doi.org/10.1577/1548-8659(1996)125<0794:NOOCAE>2.3.CO;2

    Article  Google Scholar 

  20. Gargouri Ben Abdallah, L. and Maamouri, F., Spatio-temporal dynamics of the nematode Anguillicola crassus in Northeast Tunisian lagoons, C. R. Biol., 2006, vol. 329, pp. 785−789. https://doi.org/10.3354/dao050181

    Article  PubMed  Google Scholar 

  21. Giari, L., Castaldelli, G., Gavioli, A., et al., 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., 2021, vol. 249, Article 107117. https://doi.org/10.1016/J.ECSS.2020.107117

  22. ICES, Report of the 2011 session of the Joint EIFAAC/ICES Working Group on Eels, EIFAAC Occasional Paper, No. 48, ICES CM 2011/ACOM: 18, Rome: FAO, 2011. https://doi.org/10.17895/ices.pub.8810

  23. Jakob E., Walter, T. and Hanel, R., A checklist of the protozoan and metazoan parasites of European eel (Anguilla anguilla): checklist of Anguilla anguilla parasites, J. Appl. Ichthyol., 2009, vol. 32, pp. 757−804. https://doi.org/10.1111/j.1439-0426.2009.01345.x

    Article  Google Scholar 

  24. Johnson, A., Hatfield, C. and Milne, B., Simulated diffusion dynamics in river networks, Ecol. Model., 1995, vol. 83, pp. 311−325. https://doi.org/10.1016/0304-3800(94)00107-9

    Article  Google Scholar 

  25. Kennedy, C.R., The distribution and abundance of the nematode Anguillicola australiensis in eels Anguilla reinhardtii in Queensland, Australia, Folia Parasitol., 1994, vol. 41, pp. 279−285.

    Google Scholar 

  26. Kennedy, C.R. and Fitch, D.J., Colonization, larval survival and epidemiology of the nematode Anguillicola crassus, parasitic in the eel, Anguilla anguilla, in Britain, J. Fish Biol., 1990, vol. 36, pp. 117–131. https://doi.org/10.1111/j.1095-8649.1990.tb05588.x

    Article  Google Scholar 

  27. Kettle, A.J., Asbjørn Vøllestad, L. and Wibig, J., Where once the eel and the elephant were together: Decline of the European eel because of changing hydrology in southwest Europe and northwest Africa?, Fish Fish., 2011, vol. 12, pp. 380−411. https://doi.org/10.1111/j.1467-2979.2010.00400.x

    Article  Google Scholar 

  28. Kirk, R.S., The impact of Anguillicola crassus on European eels, Fish Manag. Ecol., 2003, vol. 10, pp. 385−394. https://doi.org/10.1111/j.1365-2400.2003.00355.x

    Article  Google Scholar 

  29. Kirk, R.S., Kennedy, C.R. and Lewis, J.W., Effect of salinity on hatching, survival and infectivity of Anguillicola crassus (Nematoda: Dracunculoidea) larvae, Dis. Aquat. Org., 2000, vol. 40, pp. 211−218. https://doi.org/10.3354/dao040211

    Article  CAS  Google Scholar 

  30. Knopf, K., 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 colonized host and the original host, J. Helminthol., 2006, vol. 80, pp. 129−136. https://doi.org/10.1079/JOH2006353

    Article  CAS  PubMed  Google Scholar 

  31. Kristmundsson, Á. and Helgason, S., Parasite communities of eels Anguilla anguilla in freshwater and marine habitats in Iceland in comparison with other parasite communities of eels in Europe, Folia Parasitol., 2007, vol. 54, pp. 141–153. https://doi.org/10.14411/fp.2007.019

    Article  Google Scholar 

  32. Kutz, S.J., Hoberg, E.P., Polley, L. and Jenkins, E.J., Global warming is changing the dynamics of Arctic host-parasite systems, Proc. R. Soc. B, 2005, vol. 272, pp. 2571−2576. https://doi.org/10.1098/rspb.2005.3285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Larsen, M.H. and Mouritsen, K.N., Temperature-parasitism synergy alters intertidal soft-bottom community structure, J. Exp. Mar. Bio. Ecol., 2014, vol. 460, pp. 109–119. https://doi.org/10.1016/j.jembe.2014.06.011

