Abstract
Background
Non-native parasites are often translocated into novel areas together with their natural hosts, but the parasite diversity is frequently lower compared to the host’s native range.
Purpose
This paper provides morphological and molecular characterisation for non-native monogenean parasite Onchocleidus principalis (Ancyrocephalidae) co-introduced with its fish host to Portugal, Europe, including new details on the species’ vaginal morphology and metrics.
Methods
Two host species, the largemouth bass Micropterus salmoides and pumpkinseed sunfish Lepomis gibbosus, were sampled from two reservoirs (Landeira, Coruche) in the Atlantic Sea drainage. Morphometric analysis and sequencing of 28S rDNA were performed.
Results
Presence of O. principalis was confirmed in all individuals of largemouth bass. Accidental findings on pumpkinseed sunfish at both sampling sites represent new host records for this parasite species. The morphometric description of O. principalis showed high similarity to the species in its native range. No intraspecific sequence variation of partial 28S rDNA was observed between specimens from the two sampling sites. Presence of another North-American ancyrocephalid parasite Onchocleidus dispar was confirmed in pumpkinseed sunfish at both sites, and in largemouth bass from the Coruche Reservoir, this representing the first record of O. dispar on largemouth bass in Europe.
Conclusion
Onchocleidus principalis has been confirmed to parasitise both centrarchid fish species introduced to Europe. Compared to other studies, the species collected in Portugal exhibits pronounced vaginal armament.
References
Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630
MacLeod CJ, Paterson AM, Tompkins DM, Duncan RP (2010) Parasites lost—do invaders miss the boat or drown on arrival? Ecol Lett 13:516–527
Philipp DP, Ridgway MS (2002) Black Bass: Ecology, Conservation and Management. American Fisheries Society, Symposium 31, Bethesda, Maryland
García-Berthou E, Moreno-Amich R, Coden A (2000) Introduction of exotic fish into a Mediterranean lake over a 90-year period. Arch Hydrobiol 149:271–284
Ribeiro F, Collares-Pereira MJ, Moyle PB (2009) Non-native fish in the fresh waters of Portugal, Azores and Madeira Islands: a growing threat to aquatic biodiversity. Fisheries Manag Ecol 16:255–264
Ferreira de Lima M (1954) O Black-bass e a sua aclimatação em águas Portuguesas. Revista de Montes 56:133–134
Hoffman GL (1999) Parasites of North American freshwater fishes. Cornell University Press, Ithaca
Froese R, Pauly D (2019) FishBase. World Wide Web electronic publication. www.fishbase.org. Accessed Sept 2019
Costa APL, Takemoto RM, Vitule JRS (2018) Metazoan parasites of Microperus salmoides (Lacepede, 1802) (Perciformes, Centrarchidae): a review with evidences of spillover and spillback. Parasitol Res 117:1671–1681
Havlátová L, Ondračková M, Přikrylová I (2015) Monogenean parasites of Lepomis gibbosus Linnaeus introduced into the River Durance, France. Helminthologia 52:323–330
Ondračková M, Kvach Y, Martens A, Jurajda P (2019) Limited parasite acquisition by non-native Lepomis gibbosus (Actinopterygii: Centrarchidae) at two ponds in the Upper Rhine basin, Germany. J Helm 93:453–460
Mizelle JD, Regensberg BR (1945) Studies on Monogenetic Trematodes. XII. Dactylogyridae from Wisconsin Fishes. Am Midl Nat 43:673–700
Maitland PS, Price CE (1969) Urocleidus principalis (Mizell, 1936), a North American monogenetic trematode new to British Isles, probably introduced with the largemouth bass Micropterus salmoides (Lacepede, 1802). J Fish Biol 1:17–18
Lambert A (1978) Study of the larval stages of Monogenea of fishes. Ann Parasit Hum Comp 53:551–559
Galli P, Strona G, Benzoni F, Crosa G, Stefani F (2007) Monogenoids from freshwater fish in Italy, with comments on alien species. Comp Parasitol 74:264–272
Truter M, Přikrylová I, Weyl OLF, Smit NJ (2017) Co-introduction of ancyrocephalid monogeneans on their invasive host, the largemouth bass, Micropterus salmoides (Lacepede, 1802) in South Africa. Int J Parasitol Parasit Wildlife 6:420–429
Costa APL (2016) Fauna parasitária do peixe invasor Micropterus salmoides (Lacepede 1802): Revisão e análise da influencia da influência da pressão em reservatérios do sul do Brasil. Dissertation, Federal University of Paraná.
