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Global parasite trafficking: Asian Gyrodactylus (Monogenea) arrived to the U.S.A. via invasive fish Misgurnus anguillicaudatus as a threat to amphibians

  • Florian B. ReydaEmail author
  • Scott M. Wells
  • Alexey V. Ermolenko
  • Marek S. Ziętara
  • Jaakko I. Lumme
Original Paper

Abstract

A monogenean flatworm Gyrodactylus jennyae Paetow, Cone, Huyse, McLaughlin & Marcogliese, 2009 was previously described as a pathogen on bullfrog Lithobates catesbeianus Shaw, 1802, in a Canadian captive population originating in Missouri, U.S.A. The ITS barcoding of G. jennyae showed relatedness to Asian Gyrodactylus macracanthus Hukuda 1940, a parasite of the Asian loach Misgurnus anguillicaudatus Cantor, 1842. The resulting suggestion that the globally invasive pet-trade of fish may be a mechanism for arrival of Gyrodactylus species to North America provided the framework for the current study. The present study was undertaken following the discovery of two other species of Gyrodactylus in a population of illegally introduced M. anguillicaudatus in New York State. Here the invasion hypothesis was tested via DNA sequencing of the ITS of the two Gyrodactylus species obtained from M. anguillicaudatus from New York, termed Gyrodactylus sp. A and Gyrodactylus sp. B. Both Gyrodactylus sp. A and Gyrodactylus sp. B were closely related to G. jennyae and G. macracanthus, and all belong to a molecularly well-supported monophyletic Asian freshwater group. In conclusion, this invasive fish has trafficked at least three parasite species to the U.S.A., one of them also found on frog. This route from the Asian wetlands to other continents is similar to that of amphibian chytrid fungi of genus Batrachochytrium Longcore, Pessier & Nichols, 1999.

Keywords

Intercontinental parasite dispersal Molecular systematics Aquatic invasive species Chytrid fungus 

Notes

Acknowledgements

Late Professor Ian Whittington informed us of the Australian situation. The early molecular work in Oulu University was supported by the Academy of Finland (Grants 63787, 134592). Laura Törmälä conducted the DNA work in Oulu. The authors thank Timothy Pokorny (New York State Dept. of Environmental Conservation) for assisting with fish collections. We also acknowledge the students of the SUNY Oneonta fall 2013 parasitology class and other SUNY Oneonta students: Tara Aprill, Austin Borden, Jill Darpino, Margaret Doolin, Kathryn Forti, Kaylee Herzog, Elise Iwanyckyj, Sisina Macchiarelli, Zachary Piper, Sam VanDemark, and Craig Wert for their assistance with dissections of M. anguillicaudatus. This study was funded in part by a National Science Foundation Field Stations and Marine Laboratories Grant to W. Harman (NSF DBI 1034744). The comments of two anonymous reviewers contributed to the development of this manuscript.

Supplementary material

10530_2019_2097_MOESM1_ESM.pdf (859 kb)
Supplementary material 1 (PDF 859 kb)