    Article  Google Scholar 

  34. Lefebvre, F., Contournet, P., Priour, F., et al., Spatial and temporal variation in Anguillicola crassus counts: Results of a 4 year survey of eels in Mediterranean lagoons, Dis. Aquat. Org., 2002a, vol. 50, pp. 181–188. https://doi.org/10.3354/dao050181

    Article  CAS  Google Scholar 

  35. Lefebvre, F., Contournet, P. and Crivelli, A.J., The health state of the eel swimbladder as a measure of parasite pressure by Anguillicola crassus, Parasitol., 2002b, vol. 124, pp. 457−463. https://doi.org/10.1017/S0031182001001378

    Article  CAS  Google Scholar 

  36. Lefebvre, F., Sergent, E., Acou, A., et al., Recruitment of glass eels (Anguilla anguilla) on the French Mediterranean coast: A comparative analysis of biometric and pigmentation characteristics during the 1974−75 and 2000−2001 sampling seasons, Bull. Fr. Pêche Piscic., 2003, vol. 368, pp. 85−96.

    Article  Google Scholar 

  37. Lefebvre, F., Fazio, G., and Crivelli, A.J., Anguillicoloides crassus, in Fish Parasites: Pathobiology and Protection, Woo, P.T.K. and Buchmann, K., Eds., Oxford: CABI, 2012a.

    Google Scholar 

  38. Lefebvre, F., Wielgoss, S., Nagasawa, K., and Moravec, F., On the origin of Anguillicoloides crassus, the invasive nematode of anguillid eels, Aquat. Invas., 2012b, vol. 7, pp. 443–453.

    Article  Google Scholar 

  39. Lefebvre, F., Fazio, G., Mounaix, B., and Crivelli, A.J., Is the continental life of the European eel Anguilla anguilla affected by the parasitic invader Anguillicoloides crassus?, Proc. R. Soc. B, 2013, vol. 280, pp. 2012−2916. https://doi.org/10.1098/rspb.2012.2916

    Article  Google Scholar 

  40. Meddour, A. and Meddour-Bouderda, K., Bilan d’une pisciculture extensive et parasites des poissons de la lagune Mellah et du lac Oubeïra (Parc National d’El Kala), Procceding des Journées Internationales sur les Sciences de la Mer J’NESMA99, Atelier B, 657–670, Alger, 1999. https://www.researchgate.net/publication/270051373

  41. Moravec, F., Dracunculoid and Anguillicoloid Nematodes Parasitic in Vertebrates, Prague: Academia, 2006.

    Google Scholar 

  42. Nagasawa, K., Kim, Y.G., and Hirose, H., Anguillicola crassus and A. globiceps (Nematoda: Dracunculoidea) parasitic in the swim bladder of eels (Anguilla japonica and A. anguilla) in East Asia: A review, Folia Parasitol., 1994, vol. 41, pp. 127−137.

    Google Scholar 

  43. Neto, A.F., Passos, D., Costa, J.L., et al., Infection of Anguilla anguilla by the parasite Anguillicoloides crassus in Portuguese brackish water systems, Cah. Biol. Mar., 2014, vol. 55, pp. 213−216. https://doi.org/10.3354/DAO02166

    Article  Google Scholar 

  44. Neumann, W., Schwimmblasen parasit Anguillicola bei Aalen, Fisch. Teichwirt., 1985, vol. 36, pp. 1−322.

    Google Scholar 

  45. Ooi, H.K., Wang, W.S., Chang, H.Y., et al., An epizootic of anguillicolosis in cultured American eels in Taiwan, J. Aquat. Anim. Health., 1996, vol. 8, pp. 163−166. https://doi.org/10.1577/1548-8667(1996)008<0163:AEOAIC>2.3.CO;2

    Article  Google Scholar 

  46. Palstra, A.P., Heppener, D.F.M., van Ginneken, V.J.T., et al., Swimming performance of silver eels is severely impaired by the swim-bladder parasite Anguillicola crassus, J. Exp. Mar. Biol. Ecol., 2007, vol. 352, pp. 244−256. https://doi.org/10.1016/j.jembe.2007.08.003

    Article  Google Scholar 

  47. Panfili, J., and Ximenes, M.C., Evaluation de l’âge et de la croissance de l’anguille européenne (Anguilla anguilla L.) en milieu continental: méthodologies, validation, application en Méditerranée et comparaisons en Europe, Bull. Fr. Pêche Piscic., 1994, vol. 335, pp. 43–66.

