This study reports on three species of Dactylogyrus Diesing, 1850 (Dactylogyridae) collected from tinfoil barb, Barbonymus schwanenfeldii (Bleeker) which were imported into South Africa as ornamental fish from Sri Lanka and Thailand. Supplementary morphometric characterisation and molecular data (partial 18S and 28S rDNA, and ITS1 region sequences) are presented for Dactylogyrus lampam (Lim & Furtado, 1986), Dactylogyrus tapienensis Chinabut & Lim, 1993 and Dactylogyrus viticulus Chinabut & Lim, 1993. Prevalence of Dactylogyrus spp. infection was 87% and 80% for fish from Sri Lanka and Thailand, respectively. Composition of the parasites between the fish of each origin differed. All three species were found to infect fish from Thailand, but only D. lampam was present on the fish received from Sri Lanka. Phylogenetic analysis revealed the position of studied species, with D. lampam clustering within the lineages of varicorhini-type species, while D. tapienensis and D. viticulus form a sister lineage to Dactylogyrus spp. associated with Cyprinus carpio L. and Carassius spp., species parasitising central African large cyprinids (Labeo Cuvier), and species parasitising African and Middle Eastern Carasobarbus spp.

TITLE: Dactylogyrus spp. (Dactylogyridae, Monogenea) de Barbonymus schwanenfeldii importé en Afrique du Sud : caractérisation morphométrique et moléculaire. ABSTRACT: Cette étude porte sur trois espèces de Dactylogyrus Diesing, 1850 (Dactylogyridae), prélevées sur des Barbonymus schwanenfeldii (Bleeker) qui ont été importés en Afrique du Sud comme poissons d’ornement depuis le Sri Lanka et la Thaïlande. Une caractérisation morphométrique et des données moléculaires supplémentaires (ADNr 18S et 28S partiels et séquences de la région ITS1) sont présentées pour Dactylogyrus lampam (Lim & Furtado, 1986), Dactylogyrus tapienensis Chinabut & Lim, 1993 et Dactylogyrus viticulus Chinabut & Lim, 1993. La prévalence de l’infection par les Dactylogyrus spp. était respectivement de 87 % et 80 % pour les poissons du Sri Lanka et de Thaïlande. La composition des parasites entre les poissons des deux origines différait. Les trois espèces infectaient les poissons de Thaïlande, mais seul D. lampam était présent sur les poissons du Sri Lanka. L’analyse phylogénétique a révélé la position des espèces étudiées, D. lampam se regroupant dans les lignées d’espèces de type varicorhini, tandis que D. tapienensis et D. viticulus forment une lignée sœur des Dactylogyrus spp. associés à Cyprinus carpio L. et Carassius spp., espèces parasitant les grands cyprinidés d’Afrique centrale (Labeo Cuvier), et espèces parasitant les Carasobarbus spp. d’Afrique et du Moyen-Orient.

Department of Botany and Zoology Faculty of Science Masaryk University 611 37 Brno Czech Republic Department of Zoology Faculty of Sciences Comenius University in Bratislava 841 04 Bratislava Slovakia

DSI NRF SARChI Chair Department of Biodiversity University of Limpopo Sovenga 0727 South Africa

DSI NRF SARChI Chair Department of Biodiversity University of Limpopo Sovenga 0727 South Africa Water Research Group Unit for Environmental Sciences and Development North West University Potchefstroom 2520 South Africa

See more in PubMed

Acosta AA, Truter M, Malherbe W, Smit NJ. 2022. Morphological description and molecular characterisation of Dactylogyrus matlopong sp. n. (Monogenea: Dactylogyridae) from the South African endemic Labeobarbus aeneus (Cyprinidae: Torinae). Folia Parasitologica, 69, 21. PubMed

Apiwong K, Wongsawad C, Butboonchoo P. 2018. Morphological and molecular characterization of Haplorchoides mehrai Pande and Shukla 1976 (Digenea: Heterophyidae) from Chiang Mai province. Helminthologia, 55, 334–342. PubMed PMC

