Parasitology Research

, Volume 113, Issue 8, pp 2817–2825 | Cite as

Life cycles of three Myxobolus spp. from cyprinid fishes of Lake Balaton, Hungary involve triactinomyxon-type actinospores

  • Csaba Székely
  • Muhammad Hafiz Borkhanuddin
  • Gábor Cech
  • Olga Kelemen
  • Kálmán Molnár
Original Paper


A study on the actinosporean fauna of oligochaetes of Lake Balaton was carried out from 2009 to 2011. The morphology of actinosporean stages of myxosporeans obtained from oligochaetes was studied, and their 18S rDNA structure was analyzed by molecular biological methods. Three triactinomyxon types were released from the oligochaete Isochaetides michaelseni (Tubificidae). The sequences of Triactinomyxon type 1 proved to be identical with those of Myxobolus fundamentalis. The sequences of Triactinomyxon type 2 showed 99.9 % similarity to Myxobolus eryhtrophthalmi, while the sequences of Triactinomyxon type 3 showed a 99.9 % similarity to those of Myxobolus shaharomae. The life cycles of the above species, just like those of other species with a known life cycle, suggest that most Myxobolus spp. develop through triactinomyxon-type actinosporean stages.


Myxozoa Actinospores Developing stages Life cycle Lake Balaton Hungary 



The research was supported by the Hungarian Scientific Research Fund (OTKA) grant K 100132 and KTIA-AIK-12-1-2013-0017. The authors thank Györgyi Ostoros for her help with preparing the line drawings.