    Article  Google Scholar 

  48. Panfili, J., Pontual, H., de Troadec, H. and Wright, P.J., Manuel de sclérochronologie des poisons, Brest: Ifremer-IRD Coédition, 2002. https://doi.org/10.4000/books.irdeditions.20901

    Book  Google Scholar 

  49. Pike, C., Crook, V., and Gollock, M., Anguilla Anguilla, in The IUCN Red List of Threatened Species, 2020, e.T60344A152845178. https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T6034-4A152845178.en

  50. Sauvaget, B., Fatin, D., and Briand, C., Contamination par Anguillicola crassus de cinq populations d’anguilles (Anguilla anguilla) du littoral de Bretagne Sud (France), Bull. Fr. Pêche Piscic., 2003, vol. 368, pp. 21−26. https://doi.org/10.1051/kmae:2003033

    Article  Google Scholar 

  51. Sorci, G. and Garnier, S., Parasitism, Encyclopedia Ecol., 2008, vol. 2, pp. 2645−2650. https://doi.org/10.1016/B978-008045405-4.00814-4

    Article  Google Scholar 

  52. Tahri, M., Crivelli, A.J., Panfili, J., and Bensouilah, M., Health status of the swimbladder of the European eel Anguilla anguilla in northeastern Algeria’s Lake Oubeïra, Int. J. Fish. Aquat. Stud., 2016, vol. 4, pp. 364−369. https://www.fisheriesjournal.com/archives/2016/vol4issue1/PartE/4-1-10.pdf

    Google Scholar 

  53. Thomas, K. and Ollevier, F., Hatching, survival, activity and penetration efficiency of second-stage larvae of Anguillicola crassus (Nematoda), Parasitology, 1993, vol. 197, pp. 211−217. https://doi.org/10.1017/S0031182000067329

    Article  Google Scholar 

  54. Turner, W.C., Kamath, P.L., van Heerden, H., et al., The roles of environmental variation and parasite survival in virulence−transmission relationships, R. Soc. Open. Sci., 2021, vol. 8, Article no. 210088. https://doi.org/10.1098/rsos.210088

    Article  PubMed  PubMed Central  Google Scholar 

  55. van Banning, P. and Haenen, O.L.M., Effects of the swim bladder nematode Anguillicola crassus in wild and farmed eel, Anguilla anguilla, in Pathology in Marine Science, Perkins, F.O., Cheng, T.C., Eds., San Diego: Academic Press, 1990. https://doi.org/10.1111/j.1365-294X.2008.03855.x

    Book  Google Scholar 

  56. Wielgoss, S., Taraschewski, H., Meyer, A., and Wirth, T., Population structure of the parasitic nematode Anguillicola crassus, an invader of declining North Atlantic eel stocks, Mol. Ecol., 2008, vol. 17, pp. 3478−3495.

    Article  CAS  PubMed  Google Scholar 

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ACKNOWLEDGMENTS

We thank Dr. Seraina Emilia Bracamonte from Department of Biodiversity and Evolutionary Biology (Museo Nacional de Ciencias Naturales—MNCN, Spain) for her contribution to the creation of the GLM-model.

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  1. Marine Sciences Department, Faculty of Sciences, Chadli BenDjedid University, El Tarf, Algeria

    M. Tahri

  2. Ecobiology of Marine and Coastal Environments Laboratory, Badji Mokhtar University, Annaba, Algeria

    M. Tahri & M. Bensouilah

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Tahri, M., Bensouilah, M. The European Eel Anguilla anguilla (Anguillidae) Invasion by the Allochthone Nematode Anguillicoloïdes crassus in Southern Mediterranean. J. Ichthyol. 63, 103–111 (2023). https://doi.org/10.1134/S0032945223010150

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