Benovics M, Desdevides Y, Vukić J, Šanda R, Šimková A. 2018. The phylogenetic relationships and species richness of host-specific Dactylogyrus parasites shaped by the biogeography of Balkan cyprinids. Scientific Reports, 8, 13006–13018. PubMed PMC

Benovics M, Desdevides Y, Šanda R, Vukić J, Scheifler M, Doadrio I, Sousa-Santos C, Šimková A. 2020. High diversity of fish ectoparasitic monogeneans (Dactylogyrus) in the Iberian Peninsula: a case of adaptive radiation? Parasitology, 147, 418–430. PubMed PMC

Benovics M, Vukić J, Šanda R, Rahmouni I, Šimková A. 2020. Disentangling the evolutionary history of peri-Mediterranean cyprinids using host-specific gill monogeneans. International Journal for Parasitology, 50(12), 969–984. PubMed

Benovics M, Francová K, Volta P, Dlapka V, Šimková A. 2021. Helminth communities of endemic cyprinoids of the Apennine Peninsula, with remarks on ectoparasitic monogeneans, and a description of four new Dactylogyrus Diesing, 1850 species. Parasitology, 148, 1003–1018. PubMed PMC

Benovics M, Nejat F, Abdoli A, Šimková A. 2021. Molecular and morphological phylogeny of host-specific Dactylogyrus parasites (Monogenea) sheds new light on the puzzling Middle Eastern origin of European and African lineages. Parasites & Vectors, 14, 372. PubMed PMC

Benovics M, Vukić J, Šanda R, Nejat F, Charmpila EA, Buj I, Shumka S, Porcelloti S, Tarkan SA, Aksu S, Emiroğlu O, Šimková A. 2023. Monogeneans and chubs: ancient host-parasite system under the looking glass. Molecular Phylogenetics and Evolution, 179, 107667. PubMed

Bush AO, Lafferty KD, Lotz JM, Shostak AW. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583. PubMed

Cheong L. 1996. Overview of the current international trade in ornamental fish with special reference to Singapore. In: Preventing the spread of aquatic animal diseases. (Eds. B. J. Hill and T. Hastein). Revue Scientifique et Technique, 15, 445–481. PubMed

Chinabut L, Lim S. 1993. Seven new species of Dactylogyrus Diesing, 1850 (Monogenea) from Puntius hamilton (Cyprinidae) of Thailand. Raffles Bulletin of Zoology, 41, 47–59.

Copp GH, Wesley KJ, Vilizzi L. 2005. Pathways of ornamental and aquarium fish introductions into urban ponds of Epping Forest (London, England): the human vector. Journal of Applied Ichthyology, 21, 263–274.

Darriba D, Taboala GL, Doallo R, Posada D. 2012. JModelTest2: more models, new heuristics and parallel computing. Nature Methods, 9, 772. PubMed PMC

Dove AD, Ernst I. 1998. Concurrent invaders – four exotic species of Monogenea now established on exotic freshwater fishes in Australia. International Journal for Parasitology, 28, 1755–1764. PubMed

Ergens R. 1969. The suitability of ammonium picrate-glycerin preparing slides of lower Monogenoidea. Folia Parasitologica, 16(4), 320.

Esa Y, Japning JRR, Rahim KAA, Siraj SS, Daud SK, Tan SN, Sungan S. 2012. Phylogenetic relationships among several freshwater fishes (Family: Cyprinidae) in Malaysia inferred from partial sequencing of the cytochrome b mitochondrial DNA (mtDNA). Pertanika Journal of Tropical Agricultural Science, 35(2), 307–318.

Fricke R, Eschmeyer W, Van Der Laan R. 2021. Eschmeyer’s catalog of fishes. Genera, species references. http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp.