References

  1. Arkush KD, Mendoza L, Adkison MA, Hedrick RP (2003) Observations on the life stages of Sphaerothecum destruens n. g., n. sp., a Mesomycetozoean fish pathogen formally referred to as the Rosette Agent. J Eukaryot Microbiol 50:430–438PubMedCrossRefPubMedCentralGoogle Scholar
  2. Avise JC (2000) The history and formation of species. Harward University Press, CambridgeGoogle Scholar
  3. Bakke TA, Harris PD, Cable J (2002) Host specificity dynamics: observations on gyrodactylid monogeneans. Int J Parasitol 32:281–308PubMedCrossRefPubMedCentralGoogle Scholar
  4. Bakke TA, Cable J, Harris PD (2007) The biology of gyrodactylid monogeneans: the “Russian-Doll killers”. Adv Parasitol 64:161–377PubMedCrossRefPubMedCentralGoogle Scholar
  5. Belle CC, Stoekle BC, Cerwenka AF, Kuehn R, Mueller M, Pander J, Geist J (2017) Genetic species identification in weatherfish and first molecular confirmation of Oriental Weatherfish Misgurnus anguillicaudatus (Cantor, 1824) in Central Europe. Knowl Manage Aquat Ecosyst 418:31–35CrossRefGoogle Scholar
  6. Boeger WA, Kritsky DC, Pie MR (2003) Context of diversification of the viviparous Gyrodactylidae (Platyhelminthes, Monogenoidea). Zool Scr 32:437–448CrossRefGoogle Scholar
  7. Chang AL, Grossman JD, Spezio TS, Weiskel HW, Blum JC, Burt JW, Muir AA, Piovia-Scott J, Veblen KE, Grosholz ED (2009) Tackling aquatic invasions: risks and opportunities for the aquarium fish industry. Biol Invasions 11:773–785CrossRefGoogle Scholar
  8. Collins JP, Crump ML III (2009) Extinction in our times: global amphibian decline. Oxford University Press, OxfordGoogle Scholar
  9. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science 287:443–449PubMedCrossRefGoogle Scholar
  10. Dove AD, Ernst I (1998) Concurrent invaders—four exotic species of Monogenea now established on exotic freshwater fishes in Australia. Int J Parasitol 28:1755–1764PubMedCrossRefPubMedCentralGoogle Scholar
  11. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acid Res 32:1792–1797PubMedCrossRefPubMedCentralGoogle Scholar
  12. Ergens R (1985) Order Gyrodactylidea Bychowsky, 1937. In: Bauer ON (ed) Key to parasites of freshwater fish of the fauna of the USSR, vol 2. Parasitic metazoans. Nauka, Leningrad, pp 269–347 (In Russian)Google Scholar
  13. Fausch K (2007) Introduction, establishment and effects of non-native salmonids: considering the risk of rainbow trout invasion in the United Kingdom. J Fish Biol 71:1–32CrossRefGoogle Scholar
  14. Fisher MC, Ghosh P, Shelton JMG et al (2018) Development and worldwide use of non-lethal, and minimal population-level impact, protocols for the isolation of amphibian chytrid fungi. Sci Rep 8:7772.  https://doi.org/10.1038/s41598-018-24472-2 CrossRefPubMedPubMedCentralGoogle Scholar
  15. García-Vásquez A, Razo-Mendivil U, Rubio-Godoy M (2015) Morphological and molecular description of eight new species of Gyrodactylus von Nordmann, 1832 (Platyhelminthes: Monogenea) from poeciliid fishes, collected in their natural distribution range in the Gulf of Mexico slope, Mexico. Parasitol Res 114:3337–3355PubMedCrossRefPubMedCentralGoogle Scholar
  16. Gilmore SR, Cone DK, Lowe G, King SK, Jones SRM, Abbott CL (2012) Molecular phylogeny of Gyrodactylus (Monogenea) parasitizing fishes in fresh water, estuarine, and marine habitats in Canada. Can J Zool 90:776–786CrossRefGoogle Scholar
  17. Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474PubMedCrossRefPubMedCentralGoogle Scholar
  18. Harris PD, Shinn A, Cable J, Bakke TA (2004) Nominal species of the genus Gyrodactylus von Nordmann 1832 (Monogenea: Gyrodactylidae), with a list of principal host species. Syst Parasitol 59:1–27PubMedCrossRefPubMedCentralGoogle Scholar
  19. Hukuda M (1940) Three new species of Japanese Gyrodactylus (Trematoda). J Chosen Nat History Soc 7:37–44Google Scholar
  20. Huyse T, Vanhove MP, Mombaerts M, Volckaert FA, Verreycken H (2015) Parasite introduction with an invasive goby in Belgium: double trouble? Parasitol Res 114:2789–2793PubMedCrossRefPubMedCentralGoogle Scholar