  1. Atkinson SD, Bartholomew JL (2009) Alternate spore stages of Myxobilatus gasterostei, a myxosporean parasite of three-spined sticklebacks (Gasterosteus aculeatus) and oligochaetes (Nais communis. Parasitol Res 104:1173–1181PubMedCrossRefGoogle Scholar
  2. Barta JR, Martin DS, Libetator PA, Dashkevicz M, Anderson JW, Feighner SD, Elbrecht A, Perkins-Barrow A, Jenkins MC, Danforth HD, Ruff MD, Profous-Juchelka H (1997) Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol 83:262–271PubMedCrossRefGoogle Scholar
  3. Caffara M, Raimondi E, Florio D, Marcer F, Quaglio F, Fioravanti ML (2009) The life cycle of Myxobolus lentisuturalis (Myxozoa: Myxobolidae), from goldfish (Carassius auratus auratus), involves a Raabeia-type actinospore. Folia Parasitol 56:6–12PubMedCrossRefGoogle Scholar
  4. Canning EU, Okamura B (2004) Biodiversity and evolution of the myxozoa. Adv Parasitol 56:43–131PubMedCrossRefGoogle Scholar
  5. Eiras JC, Molnár K, Lu YS (2005) Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 61:1–46PubMedCrossRefGoogle Scholar
  6. El-Mansy A, Molnár K (1997a) Extrapiscine development of Myxobolus drjagini Akhmerov, 1954 (Myxosporea: Myxobolidae) in oligochaete alternate hosts. Acta Vet Hung 45:427–438PubMedGoogle Scholar
  7. El-Mansy A, Molnár K (1997b) Development of Myxobolus hungaricus (Myxosporea: Myxobolidae) in oligochaete alternate hosts. Dis Aquat Org 31:227–232CrossRefGoogle Scholar
  8. El-Mansy A, Molnár K, Székely C (1998a) Development of Myxobolus portucalensis Saraiva & Molnár, 1990 (Myxosporea: Myxobolidae) in the oligochaete Tubifex tubifex (Müller). Syst Parasitol 41:95–103CrossRefGoogle Scholar
  9. El-Mansy A, Székely C, Molnár K (1998b) Studies on the occurrence of actinosporean stages of fish myxosporeans in a fish farm of Hungary, with the description of triactinomyxon, raabeia, aurantiactinomyxon and neoactinomyxon types. Acta Vet Hung 466:259–284Google Scholar
  10. El-Mansy A, Székely C, Molnár K (1998c) Studies on the occurrence of actinosporean stages of myxosporeans in Lake Balaton, Hungary, with the description of triactinomyxon, raabeia, and aurantiactinomyxon types. Acta Vet Hung 46:437–450PubMedGoogle Scholar
  11. El-Matbouli M, Hoffmann RW (1989) Experimental transmission of two Myxobolus spp. developing by sporogeny via tubificid worms. Parasitol Res 75:461–464PubMedCrossRefGoogle Scholar
  12. El-Matbouli M, Hoffmann RW (1993) Myxobolus carassii Klokaceva, 1914 also requires an aquatic oligochaete, Tubifex tubifex as intermediate host in its life cycle. Bull Eur Assoc Fish Pathol 13:189–192Google Scholar
  13. Eszterbauer E, Székely C (2004) Molecular phylogeny of the kidney parasitic Sphaerospora renicola from common carp (Cyprinus carpio) and Sphaerospora sp. from goldfish (Carassius auratus auratus). Acta Vet Hung 52:469–478PubMedCrossRefGoogle Scholar
  14. Eszterbauer E, Székely C, Molnár K, Baska F (2000) Development of Myxobolus bramae (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. J Fish Dis 23:19–25CrossRefGoogle Scholar
  15. Eszterbauer E, Marton S, Rácz OZ, Letenyei M, Molnár K (2006) Morphological and genetic differences among actinosporean stages of fish-parasitic myxosporeans (Myxozoa): difficulties of species identification. Syst Parasitol 65:97–114PubMedCrossRefGoogle Scholar
  16. Ferraguti M, Marotta R, Martin P (2002) The double sperm line in Isochaetides (Annelida, Clitellata, Tubificidae). Tissue Cell 34:305–314PubMedCrossRefGoogle Scholar
  17. 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 46:197–212PubMedCrossRefGoogle Scholar
  18. Hallett SL, Atkinson SD, El-Matbouli M (2002) Molecular characterization of two aurantiactinomyxon (Myxozoa) phenotypes reveals one genotype. J Fish Dis 25:627–631CrossRefGoogle Scholar
  19. Hallett SL, Atkinson SD, Erséus C, El-Matbouli M (2004) Molecular methods clarify morphometric variation in triactinomyxon spores (Myxozoa) released from different oligochaete hosts. Syst Parasitol 57:1–14PubMedCrossRefGoogle Scholar
  20. Hallett SL, Atkinson SD, Erséus C, El-Matbouli M (2005) Dissemination of triactinomyxons (Myxozoa) via oligochaetes used as live food for aquarium fishes. Dis Aquat Org 65:137–152PubMedCrossRefGoogle Scholar
