Parasitology Research

, Volume 118, Issue 1, pp 159–167 | Cite as

Co-existence of Myxobolus spp. (Myxozoa) in gray mullet (Mugil cephalus) juveniles from the Mediterranean Sea

  • Galit SharonEmail author
  • Michal Ucko
  • Ben Tamir
  • Arik Diamant
Fish Parasitology - Original Paper


Gray mullet (Mugilidae) occur in all seas and are farmed widely around the world, and thus, the risk of their parasites spreading through transport of aquaculture seed is a serious concern. Among others, gray mullets typically host a diversity of myxosporeans, a group in which spore morphometrics of genera has been consistently shown to be inadequate for determination of species. In this study, we investigated Myxobolus Bütschli 1882 (Myxosporea) species found in two fingerling stocks of Mugil cephalus caught in the wild off the coasts of the eastern (Israel) and western (Spain) Mediterranean. Although we observed similar morphological features, significant dissimilarities in spore size and differences in Myxobolus species SSU rDNA sequences were noted. Genetic analyses demonstrated that multiple Myxobolus species, some with SSU rDNA sequences new to GenBank, infected the stock from Spain. In addition, Myxobolus DNA was found associated with several types of host tissue (gill, tail, and internal organs), and sequence analyses indicated that multiple species of Myxobolus were also present, sometimes in different tissues from the same fish. The results suggest that the gray mullets supported a collection of several different Myxobolus species with similar morphology.