Gertzen E, Familiar O, Leung B. 2008. Quantifying invasion pathways: fish introductions from the aquarium trade. Canadian Journal of Fisheries and Aquatic Sciences, 65(7), 1265–1273.

Gibson DI, Timofeeva TA, Gerasev PI. 1996. A catalogue of the nominal species of the monogenean genus Dactylogyrus Diesing, 1850 and their host genera. Systematic Parasitology, 35, 3–48.

Guindon S, Gascuel O. 2003. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 27, 1759–1767. PubMed

Gussev AV. 1985. Metazoan parasites. Part I. Key to parasites of freshwater fish of USSR, Vol. 2. Leningrad: Nauka.

Ha K. 1971. New species of monogenean form freshwater fishes of Morth Vietnam. II. Parazitologia, 5, 429–440.

Hafiza N, Shaharom-Harrison F. 2020. The description of Nematode in Barbonymus schwanenfeldii at Kenyir Lake, Terengganu. Universiti Malaysia Terengganu Journal of Undergraduate Research, 2, 31–36.

Hassouna N, Michot B, Bachellerie JP. 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 Research, 12, 3563–3583. PubMed PMC

Jiménez-García MI, Vidal-Martínez VM, López-Jiménez S. 2001. Monogeneans in introduced and native cichlids in Mexico: evidence for transfer. Journal of Parasitology, 87, 907–909. PubMed

Kamarudin KR, Esa Y. 2009. Phylogeny and phylogeography of Barbonymus schwanenfeldii (Cyprinidae) from Malaysia inferred using partial cytochrome b mtDNA gene. Journal of Tropical Biology and Conservation, 5, 1–13.

Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on Fourier transform. Nucleic Acids Research, 30, 3059–3066. PubMed PMC

Lim LHS, Furtado JI. 1986. Sixteen new species of Dactylogyrus from Genus Puntius Hamilton (Cyprinidae). Folia Parasitologia, 33, 21–34.

Lintermans M. 2004. Human-assisted dispersal of alien freshwater fish in Australia. New Zealand Journal of Marine and Freshwater Research, 38, 481–501.

Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL. 2014. Co-invaders: the effects of alien parasites on native hosts. International Journal for Parasitology: Parasites and Wildlife, 3, 171–177. PubMed PMC

Malmberg G. 1957. On a new genus of viviparous monogenetic trematode. Arkiv for Zoologi, 10, 317–329.

Mendoza-Palmero CA, Blasco-Costa I, Scholz T. 2015. Molecular phylogeny of Neotropical monogeneans (Platyhelminthes: Monogenea) from catfishes (Siluriformes). Parasites & Vectors, 8, 164. PubMed PMC

Mizelle JD. 1936. New species of trematodes from the gills of Illinois fishes. American Midland Naturalist, 17, 785–806.

Mohanta SK, Chandra KJ. 2000. Monogenean infestations in Thai silver barb (Barbodes gonionotus Bleeker) and their adaptations in Bangladesh waters. Bangladesh Journal of Fisheries Research, 4(2), 147–155.

Mouton A, Basson L, Impson D. 2001. Health status of ornamental freshwater fishes imported to South Africa: a pilot study. Aquarium Sciences and Conservation, 3, 313–319.

Musilová N, Řehulková E, Gelnar M. 2009. Dactylogyrids (Platyhelminthes: Monogenea) from the gills of the African carp, Labeo coubie Rüppell (Cyprinidae), from Senegal, with descriptions of three new species of Dactylogyrus and the redescription of Dactylogyrus cyclocirrus Paperna, 1973. Zootaxa, 2241(1), 47–68.