  21. Holzer AS, Sommerville C, Wootten R (2004) Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. Int J Parasitol 34:1099–1111PubMedCrossRefGoogle Scholar
  22. Kallert DM, Eszterbauer E, El-Matbouli M, Erséus C, Haas W (2005) Life cycle studies of Myxobolus parviformis sp. n. (Myxozoa: Myxobolidae) from bream. Dis Aquat Org 66:233–243PubMedCrossRefGoogle Scholar
  23. Kent ML, Whitaker DJ, Margolis L (1993) Transmission of Myxobolus arcticus Pugachev and Khokhlov, 1979, via a triactinomyxon from the aquatic oligochaete Stylodrilus heringianus (Lumbriculidae). Can J Zool 71:1207–1211CrossRefGoogle Scholar
  24. Kent ML, Margolis L, Corliss JO (1994) The demise of a class of protists: taxonomic and nomenclatural revisions proposed for the protist phylum Myxozoa Grasse, 1970. Can J Zool 72:932–937CrossRefGoogle Scholar
  25. Køie M (2000) First record of an actinosporean (Myxozoa) in a marine polychaete annelid. J Parasitol 86:871–872PubMedCrossRefGoogle Scholar
  26. Køie M (2002) Spirorbid and serpulid polychaetes are candidates as invertebrate hosts for Myxozoa. Folia Parasitol 49:160–162PubMedCrossRefGoogle Scholar
  27. Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36PubMedCrossRefGoogle Scholar
  28. Lom J, Molnár K (1983) Myxobolus basilamellaris sp. n. (Myxozoa: Myxosporea), a parasite of the gills of common carp (Cyprinus carpio L.). Folia Parasitol 30:1–3Google Scholar
  29. Lom J, McGeorge J, Feist SW, Morris D, Adams A (1997) Guidelines for the uniform characterisation of the actinosporean stages of the phylum Myxozoa. Dis Aquat Org 30:1–9CrossRefGoogle Scholar
  30. Molnár K (2000) Myxobolus species infecting the cartilaginous rays of the gill filaments in cyprinid fishes. Acta Parasitol 53:330–338CrossRefGoogle Scholar
  31. Molnár K, Székely C (1995) Parasitological survey of some important fish species of Lake Balaton. Parasit Hung 28:63–82Google Scholar
  32. Molnár K, El-Mansy A, Székely C, Baska F (1999) Development of Myxobolus dispar (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. Folia Parasitol 46:15–21Google Scholar
  33. Molnár K, Eszterbauer E, Székely C, Dán Á, Harrach B (2002) Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. J Fish Dis 25:643–652CrossRefGoogle Scholar
  34. Molnár K, Marton S, Eszterbauer E, Székely C (2007) Description of Myxobolus gayerae sp. n. and re-description of M. leuciscini infecting European chub from the Hungarian stretch of the river Danube. Dis Aquat Org 78:147–153PubMedCrossRefGoogle Scholar
  35. Molnár K, Cech G, Székely C (2008) Myxobolus species infecting the cartilaginous rays of the gill filaments in cyprinid fishes. Acta Parasitol 53:330–338CrossRefGoogle Scholar
  36. Molnár K, Eszterbauer E, Marton S, Cech G, Székely C (2009) Myxobolus erythrophthalmi sp. n. and Myxobolus shaharomae sp. n. (Myxozoa: Myxobolidae) from the internal organs of rudd, Scardinius erythrophthalmus (L.), and bleak, Alburnus alburnus (L.). J Fish Dis 32:219–231PubMedCrossRefGoogle Scholar
  37. Molnár K, Eszterbauer E, Marton S, Cech G, Székely C (2010) Differentiation of Myxobolus spp. (Myxozoa: Myxobolidae) infecting roach (Rutilus rutilus) in Hungary. Parasitol Res 107:1137–1150PubMedCrossRefGoogle Scholar
  38. Özer A, Wootten R, Shinn A (2002) Survey on actinosporean types (Myxozoa) belonging to seven collective groups found in a freshwater salmon farm in Northern Scotland. Folia Parasitol 51:199–207Google Scholar
  39. Rácz, OZ, Eszterbauer E, Molnár K, (2005) Hungactinomyxon, a new actinosporean type and collective group Myxozoa from Branchiura sowerbyi Beddard Oligochaeta. Systematic Parasitology 61(2):107–113Google Scholar
  40. Rácz OZ, Székely C, Molnár K (2004) Intraoligochaete development of Myxobolus intimus (Myxosporea: Myxobolidae), a gill myxosporean of the roach (Rutilus rutilus). Folia Parasitol 51:199–207PubMedCrossRefGoogle Scholar
  41. Rangel LF, Cech G, Székely C, Santos MJ (2011) A new actinospore type Unicapsulactinomyxon (Myxozoa), infecting the marine polychaete, Diopatra neapolitana (Polychaeta: Onuphidae) in the Aveiro Estuary (Portugal). Parasitol 138:698–712CrossRefGoogle Scholar
