Skip to main content
Log in

Alien parasites on an alien fish species: monogeneans from the black bullhead Ameiurus melas (Siluriformes) in the Lake Srebarna Biosphere Reserve, Bulgaria, with the first record of Gyrodactylus nebulosus in the Palaearctic

  • Fish Parasitology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Black bullhead Ameiurus melas (Actinopterygii: Siluriformes) is an alien fish species of North American origin, which has expanded its invasive geographical range in Europe. In 2017–2019, 32 black bullhead specimens from the Lake Srebarna Biosphere Reserve, Bulgaria, were examined for monogenean parasites. Two species of monogeneans were recorded and identified on the basis of morphological and molecular data: Ligictaluridus pricei (Ancyrocephalidae), with prevalence 100% and intensity 2–32 (mean 13.3 ± 6.8), and Gyrodactylus nebulosus (Gyrodactylidae), with prevalence 72.0% and intensity 1–15 (mean 7.4 ± 4.3). Partial 18S rDNA and the ITS1 region of L. pricei were sequenced. For G. nebulosus, sequenced genes included the partial 18S rDNA and the entire ITS1–5.8S rDNA–ITS2 region as well as the mitochondrial COI gene. Both recorded monogenean species are specific parasites of North American ictalurid fishes and alien to Europe. The present study is the first record of L. pricei from Bulgaria and the first record of G. nebulosus from Europe and the Palaearctic Region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Beverley-Burton M (1984) Monogenea and Turbellaria. In: Margolis L, Kabata Z (eds) Guide to the Parasites of Fishes of Canada. Part I. (Canadian Special Publication of Fisheries and Aquatic Sciences 74). Department of Fisheries and Oceans, Ottawa, pp 5–209

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cone D, Abbott C, Gilmore S, Burt M (2010) A new genus and species of gyrodactylid (Monogenea) from Silver Hake, Merluccius bilinearis, in the Bay of Fundy, New Brunswick, Canada. J Parasitol 96:681–684

    Article  Google Scholar 

  • Copp GH, Tarkan AS, Masson G, Godard MJ, Koščo J, Kováč V, Novomeská A, Miranda R, Cucherousset J, Pedicillo G, Blackwell BG (2016) A review of growth and life-history traits of native and non-native European populations of black bullhead Ameiurus melas. Rev Fish Biol Fisheries 26:441–469

    Article  Google Scholar 

  • Dunn AM (2009) Parasites and biological invasions. Adv Parasitol 68:161–184

    Article  Google Scholar 

  • Dunn AM, Torchin ME, Hatcher MJ, Kotanen PM, Blumenthal DM, Byers JE, Coon CAC, Frankel VM, Holt RD, Hufbauer RA, Kanarek AR, Schierenbeck KA, Wolfe LM, Perkins SE (2012) Indirect effects of parasites in invasions. Funct Ecol 26:1262–1274

    Article  Google Scholar 

  • Easy RH (2019) Screening for Gyrodactylus nebulosus Kritsky and Mizelle, 1968 (Monogenea) on 0+ age Ameiurus nebulosus (Siluriformes) considered for commercial grow-out in southwestern Nova Scotia, Canada (unpublished). GenBank. https://www.ncbi.nlm.nih.gov/nuccore/MK863255.1

  • Froese R, Pauly D (Eds) (2019) FishBase. World Wide Web electronic publication. https://www.fishbase.org (08/2019)

  • Galli P, Stefani F, Zaccara S, Crosa G (2002) Occurrence of Monogenea in Italian freshwater fish (Po River basin). Parassitologia 44:189–197

    PubMed  CAS  Google Scholar 

  • 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 90:776–786

    Article  CAS  Google Scholar 

  • Gussev AV (1983) Methodology of collecting and processing specimens of monogeneans parasitic on fishes. Nauka, Leningrad (In Russian)

    Google Scholar 

  • Hardman M, Page LM (2003) Phylogenetic relationships among bullhead catfishes of the genus Ameiurus (Siluriformes: Ictaluridae). Copeia 2003:20–33

    Article  Google Scholar 

  • Hargis WJ (1953) Monogenetic trematodes of Westhampton Lake fishes. III. Part 1. Comparative morphology of the species encountered. J Parasitol 39:88–105

    Article  Google Scholar 

  • Hoffman GL (1999) Parasites of North American freshwater fishes, 2nd edn. Cornell University Press, Ithaca

    Google Scholar 

  • Huyse T, Malmberg G, Volckaert FAM (2004) Four new species of Gyrodactylus von Nordmann, 1832 (Monogenea, Gyrodactylidae) on gobiid fishes: combined DNA and morphological analyses. Syst Parasitol 59:103–120

    Article  Google Scholar 

  • Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056

    Article  CAS  Google Scholar 

  • Kiškaroly M (1988) Istraživanje parazitofaune riba slatkovodnih ribnjaka Bosne i Hercegovine i Monogeni trematodi 6. Veterinaria Sarajevo 37:199–210

    Google Scholar 

  • Klassen GJ, Beverley-Burton M (1985) Ligictaluridus Beverley-Burton, 1984 (Monogenea: Ancyrocephalidae) from catfishes (Siluriformes: Ictaluridae) in North America with redescriptions of the type species, Ligictaluridus pricei (Mueller, 1936), and three others. Can J Zool 63:715–727