  21. Ieshko E, Lebedeva D, Lumme J (2015) A new Gyrodactylus strain on brown trout (Salmo trutta) in Jänisjärvi, Russian Karelia, and a literature revision of salmonid parasites of the genus Gyrodactylus in North-Western Russia and adjacent areas. Acta Parasitol 60:75–84Google Scholar
  22. Johnsen BO, Jensen AJ (1991) The Gyrodactylus story in Norway. Aquaculture 98:289–302CrossRefGoogle Scholar
  23. King SD, Cone DK, Mackley MP, Bentzen P (2013) Gyrodactylus laevisoides n. sp. (Monogenea: Gyrodactylidae) infecting northern redbelly dace Phoxinus eos Cope (Cyprinidae) from Nova Scotia, Canada. Syst Parasitol 86:285–291PubMedCrossRefPubMedCentralGoogle Scholar
  24. Kottelat M (2012) Conspectus cobitidum: an inventory of the loaches of the world (Teleostei: Cypriniformes: Cobitoidei). Raffles Bull Zool 26:1–199Google Scholar
  25. Kuusela J, Ziętara M, Lumme J (2008) Description of three new European cryptic species of Gyrodactylus Nordmann, 1832 supported by nuclear and mitochondrial phylogenetic characterization. Acta Parasitol 53:120–126CrossRefGoogle Scholar
  26. LeBlanc J, Hansen H, Burt M, Cone D (2006) Gyrodactylus neili n. sp. (Monogenea: Gyrodactylidae), a parasite of chain pickerel Esox niger Lesueur (Esocidae) from freshwaters of New Brunswick, Canada. Syst Parasitol 65:43–48PubMedCrossRefPubMedCentralGoogle Scholar
  27. Lee JJ (2014) Do you know where your aquarium fish come from. National Geographic, Washington, DCGoogle Scholar
  28. Lindenstrøm T, Collins CN, Bresciani J, Cunningham CO, Buchmann K (2003) Characterization of Gyrodactylus salaris variant: infection biology, morphology and molecular genetics. Parasitology 127:165–177PubMedCrossRefPubMedCentralGoogle Scholar
  29. Lumme J, Ozerov M, Veselov A, Primmer CR (2015) The formation of landlocked populations of Atlantic salmon. In: Vladiĉ T, Petersson E (eds) Evolutionary biology of the Atlantic salmon. CRC Press, Boca Raton, pp 26–43CrossRefGoogle Scholar
  30. Lumme J, Anttila P, Rintamäki P, Koski P, Romakkaniemi A (2016a) Genetic gradient of a host-parasite pair persisted ten years against physical mobility: Baltic Salmo salar vs. Gyrodactylus salaris. Infect Genet Evol 45:33–39PubMedCrossRefPubMedCentralGoogle Scholar
  31. Lumme J, Mäkinen H, Ermolenko AV, Gregg JL, Ziętara MS (2016b) Displaced phylogeographic signals from Gyrodactylus arcuatus, a parasite of the three-spined stickleback Gasterosteus aculeatus, suggest freshwater glacial refugia in Europe. Int J Parasitol 46:545–554PubMedCrossRefPubMedCentralGoogle Scholar
  32. Maceda-Veiga A, Cable J (2019) Diseased fish in the freshwater trade: from retailers to private aquarists. Dis Aquat Organ 132:157–162PubMedCrossRefPubMedCentralGoogle Scholar
  33. Malmberg G (1970) The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Ark Zool 23:1–235Google Scholar
  34. Martel A, Spitzen-van der Sluijs A, Blooi M, Bert W, Ducatelle R, Fisher MC, Woeltjes A, Bosman W, Chiers K, Bossuyt F, Pasmans F (2013) Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proc Natl Acad USA 110:15325–15329CrossRefGoogle Scholar
  35. Mata-López R, García-Prieto L, León-Règagnon V (2010) Helminths of the American bullfrog, Lithobates catesbeianus (Shaw, 1802), from Pawnee Lake, Lancaster, Nebraska, USA with a checklist of its helminth parasites. Zootaxa 2544:1–53CrossRefGoogle Scholar
  36. Matĕjusová I, Gelnar M, McBeath AJ, Collins CM, Cunningham CO (2001) Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). Int J Parasitol 31:738–745PubMedCrossRefPubMedCentralGoogle Scholar
  37. Matĕjusová I, Gelnar M, Verneau O, Cunningham CO, Littlewood DTJ (2003) Molecular phylogenetic analysis of the genus Gyrodactylus (Platyhelminthes: Monogenea) inferred from rDNA ITS region: subgenera versus species groups. Parasitology 127:603–611PubMedCrossRefPubMedCentralGoogle Scholar
  38. Mendoza-Palmero CA, Blasco-Costa I, de Leon GPP (2019) Morphological and molecular characterisation of a new species of Gyrodactylus von Nordmann, 1832 (Monogenoidea: Gyrodactylidae) of cichlid fishes (Perciformes) from Mexico. Parasitol Int 70:102–111PubMedCrossRefPubMedCentralGoogle Scholar