Namsanor J, Kiatsopit N, Laha T, Andrews RH, Petney TN, Sithithaworn P. 2020. Infection dynamics of Opisthorchis viverrine Metacercariae in Cyprinid fishes from two endemic areas in Thailand and Lao PDR. American Journal of Tropical Medicine and Hygiene, 102, 110–116. PubMed PMC

Pettersen RA, Ostbye K, Holmen J, Vollestad LA, Mo TA. 2016. Gyrodactylus spp. Diversity in native and introduced minnow (Phoxinus phoxinus) populations: no support for “the enemy release” hypothesis. Parasites & Vectors, 9, 51. PubMed PMC

Pugachev ON, Gerasev PI, Gussev AV, Ergens R, Khotenowsky I. 2009. Guide to Monogenoidea of freshwater fish of Palaearctic and Amur regions. Milan: Ledizione-LediPublishing, 568 p.

Rahmouni I, Řehulková E, Pariselle A, Rkhami OB, Šimková A. 2017. Four new species of Dactylogyrus (Monogenea: Dactylogyridae) parasitizing the gills of northern Moroccan Luciobarbus (Cyprinidae): morphological and molecular characterization. Systematic Parasitology, 94, 575–591. PubMed

Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67, 901–904. PubMed PMC

Raphahlelo ME, Přikrylová I, Matla MM. 2020. Dactylogyrus spp. (Monogenea, Dactylogyridae) from the gills of Enteromius spp. (Cypriniformes, Cyprinidae) from the Limpopo Province, South Africa with descriptions of three new species. Acta Parasitologica, 65, 396–412. PubMed

Řehulková E, Seifertová M, Přikrylová I, Francová K. 2018. Monogenea, in A guide to the parasites of African freshwater fishes, Scholz T, Vanhove MPM, Smit N, Jayasundera Z, Gelnar M, Editors. RBINS′ Scientific Publication Unit, ABC Taxa: Brussels. p. 185–243.

Řehulková E, Benovics M, Šimková A. 2020. Uncovering the diversity of monogeneans (Platyhelminthes) on endemic cypriniform fishes of the Balkan Peninsula: new species of Dactylogyrus and comments on their phylogeny and host-parasite associations in a biogeographic context. Parasite, 27, 66. PubMed PMC

Řehulková E, Rahmouni I, Pariselle A, Šimková A. 2021. Integrating morphological and molecular approaches for characterizing four species of Dactylogyrus (Monogenea: Dactylogyridae) from Moroccan cyprinids, with comments on their host specificity and phylogenetic relationships. PeerJ, 9, 1067. PubMed PMC

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across large model space. Systematic Biology, 61, 539–542. PubMed PMC

Šimková A, Plaisance L, Matějusová I, Morand S, Verneau O. 2003. Phylogenetic relationships of the Dactylogyridae Bychowsky, 1933 (Monogenea: Dactylogyridae): the need for the systematic revision of the Ancyrophalinae Bychowsky, 1937. Systematic Parasitology, 54, 1–11. PubMed

Šimková A, Morand S, Jobet E, Gelnar M, Verneau O. 2004. Molecular phylogeny of congeneric monogenean parasites (Dactylogyrus): a case of intrahost speciation. Evolution, 58, 1001–1018. PubMed

Šimková A, Matějusová I, Cunningham CO. 2006a. 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. PubMed

Šimková A, Verneau O, Gelnar M, Morand S. 2006b. Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish. Evolution, 60, 1023–1037. PubMed

Šimková A, Pečínková M, Řehulková E, Vyskočilová M, Ondračková M. 2007. Dactylogyrus species parasitizing European Barbus species: morphometric and molecular variability. Parasitology, 134, 1751–1765. PubMed

Šimková A, Benovics M, Rahmouni I, Vukić J. 2017. Host-specific Dactylogyrus parasites revealing new insights on the historical biogeography of Northwest African and Iberian cyprinid fish. Parasites & Vectors, 10, 58. PubMed PMC

Šimková A, Řehulková E, Choudhury A, Seifertová M. 2022. Host-specific parasites reveal the history and biogeographical contacts of their hosts: the monogenea of Nearctic cyprinoid fishes. Biology, 11(2), 223. PubMed PMC