    Article  Google Scholar 

  • Kritsky DC, Mizelle JD (1968) Studies on monogenetic trematodes XXXV. Some new and previously described North American species of Gyrodactylus. Am Midl Nat 79:205–215

    Article  Google Scholar 

  • Leis E, Easy R, Cone D (2018) Supplemental diagnosis of Gyrodactylus fairporti Van Cleave, 1921 (Monogenea) from 1 month old black bullhead (Ameiurus melas) in riverside pools in Wisconsin. Parasitol Res 117:1265–1269

    Article  Google Scholar 

  • Lumme J, Ziętara MS, Lebedeva D (2017) Ancient and modern genome shuffling: reticulate mitonuclear phylogeny of four related allopatric species of Gyrodactylus von Nordmann, 1832 (Monogenea: Gyrodactylidae), ectoparasites on the Eurasian minnow Phoxinus phoxinus (L) (Cyprinidae). Syst Parasitol 94:183–200

    Article  Google Scholar 

  • Malmberg G (1970) The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Ark Zool 23:1–237

    Google Scholar 

  • Matějusová I, Gelnar M, McBeath AJA, Collins CM, Cunningham CO (2001) Molecular markers for gyrodactylids (Gyrodactylidae: Monogenea) from five fish families (Teleostei). Int J Parasitol 31:738–745

    Article  Google Scholar 

  • Moravec F (2001) Checklist of the metazoan parasites of fishes of the Czech Republic and the Slovak Republic. Academia, Prague

    Google Scholar 

  • Pehlivanov L, Stefanov T, Todorov M, Kutsarov Y, Trichkova T (2016) First records of the black bullhead Ameiurus melas (Rafinesque, 1820) along the Bulgarian section of the Danube River. In: 41st International Association for Danube Research (IAD) Conference. Sibiu, Romania, pp 34–34

    Google Scholar 

  • Prost M (1973) Fish Monogenoidea of Poland II. Parasites of Ictalurus nebulosus (Le Sueur). Revision of genera Cleidodiscus Mueller, 1934 and Urocleidus Mueller, 1934. Acta Parasitol 21:315–326

    Google Scholar 

  • Rogers WA (1968) Eight new species of Gyrodactylus (Monogenea) from the southeastern US with redescriptions of G. fairporti Van Cleave, 1921, and G. cyprini Diarova, 1964. J Parasitol 54:490–495

    Article  Google Scholar 

  • 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(3):185–195

    Article  CAS  Google Scholar 

  • Rutkayová J, Biskup R, Harant R, Šlechta V, Koščo J (2013) Ameiurus melas (black bullhead): morphological characteristics of new introduced species and its comparison with Ameiurus nebulosus (brown bullhead). Rev Fish Biol Fisheries 23:51

    Article  Google Scholar 

  • Šimková A, Plaisance L, Matĕjusová I, Morand S, Verneau O (2003) Phylogenetic relationships of the Dactylogyridae Bychowsky, 1933 (Monogenea: Dactylogyridea): the need for the systematic revision of the Ancyrocephalinae Bychowsky, 1937. Syst Parasitol 54:1–11

    Article  Google Scholar 

  • Sinnappah ND, Lim L-HS, Rohde K, Tinsley R, Combes C, Verneau O (2001) A paedomorphic parasite associated with a neotenic amphibian host: phylogenetic evidence suggests a revised systematic position for Sphyranuridae within anuran and turtle polystomatoineans. Mol Phylogenet Evol 18:189–201

    Article  CAS  Google Scholar 

  • Welcomme RL (1988) International introductions of inland aquatic species. FAO Fish Tech Pap 294

  • Williams BD, Schrank B, Huynh C, Shownkeen R, Waterston RH (1992) A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence–tagged sites. Genetics 131:609–624

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ziętara MS, Arndt A, Geets A, Hellemans B, Volckaert FAM (2000) The nuclear rDNA region of Gyrodactylus arcuatus and G. branchicus (Monogenea: Gyrodactylidae). J Parasitol 86:1368–1373

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to our colleagues Dr. Stefan Kazakov and Prof. Valko Biserkov for their assistance in providing some fish individuals for examination, and to Dr. Borislav Stoyanov for useful suggestions in the course of the present study. This study in the Srebarna Lake Biosphere Reserve was carried out with permission of the Ministry of Environment and Waters of the Republic of Bulgaria, nos. NSZP–442/16.08.2018 NSZP–54/14.02.2019 and NSZP–253/17.05.2019.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Boyko B. Georgiev.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The authors carefully reviewed the ethical standards of the journal and hereby certify that the procedures used with the investigated species comply fully with those standards. The methods used in the current study were approved by the Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences.

Additional information

Section Editor: Stephen A. Bullard

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vancheva, N., Bobeva, A., Pehlivanov, L. et al. Alien parasites on an alien fish species: monogeneans from the black bullhead Ameiurus melas (Siluriformes) in the Lake Srebarna Biosphere Reserve, Bulgaria, with the first record of Gyrodactylus nebulosus in the Palaearctic. Parasitol Res 119, 2105–2112 (2020). https://doi.org/10.1007/s00436-020-06699-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-020-06699-z

Keywords

Navigation