  39. Nieto NC, Camann MA, Foley JE, Reiss JO (2007) Disease associated with integumentary and cloacal parasites in tadpoles of northern red-legged frog Rana aurora aurora. Dis Aquat Organ 78:61–71PubMedCrossRefPubMedCentralGoogle Scholar
  40. O’Hanlon SJ, Rieux A, Farrer RA et al (2018) Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360:621–627PubMedPubMedCentralCrossRefGoogle Scholar
  41. Ondračková M, Matějusová I, Grabowska J (2012) Introduction of Gyrodactylus perccotti (Monogenea) into Europe on its invasive fish host, Amur sleeper (Perccottus glenii, Dybowski 1877). Helminthologia 49:21–26CrossRefGoogle Scholar
  42. Paetow L, Cone DK, Huyse T, McLaughlin JD, Marcogliese DJ (2009) Morphology and molecular taxonomy of Gyrodactylus jennyae n. sp. (Monogenea) from tadpoles of captive Rana catesbeiana Shaw (Anura), with a review of the species of Gyrodactylus Nordmann, 1832 parasitising amphibians. Syst Parasitol 73:219–227PubMedCrossRefPubMedCentralGoogle Scholar
  43. Paetow LJ, McLaughlin JD, Pauli PD, Marcogliese DJ (2013) Mortality of American bullfrog tadpoles Lithobates catesbeianus infected by Gyrodactylus jennyae and experimentally exposed to Batrachochytrium dendrobatidis. J Aquat Anim Health 25:15–26PubMedCrossRefPubMedCentralGoogle Scholar
  44. Paladini G (2012) Aspects of systematics and host specificity for Gyrodactylus species in aquaculture. Ph.D. Thesis, University of Stirling, ScotlandGoogle Scholar
  45. Perkins EM, Donnellan SC, Bertozzi T, Chisholm LA, Whittington ID (2009) Looks can deceive: molecular phylogeny of a family of flatworm ectoparasites (Monogenea: Capsalidae) does not reflect current morphological classification. Mol Phylogenet Evol 52:705–714PubMedCrossRefPubMedCentralGoogle Scholar
  46. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288CrossRefGoogle Scholar
  47. Pinder A, Gozlan R, Britton J (2005) Dispersal of the invasive topmouth gudgeon, Pseudorasbora parva in the UK: a vector for an emergent infectious disease. Fish Manage Ecol 12:411–414CrossRefGoogle Scholar
  48. Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman B, Schander C, Sundberg P, Thollesson M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol Phylogenet Evol 48:369–371PubMedCrossRefPubMedCentralGoogle Scholar
  49. Pounds JA, Masters KL (2009) Amphibian mystery misread. Nature 462:38–39CrossRefGoogle Scholar
  50. Přikrylová I, Blažek R, Vanhove MP (2012) An overview of the Gyrodactylus (Monogenea: Gyrodactylidae) species parasitizing African catfishes, and their morphological and molecular diversity. Parasitol Res 110:1185–1200PubMedCrossRefPubMedCentralGoogle Scholar
  51. Pugachev ON, Gerasev PI, Gussev AV, Ergens R, Khotenowsky I (2009) Guide to Monogenoidea of freshwater fish of Palearctic and Amur regions. Ledizione-Ledi Publishing, Milan, p 564Google Scholar
  52. Ragan MA, Goggin CL, Cawthorn RJ, Cerenius L, Jamieson AV, Plourde SM, Rand TG, Söderhäll K, Gutell RR (1996) A novel clade of protistan parasites near the animal-fungal divergence. Proc Natl Acad Sci 93:11907–11912PubMedCrossRefPubMedCentralGoogle Scholar
  53. Rokicka M, Lumme J, Ziętara MS (2007) Identification of Gyrodactylus ectoparasites in Polish salmonid farms by PCR-RFLP of the nuclear ITS segment of ribosomal DNA (Monogenea: Gyrodactylidae). Acta Parasitol 52:185–195CrossRefGoogle Scholar
  54. Rokicka M, Lumme J, Ziętara MS (2009) Two new Antarctic Gyrodactylus species (Monogenoidea): description and phylogenetic characterization. J Parasitol 95:1112–1119PubMedCrossRefPubMedCentralGoogle Scholar
  55. Rubio-Godoy M, Paladini G, Freeman MA, Garcia-Vasquez A, Shinn AP (2012) Morphological and molecular characterisation of Gyrodactylus salmonis (Platyhelminthes, Monogenea) isolates collected in Mexico from rainbow trout (Oncorhynchus mykiss Walbaum). Vet Parasitol 186:289–300PubMedCrossRefPubMedCentralGoogle Scholar