  42. Székely Cs, Molnár K (1997) Preliminary survey of the parasite fauna of some important fish species in the Upper-Reservoir of the Kis Balaton System. Parasit Hung 29–30:45–54Google Scholar
  43. Székely C, Molnár K, Eszterbauer E, Baska F (1999) Experimental detection of the actinospores of Myxobolus pseudodispar (Myxosporea: Myxobolidae) in oligochaete alternate hosts. Dis Aquat Org 38:219–224PubMedCrossRefGoogle Scholar
  44. Székely C, Molnár K, Rácz O (2001) Complete developmental cycle of Myxobolus pseudodispar (Gorbunova) (Myxosporea: Myxobolidae). J Fish Dis 21:461–468CrossRefGoogle Scholar
  45. Székely C, Rácz O, Molnár K, Eszterbauer E (2002) Development of Myxobolus macrocapsularis (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. Dis Aquat Org 48:117–123PubMedCrossRefGoogle Scholar
  46. Székely C, Hallett SL, Al-Samman A, Dayoub A (2007) First description of myxozoans from Syria: novel records of hexactinomyxon, triactinomyxon and endocapsa actinospore types. Dis Aquat Org 74:127–137PubMedCrossRefGoogle Scholar
  47. Székely C, 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 85:147–155PubMedCrossRefGoogle Scholar
  48. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRefGoogle Scholar
  49. Timm T (1999) A guide to the Estonian Annelida. Estonian Academy Publishers, Tartu-TallinnGoogle Scholar
  50. Urawa S (1994) Life cycle of Myxobolus arcticus, a myxosporean parasite of salmonid fishes. In Abstracts of International Symposium on Aquatic Animal Health, Seattle, Washington, September 4–8, 1994. W-10.3Google Scholar
  51. Urawa S, Freeman MA, Johnson SC, Jones SRM, Yokoyama H (2011) Geographical variation in spore morphology, gene sequences, and host specificity of Myxobolus arcticus (Myxozoa) infecting salmonid nerve tissues. Dis Aquat Org 96:229–237PubMedCrossRefGoogle Scholar
  52. Wolf K, Markiw ME (1984) Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 225:1449–1452PubMedCrossRefGoogle Scholar
  53. Xiao C, Desser SS (1998) Actinosporean stages of Myxozoan parasites of oligochaetes from Lake Sasajewun, Algonquin Park, Ontario: new forms of echinactomyxon, neoactinomyxum, aurantiactinomyxon, guyenotia, synactinomyxon and antonactinomyxon. J Parasitol 84:1010–1019PubMedCrossRefGoogle Scholar
  54. Yokoyama H, Ogawa K, Wakabayashi H (1991) A new collection method of actinosporeans. A probable infective stage of myxosporeans to fishes from tubificids and experimental infection of goldfish with the actinosporean, Raabeia sp. Fish Pathol 26:133–138CrossRefGoogle Scholar
  55. Yokoyama H, Ogawa K, Wakabayashi H (1995) Myxobolus cultus n. sp. (Myxosporea: Myxobolidae) in the goldfish Carassius auratus transformed from the actinosporean stage in the oligochaete Branchiura sowerbyi. J Parasitol 81:446–451PubMedCrossRefGoogle Scholar
  56. Yokoyama H, Grabner D, Shirakashi S (2012) Transmission Biology of the Myxozoa, Health and Environment in Aquaculture. Dr. Edmir Carvalho (Ed.), ISBN: 978-953-51-0497-1, In Tech, Available from:
  57. Zhai YH, Zhou L, Gui JF (2012) Identification and characterization of one novel type of Triactinospomyxon with short spore axis. Parasitol Res 110:2385–2393PubMedCrossRefGoogle Scholar
  58. Zhang JY, Yokoyama H, Wang JG, Li AH, Gong XN, Ryu-Hasegawa A, Iwashita M, Ogawa K (2010) Utilization of tissue habitats by Myxobolus wulii Landsberg & Lom, 1991 in different carp hosts and disease resistance in allogynogenetic gibel carp: redescription of M. wulii from China and Japan. J Fish Dis 33:57–68PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Csaba Székely
    • 1
  • Muhammad Hafiz Borkhanuddin
    • 1
    • 2
  • Gábor Cech
    • 1
  • Olga Kelemen
    • 1
  • Kálmán Molnár
    • 1
  1. 1.Institute for Veterinary Medical Research, Centre for Agricultural ResearchHungarian Academy of SciencesBudapestHungary
  2. 2.School of Marine Science and EnvironmentUniversiti Malaysia TerengganuTerengganuMalaysia

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