Fish Parasite Myxosporea Aquaculture 



  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410CrossRefGoogle Scholar
  2. Andree KB, Szekely C, Molnár K, Gresoviac SJ, Hedrick RP (1999) Relationships among members of the genus Myxobolus (Myxozoa; Bivalvulida) based on small subunit ribosomal DNA sequences. J Parasitol 85:68–74CrossRefGoogle Scholar
  3. Atkinson SD, Bartošová-Sojková P, Whipps CM, Bartholomew JL (2015) Approaches for characterising Myxozoan species. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development (part I). Springer International Publishing, Cham, pp 111–123CrossRefGoogle Scholar
  4. Bahri S, Marques A (1996) Myxosporean parasites of the genus Myxobolus from Mugil cephalus in Ichkeul lagoon, Tunisia: description of two new species. Dis Aquat Org 27:115–122CrossRefGoogle Scholar
  5. Bahri S, Andree KB, Hedrick RP (2003) Morphological and phylogenetic studies of marine Myxobolus spp. from mullet in Ichkeul Lake, Tunisia. J Eukaryot Microbiol 50(6):463–470CrossRefGoogle Scholar
  6. Bartholomew JL, Reno PW (2002) The history and dissemination of whirling disease. In: American fisheries society symposium. American fisheries Society, pp 3–24Google Scholar
  7. Brown LL, Bruno DW (2006) Infectious diseases of Coldwater fish in fresh water. In: Woo PTK, Bruno DW, Lim LHS (eds) Diseases and disorders of finfish in cage culture. CAB International, Wallingford, pp 107–170Google Scholar
  8. Carriero MM, Adriano EA, Silva MRM, Ceccarelli PS, Maia AAM (2013) Molecular phylogeny of the Myxobolus and Henneguya genera with several new South American species. PLoS One 8(9):e73713CrossRefGoogle Scholar
  9. Cech G, Molnár K, Székely C (2012) Molecular genetic studies on morphologically indistinguishable Myxobolus spp. infecting cyprinid fishes, with the description of three new species, M. alvarezae sp. nov., M. sitjae sp. nov. and M. eirasianus sp. nov. Acta Protozool 57(4):354–366Google Scholar
  10. Diamant A, Ucko M, Paperna I, Colorni A, Lipshitz A (2005) Kudoa iwatai (Myxosporea: Multivavulida) in wild and cultured fish in the Red Sea: Redescription and molecular phylogeny. J Parasitol 91(5):1175–1189CrossRefGoogle Scholar
  11. Eiras JC, Molnár K, Lu YS (2005) Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 61:1–46CrossRefGoogle Scholar
  12. Eiras JC, Abreu PC, Robaldo R, Pereira Junior J (2007) Myxobolus platanus n. sp. (Myxosporea, Myxobolidae), a parasite of Mugil platanus Gunther, 1880 (Osteichthyes, Mugilidae) from Lagoa dos Patos, RS, Brasil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 59(4):895–898CrossRefGoogle Scholar
  13. Eiras JC, Zhang J, Molnar K (2014) Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea, Myxobolidae) described between 2005 and 2013. Syst Parasitol 88:11–36CrossRefGoogle Scholar
  14. Ferguson JWH (2002) On the use of genetic divergence for identifying species. Biol J Linn Soc 75(4):509–516CrossRefGoogle Scholar
  15. Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534CrossRefGoogle Scholar
  16. Hallett SL, Diamant A (2001) Ultrastructure and small-subunit ribosomal DNA sequence of Henneguya lesteri n.sp. (Myxosporea), a parasite of sand whiting Sillago analis (Sillaginidae) from the coast of Queensland, Australia. Dis Aquat Org 46:197–212CrossRefGoogle Scholar
  17. Hedrick RP, Adkison MA, El-Matbouli M, MacConnell E (1998) Whirling disease: re-emergence among wild trout. Immunol Rev 166(1):365–376CrossRefGoogle Scholar
  18. Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66(4):411–453CrossRefGoogle Scholar
  19. Hoffman GL (1990) Myxobolus cerebralis, a worldwide cause of salmonid whirling disease. J Aquat Anim Health 2(1):30–37CrossRefGoogle Scholar
  20. Kent ML, Margolis L, Corliss JO (1994) The demise of class protists: taxonomic and nomenclatural revision proposed for the protest phylum Myxozoa Grassé, 1970. Can J Zool 72:932–937CrossRefGoogle Scholar
  21. Kent ML, Andree KB, Bartholomewc JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJG, Longshaw M, Palenzeula O, Siddall ME, Xiao C (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48(4):395–413CrossRefGoogle Scholar
  22. Kim WS, Kim JH, Oh MJ (2013a) Morphologic and genetic evidence for mixed infection with two Myxobolus species (Myxozoa: Myxobolidae) in gray mullets, Mugil cephalus, from Korean waters. Korean J Parasitol 51(3):369–373CrossRefGoogle Scholar
  23. Kim WS, Kim JH, Jang MS, Jung SJ, Oh MJ (2013b) Infection of wild mullet (Mugil cephalus) with Myxobolus episquamalis in Korea. Parasitology Research 112:447–451CrossRefGoogle Scholar
  24. Lafferty KD, Harvell CD, Conrad JM, Friedman CS, Kent ML, Kuris AM, Saksida SM (2015) Infectious diseases affect marine fisheries and aquaculture economics. Annu Rev Mar Sci 7(1):471–496CrossRefGoogle Scholar
  25. Lane HS, Booth K, Pande A, Jones JB (2015) First report of the myxozoan parasite Myxobolus episquamalis infecting grey mullet (Mugil cephalus) from New Zealand. N Z J Mar Freshw Res 49(2):173–177CrossRefGoogle Scholar
  26. Liu Y, Whipps CM, Gu ZM, Zeng LB (2010) Myxobolus turpisrotundus (Myxosporea: Bivalvulida) spores with caudal appendages: investigating the validity of the genus Henneguya with morphological and molecular evidence. Parasitol Res 107:699–706CrossRefGoogle Scholar
  27. Lom J, Dyková I (1992) Protozoan parasites of fishes. Development in aquaculture and fisheries sciences, Elsevier, 26: 160–235Google Scholar
  28. Lom J, Dyková I (1995) Note on the ultrastructure of two myxosporean (Myxozoa) species, Zschokkella pleomorpha and Ortholinea fluviatilis. Folia Parasitol 43:189–202Google Scholar
  29. Maíllo-Bellón PA, Marques A, Graciaroyo MP (2011) Myxosporean infection of grey mullet in the Ebro Delta: identification and ultrastructure of Myxobolus ichkeulensis Bahri & Marques, 1996. Infecting the gills of Mugil cephalus L. Acta Protozool 50:67–71Google Scholar
  30. Merella P, Garippa G (2001) Metazoan parasites of grey mullets (Teleostea: Mugilidae) from the Mistras lagoon (Sardinia, western Mediterranean). Sci Mar 65(3):201–206CrossRefGoogle Scholar
  31. Montero FE, Cuadrado M, Padros F, Crespo S, Raga JA (2007) Cryptocaryon irritans and Enteromyxum leei, two threats for the culture of Diplodus puntazzo in the Mediterranean. Bull Eur Assoc Fish Pathol 27(6):242–249Google Scholar
  32. Pruginin Y, Shilo S, Mires D (1975) Grey mullet: a component in polyculture in Israel. Aquaculture 5:291–298CrossRefGoogle Scholar
  33. Rigos G, Christophilogiannis P, Yiagnisi M, Andriopoulou A, Koutsodimou M, Nengas I, Alexis M (1999) Myxosporean infections in Greek Mariculture. Aquaculture International 7(5):361–364CrossRefGoogle Scholar
  34. Salim KY, Desser SS (2000) Descriptions and phylogenetic systematics of Myxobolus spp. from cyprinids in Algonquin Park, Ontario. J Eukaryot Microbiol 47:309–318CrossRefGoogle Scholar
  35. Shvedko MB, Aseev NL (2008) Parasites on mullets from southern Far East Russia. In Proceedings of the Scientific Conference on the Current Status of Aquatic Bio Resources, Vladivostok pp 316–320Google Scholar
  36. Siddall EM, Martin SD, Bridge D, Desser SS, Cone KD (1995) The demise of a phylum of protists: phylogeny of Myxozoa and other parasitic Cnidaria. J Parasitol 81(6):961–967CrossRefGoogle Scholar
  37. Székely CS, Hallett SL, Atkinson SD, Molnár K (2009) Complete life cycle of Myxobolus rotundus (Myxosporea: Myxobolidae), a gill myxozoan of common bream Abramis brama. Dis Aquat Org 85:147–155CrossRefGoogle Scholar
  38. Yurakhno V, Ovcharenko MO (2014) Study of Myxosporea (Myxozoa), infecting worldwide mullets with description of a new species. Parasitol Res 113:3661–3674CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Galit Sharon
    • 1
    Email author
  • Michal Ucko
    • 1
  • Ben Tamir
    • 1
  • Arik Diamant
    • 1
  1. 1.Israel Oceanographic and Limnological Research, National Center for MaricultureEilatIsrael

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