Mendoza-Garfias B, García-Prieto L, De León GPP (2017) Checklist of the Monogenea (Platyhelminthes) parasitic in Mexican aquatic vertebrates. Zoosystema 39:501–598
Grupcheva GI, Nedeva IL (1999) Parasite fauna of the crucian carp (Carassius auratus gibelio Bloch) in the Zrebchevo reservoir (Bulgaria). Acta Zool Bulgar 51:115–122
Kvach Y, Ondračková M, Janáč M, Jurajda P (2016) Methodological issues affecting the study of fish parasites. 1. Duration of live fish storage prior to dissection. Dis Aquat Organ 192:107–115
Malmberg G (1970) The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Ark Zool 23:1–235
Lim LHS, Gibson DI (2008) Redescriptions of species of Ancyrocephaloides Yamaguti, 1938 (Monogenea: Ancyrocephalidae) from triacanthid fishes caught off Peninsular Malaysia and a report of their haptoral secretions. Syst Parasitol 69:59–73
Beverley-Burton M (1984) Monogenea and Turbellaria. In: Margolis L, Kabata Z (eds) Guide to the parasites of fishes of Canada. Part I. Can Publ Fish Aquat Sci, Canada
Gusev AV, Dubinina MN, Raikova EV, Khotenkovskiy IA, Pugachev ON, Ergens R (1985) Paraziticheskiye mnogokletochnye. Part 1. Monogenea. In: Bauer ON (ed) Opredelitel parazitov presnovodnykh ryb fauny SSSR, vol 2. Nauka, Leningrad, pp 1–425
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
Hassouna N, Mithot B, Bachellerie J-P (1984) The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Res 12:3563–3583
Wheeler TA, Beverley-Burton M (1989) Systematics of Onchocleidus Mueller, 1936 (Monogenea: Ancyrocephalidae): generic revision. Can J Zool 67:136–157
Anastácio PM, Ribeiro F, Capinha C, Banha F, Gama M, Filipe AF, Rebelo R, Sousa R (2019) Non-native freshwater fauna in Portugal: a review. Sci Total Environ 650:1923–1934
Ondračková M, Dávidová M, Přikrylová I, Pečínková M (2011) Monogenean parasites of introduced pumpkinseed Lepomis gibbosus (Centrarchidae) in the Danube River Basin. J Helminthol 85:435–441
Rohde K (1991) Size differences in hamuli of Kuhnia scombri (Monogenea: Polyopisthocotylea) from different geographical areas not due to differences in host size. Int J Parasitol 21:113–114
Simkova A, Matejusova I, Cunningham CO (2006) A molecular phylogeny of the Dactylogyridae sensu Kritsky & Boeger (1989) (Monogenea) based on the D1–D3 domains of large subunit rDNA. Parasitology 133:43–53
Acknowledgements
The authors would like to thank Nikol Kmentová and Pavel Jurajda for help with fish and parasite sampling, and Kevin Roche for English correction. This work was supported by the FRISK Project (Ref. PTDC/AAG-MAA/0350/2014) and by the strategic plan of MARE—Marine and Environmental Sciences Centre (UID/MAR/04292/2013). MP was supported by the project PROFISH CZ.02.1.01/0.0/0.0/16_019/0000869.
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MO conceived and designed the study, determined parasite species and wrote the paper. FR collected fish hosts, MP, IP, YK performed the parasitological examination and specimens collection. MP performed the morphometrical analysis, MS performed molecular analysis. All authors contributed to the final version of the manuscript.
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All national and institutional guidelines for the care and use of animals were followed. Fish sampling carried out in compliance with fishing permits No. 410/2016/CAPT and 411/2016/CAPT.
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Ondračková, M., Pravdová, M., Seifertová, M. et al. Onchocleidus principalis (Monogenea: Ancyrocephalidae) Co-introduced to Europe with Centrarchid Fish. Acta Parasit. 65, 974–979 (2020). https://doi.org/10.2478/s11686-020-00217-y
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DOI: https://doi.org/10.2478/s11686-020-00217-y