Smit NJ, Malherbe W, Hadfield KA. 2017. Alien freshwater fish parasites from South Africa: diversity, distribution, status and the way forward. International Journal for Parasitology: Parasites and Wildlife, 6, 386–401. PubMed PMC

Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690. PubMed

Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analyses and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. PubMed PMC

Stout CC, Tan M, Lemmon AR, Lemmon EM, Armbruster JW. 2016. Resolving Cypriniformes relationships using an anchored enrichment approach. BMC Evolutionary Biology, 16, 1–13. PubMed PMC

Székely Cs, Shaharom-Harrison F, Cech G, Ostoros G, Molnár K. 2009. Myxozoan infections in fishes of the Tasik Kenyir water reservoir, Terengganu, Malaysia. Diseases of Aquatic Organisms, 83, 37–48. PubMed

Tan M, Armbruster JW. 2018. Phylogenetic classification of extant genera of fishes of the order Cypriniformes (Teleostei: Ostariophysi). Zootaxa, 4476, 006–039. PubMed

Tancredo KR, Martins ML. 2019. Three previous recorded species of Dactylogyrus Diesing, 1850 (Monogenea: Dactylogyridae) infecting cultured Carassius auratus in southern Brazil. Journal of Parasitic Diseases, 43(3), 522–527. PubMed PMC

Tavakol S, Halajian A, Smit WJ, Hoffman A, Luus-Powell WJ. 2017. Guppies (Poecilia reticulata) introducing an alien parasite, Camallanus cotti (Nematoda: Camallanidae) to Africa, the first report. Parasitology Research, 116(12), 3441–3445. PubMed

Thilakaratne I, Rajapaksha G, Hewakopara A, Rajapakse R, Faizal A. 2003. Parasitic infections in freshwater ornamental fish in Sri Lanka. Diseases of Aquatic Organisms, 54, 157–162. PubMed

Trujillo-González A, Becker JA, Hutson KS. 2018. Parasite dispersal from the ornamental goldfish trade. Advances in Parasitology, 100, 239–281. PubMed

Trujillo-González A, Edmunds RC, Becker JA, Hutson KS. 2019. Parasite detection in the ornamental fish trade using environmental DNA. Scientific Reports, 9, 5173. PubMed PMC

Truter M, Přikrylová I, Weyl OL, Smit NJ. 2017. Co-introduction of ancyrocephalid monogeneans on their invasive host, the largemouth bass, Micropterus salmoides (Lacepéde, 1802) in South Africa. International Journal for Parasitology: Parasites and Wildlife, 6, 420–429. PubMed PMC

Truter M, Smit NJ, Malherbe W, Přikrylová I. 2021. Description of Gyrodactylus paludinosus sp. nov. (Monogenea: Gyrodactylidae) from the Straightfin Barb, Enteromius paludinosus (Peters, 1852), in South Africa. Acta Parasitologica, 67(1), 446–453. PubMed

Tu X, Ling F, Huang A, Wang G. 2015. An infection of Gyrodactylus kobayashii Hukuda, 1940 (Monogenea) associated with the mortality of goldfish (Carassius auratus) from central China. Parasitology Research, 114(2), 737–745. PubMed

Whittington RJJ, Chong R. 2007. Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Preventive Veterinary Medicine, 81, 92–116. PubMed

Yang L, Sado T, Hirt VM, Pasco-Viel E, Arunachalm M, Li J, Wang X, Freyhof J, Saitoh K, Simons AM, Miya M, He S, Mayden RL. 2015. Phylogeny and polyploidy: resolving the classification of cyprinine fishes (Teleostei: Cypriniformes). Molecular Phylogenetics and Evolution, 85, 97–116. PubMed

Zakaria-Ismail M. 1990. Cyprinid fishes of the Genus Cyclocheilichtys in Peninsular Malaysia. Malayan Nature Journal, 44, 109–121.