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Are African Longfin Eel Imports a Potential Pathway for Parasite

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Are African Longfin Eel Imports a Potential Pathway for Parasite Journal of Fish Diseases 2014, 37, 843–845 doi:10.1111/jfd.12173 Short Communication Are African longfin eel imports a potential pathway for parasite invasions? O L F Weyl1, H Taraschewski2 and F Moravec3 1 Center for Invasion Biology, South African Institute for Aquatic Biodiversity (SAIAB), Grahamstown, South Africa 2 Department of Ecology and Parasitology, Zoological Institute, Karlsruher Institut fur€ Technologie (KIT), Karlsruhe, Germany 3 Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Ceske Budejovice, Czech Republic Keywords: Anguilla, Anguillicola, Anguillicoloides,inva- populations in Europe (Wirth & Bernatchez sion,pathway,trade. 2003; Wielgoss et al. 2008). In a recent phylogenetic assessment, Laetsch Live eels of the genus Anguilla Schrank are traded et al. (2012) demonstrated that A. crassus was clo- globally for human consumption, stock enhance- sely related to other species in the family Anguilli- ment and aquaculture (Tesch 2003). Live animal colidae Yamaguti. Consequently, Laetsch et al. imports are a global problem and have been a (2012) proposed that other Anguillicoloides species major pathway for introductions of parasitic might transfer to and be pathogenic in na€ıve organisms into novel ecosystems and hosts (Taras- Anguilla species. This hypothesis is partly sup- chewski 2006; Costello et al. 2007). Impacts of ported by the Anguillicoloides novaezelandiae such introductions can be severe, particularly (Moravec & Taraschewski) infestation of when parasites infect hosts that have not evolved a A. anguilla in Italy (Grabner, Dangel & Sures resistance to them (Kennedy 2007). A good exam- 2012) and the successful experimental infection of ple is Anguillicoloides crassus Kuwahara, Niimi & A. anguilla with the African Anguillicoloides paper- Itagaki (Anguillicola according to Laetsch et al. nai (Moravec & Taraschewski) (Taraschewski 2012), a blood-feeding parasite of eel swimblad- et al. 2005). Preventing the introduction and ders that has spread from its natural host the Japa- spread of Anguillicoloides species should therefore nese eel Anguilla japonica Temminck & Schlegel be a high priority, particularly in countries where to na€ıve eel hosts on four continents (Lefebvre eels are economically important. et al. 2012). In na€ıve European eel Anguilla angu- The decline in European and Japanese eel illa L., A. crassus are larger and more fecund and stocks has resulted in an interest in African eel occur at higher prevalence and intensity than in species, and Madagascar, currently the only Afri- their native host (Weclawski et al. 2013). This can producer of eels, has recently started exporting can result in severe impacts on the host popula- eels to Hong Kong, the Republic of Korea and tion, and the A. crassus invasion is thought to have Japan (Crook & Nakamura 2013). The aim of contributed to the decline in A. anguilla the current study was to assess the parasite transfer risks associated with importing these eels. Fifty medium-sized (mean Æ STD total length Correspondence O L F Weyl, Center for Invasion Biology, (TL) = 46.9 Æ 4.5 cm, weight: 238.6 Æ 77.9 g) South African Institute for Aquatic Biodiversity (SAIAB), Private yellow stage African longfin eel Anguilla mossamb- Bag 1015, Grahamstown, South Africa (e-mail: o.weyl@saiab. ac.za) ica Peters, the most common species inhabiting Ó 2013 John Wiley & Sons Ltd 843 Journal of Fish Diseases 2014, 37, 843–845 O L F Weyl et al. Eel trade parasite invasion risk Table 1 Parasite infestation of Anguilla mossambica from Madagascar Intensity Parasite Organ Prevalence (%) Min. Max. Mean Abundance Anguillicoloides papernai (adult) SB 26.5 1 7 2.2 0.59 A. papernai (larva) SB 18.4 1 2 1.4 0.27 Heliconema africanum ST 73.4 1 553 128.6 16.47 Spinitectus sp. ST 18.4 1 5 1.9 0.35 Cestode (larva) ST 2.0 2 2 2.0 0.04 Paraquimperia africana IN 40.8 1 12 3.4 1.39 Nematode (cyst) CA 8.2 1 6 2.3 0.18 SB, swimbladder; ST, stomach; IN, intestine; CA, cavity (n = 50). East Africa and Madagascan Rivers (Lin et al. including the global invader Pseudodactylogyrus 2012) and the natural host of A. papernai (Taras- anguillae (Yin & Sproston) (Parker, Weyl & Tar- chewski et al. 2005), were obtained from a com- aschewski 2011), the lack of external parasites was mercial eel supplier based in Madagascar. not surprising because the fish may have been According to the supplier, the eels were collected treated using one of a variety of treatments avail- from the Maningory River system (17°49′53″S, able for external parasites (e.g. Buchmann & Bjer- 48°25′44″E). They were issued with a veterinary regaard 1990). Veterinary certification was most certificate, packaged and airfreighted to South likely issued on the basis of their healthy, and par- Africa on 27 May 2008. asite free, external appearance. Internally these fish On arrival, eels were killed by concussion and were however heavily parasitized, and live A. mos- destruction of the brain. Internal organs (gills, swim- sambica are therefore a potential vector and their bladder, stomach and intestine) were dissected from trade a potential pathway for new parasitic inva- the fish and examined for parasites, which were col- sions. Countries should therefore apply a precau- lected, identified to the lowest possible taxon and tionary approach regarding the importation of counted. Prevalence, intensity and abundance, cal- A. mossambica, at least until the associated risks culated after Busch et al. (1997), are reported in are better understood. Table 1. No parasites were observed either on the skin or gills, but internal parasites were collected Acknowledgements from most (92%) of the sample. These included A. papernai from the swimbladder and the gastroin- We would like to thank the National Research testinal parasites Heliconema africanum (Linstow), a Foundation of South Africa (NRF) SA/Germany Spinitectus Fourment sp. and Paraquimperia africana Research Cooperation Programme (UID 72088) Moravec, Boomker & Taraschewski. Two unidenti- for funding; the South African Department of Eco- fied larval cestodes and cysts of an unidentified nem- nomic Development and Environmental Affairs, atode were also sampled. Marine and Coastal Management and the Depart- While A. papernai, H. africanum and P. afri- ment of Agriculture for Providing Import Permits; cana are common parasites of A. mossambica and Jessica Escobar for Laboratory Assistance. (Taraschewski et al. 2005; Moravec, Weyl & Tar- aschewski 2013), no Spinitectus sp. or any cestodes References have previously been documented from A. mos- sambica, and these should be considered a poten- Buchmann K. & Bjerregaard J. (1990) Mebendazole treatment tial invasion risk to mainland Africa. Even more of pseudodactylogyrosis in an intensive eel-culture system. Aquaculture 86, 139–153. concerning is that the trade of live A. mossambica will most likely facilitate the transport of the Busch A.O., Lafferty K.D., Lotz J.M. & Shostak A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. A. papernai, H. africanum and P. africana to Revisited. Journal of Parasitology 83, 575–583. novel host systems in Asia. Costello C., Springborn M., McAusland C. & Solow A. The results also illustrate the difficulty in deal- (2007) Unintended biological invasions: does risk vary by ing with internal parasites of fishes. Although Afri- trading partner? Journal of Environmental Economics and can eels are susceptible to external parasites, Management 54, 262–276. Ó 2013 John Wiley & Sons Ltd 844 Journal of Fish Diseases 2014, 37, 843–845 O L F Weyl et al. Eel trade parasite invasion risk Crook V. & Nakamura M. (2013) Assessing supply chain and Parker D., Weyl O.L.F. & Taraschewski H. (2011) Invasion of market impacts of a CITES listing on Anguilla species. a South African Anguilla mossambica (Anguillidae) TRAFFIC Bulletin 25,24–30. population by the alien gill worm Pseudodactylogyrus 46 – Grabner D.S., Dangel K.C. & Sures B. (2012) Merging anguillae (Monogenea). African Zoology , 371 377. species? Evidence for hybridization between the eel parasites Taraschewski H. (2006) Hosts and parasites as aliens. Journal Anguillicola crassus and A. novaezelandiae (Nematoda, of Helminthology 80,99–128. 5 Anguillicolidea). Parasites & Vectors , 244. Taraschewski H., Boomker J., Knopf K. & Moravec F. (2005) Kennedy C.R. (2007) The pathogenic helminth parasites of Anguillicola papernai (Nematoda: Anguillicolidae) and other eels. Journal of Fish Diseases 30, 319–334. helminths parasitizing the African longfin eel Anguilla 63 – Laetsch D.R., Heitlinger E.G., Taraschewski H., Nadler S.A. mossambica. Diseases of Aquatic Organisms , 185 195. & Blaxter M.L. (2012) The phylogenetics of Anguillicolidae Tesch F.W. (2003) The eel. Blackwell Science and the Fisheries (Nematoda: Anguillicolidea), swimbladder parasites of eels. Society of the British Isles, Oxford, UK. 12 BMC Evolutionary Biology , 60. Weclawski U., Heitlinger E.G., Baust T., Klar B., Petney T., Lefebvre F., Wielgoss S., Nagasawa K. & Moravec F. San Han Y. & Taraschewski H. (2013) Evolutionary (2012) On the origin of Anguillicoloides crassus, the divergence of the swim bladder nematode Anguillicola crassus invasive nematode of anguillid eels. Aquatic Invasions 7, after colonization of a novel host, Anguilla anguilla. BMC 443–453. Evolutionary Biology 13, 78. Lin Y.-J., Jessop B.M., Weyl O.L.F., Iizuka Y., Lin S.-H., Wielgoss S., Taraschewski H., Meyer A. & Wirth T. (2008) Tzeng W.N. & Sun C.L. (2012) Regional variation in Population structure of the parasitic nematode Anguillicola otolith Sr:Ca ratios of African longfinned eel Anguilla crassus, an invader of declining North Atlantic eel stocks. mossambica and mottled eel Anguilla marmorata: a challenge Molecular Ecology 17, 3478–3495. to the classic tool for reconstructing migratory histories of Wirth T. & Bernatchez L. (2003) Decline of North Atlantic 81 – fishes. Journal of Fish Biology , 427 441. eels: a fatal synergy? Proceedings of the Royal Society London. Moravec F., Weyl O. & Taraschewski H. (2013) Redescription Biology 270, 681–688. of Heliconema africanum (Linstow, 1899) n.
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