  56. Spikmans F, van Tongeren T, van Alen TA, van der Velde G, Op den Camp HJM (2013) High prevalence of the parasite Sphaerothecum destruens in the invasive topmouth gudgeon Pseudorasbora parva in the Netherlands, a potential threat to native freshwater fish. Aquat Invasions 8:355–360CrossRefGoogle Scholar
  57. Storfer A (2003) Amphibian declines: future directions. Divers Distrib 9:151–163CrossRefGoogle Scholar
  58. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630PubMedCrossRefPubMedCentralGoogle Scholar
  59. Verneau O, Palacios C, Platt T, Alday M, Billard E, Allienne J, Basso C, Du Preez L (2011) Invasive species threat: parasite phylogenetics reveals patterns and processes of host-switching between non-native and native captive freshwater turtles. Parasitology 138:1778–1792PubMedCrossRefPubMedCentralGoogle Scholar
  60. Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, Cook D, Webb R, Alford RA, Skerratt LF, Speare R (2009) Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326:582–585PubMedCrossRefPubMedCentralGoogle Scholar
  61. Wells S (2014) Monitoring feral oriental weatherfish infestations in New York State. Am Curr Summer 2014:18–21Google Scholar
  62. You P, Easy R, Cone D (2008) Gyrodactylus parvae n. sp. (Monogenea) from the fins and body surface of Pseudorasbora parva (Cyprinidae) in central China. Comp Parasitol 75:28–32CrossRefGoogle Scholar
  63. You P, Guo Z, King SD, Cone DK (2010) A new Gyrodactylid species from Cobitis granoei (Rendahl) (Cobitidae) in Central China. J Parasitol 96:897–899PubMedCrossRefPubMedCentralGoogle Scholar
  64. Ziętara MS, Lumme J (2002) Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea: Gyrodactylidae). Evolution 56:2445–2458PubMedCrossRefPubMedCentralGoogle Scholar
  65. Ziętara MS, Lumme J (2003) The crossroads of molecular, typological and biological species concepts: two new species of Gyrodactylus Nordmann, 1832 (Monogenea, Gyrodactylidae). Syst Parasitol 55:39–52PubMedCrossRefPubMedCentralGoogle Scholar
  66. Ziętara M, Lumme J (2004) Comparison of molecular phylogeny and morphological systematics in fish parasite genus Gyrodactylus Nordmann, 1832 (Monogenea, Gyrodactylidae). Zool Poloniae 49:5–28Google Scholar
  67. Ziętara MS, Huyse T, Lumme J, Volckaert FA (2002) Deep divergence among subgenera of Gyrodactylus inferred from rDNA ITS region. Parasitology 124:39–52PubMedCrossRefPubMedCentralGoogle Scholar
  68. Ziętara MS, Kuusela J, Lumme J (2006) Escape from an evolutionary dead-end: a triploid clone of Gyrodactylus salaris is able to revert to sex and switch host (Platyhelminthes, Monogenea, Gyrodactylidae). Hereditas 143:86–92CrossRefGoogle Scholar
  69. Ziętara MS, Kuusela J, Veselov AJe, Lumme J (2008) Molecular faunistics of accidental infections of Gyrodactylus Nordmann, 1832 (Monogenea) parasitic on salmon Salmo salar L. and brown trout Salmo trutta L. in NW Russia. Syst Parasitol 69:123–135PubMedCrossRefPubMedCentralGoogle Scholar
  70. Ziętara MS, Rokicka M, Stojanovski S, Lumme J (2010) Introgression of distant mitochondria into the genome of Gyrodactylus salaris: Nuclear and mitochondrial markers are necessary to identify parasite strains. Acta Parasitol 55:20–28CrossRefGoogle Scholar
  71. Ziętara MS, Lebedeva D, Muñoz G, Lumme J (2012) A monogenean fish parasite, Gyrodactylus chileani n. sp., belonging to a novel marine species lineage found in the South-Eastern Pacific and the Mediterranean and North Seas. Syst Parasitol 83:159–167PubMedPubMedCentralCrossRefGoogle Scholar
  72. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415PubMedPubMedCentralCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Biology Department and Biological Field StationState University of New York College at OneontaOneontaUSA
  2. 2.Region 4 Bureau of FisheriesNew York State Department of Environmental ConservationStamfordUSA
  3. 3.Institute of Biology and Soil ScienceVladivostokRussia
  4. 4.Department of Molecular Evolution, Faculty of BiologyUniversity of GdańskGdańskPoland
  5. 5.Ecology and GeneticsUniversity of OuluOuluFinland

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