Parasitology Research

, Volume 114, Issue 1, pp 37–45 | Cite as

Thelohanellus wangi n. sp. (Myxozoa, Myxosporea), a new gill parasite of allogynogenetic gibel carp (Carassius auratus gibelio Bloch) in China, causing severe gill myxosporidiosis

  • S. Yuan
  • B. W. Xi
  • J. G. Wang
  • J. Xie
  • J. Y. Zhang
Original Paper


We describe here a new myxozoan, Thelohanellus wangi n. sp., infecting the allogynogenetic gibel carp, Carassius auratus gibelio (Bloch), in a fry nursery farm in Jiangsu Province, China. Polysporous gray white round or ovoid plasmodia, 500–1,500 μm in size, were found exclusively in the gill filaments. The diagnostic characteristics of the myxospores are as follows: spore melon seed shaped in frontal view with smooth surface and asymmetrical valves; convex-shaped in sutural view with straight or slightly bent and thick sutural line, averaging 20.2 (16.5–22.3) × 9.9 (9.1–10.8) × 9.3 μm (8.2–10.4) in size; and one elliptical polar capsules with subulate anterior end and round posterior end, averaging 10.1 (8.4–11.2) × 6.5 μm (6.1–7.0) in size. Polar filaments coil six to seven turns and are slightly oblique to the longitudinal axis of the polar capsule. An elongate melon seed-shaped mucus envelope surrounds almost completely the spore, but with largest distance in posterior end between spore valve and mucus envelope. Granular sporoplasm contains two slightly oval nuclei, and no iodinophilous vacuole is observed. Histopathological analysis showed that the plasmodia embedded in the gill filaments and occasionally extended into the connective tissue of the gill arch. No significant inflammatory responses were provoked by the infection. The development of parasite is asynchronous, with mature spores centrally locating and trophozoites and pre-sporogonic stages peripherally locating within the plasmodia. Overall prevalence was 74 % (37/50). Infection intensity was usually high, with about 10–30 cysts per fish. Phylogenetical analysis shows that T. wangi n. sp. is most closely related to several Thelohanellus species infecting cyprinid fish and formed a Thelohanellus clade based on the ribosomal DNA data. The cysts of this myxosporean were only found from fry seed with body length below 7 cm, generally from late April to early June when the fry fish of allogynogenetic gibel carp were nursed in the epizootic areas.


Thelohanellus wangi n. sp. Allogynogenetic gibel carp Histopathology Morphology Phylogeny 



The present work was financially supported by the Jiangsu Province Fund of Sciences (BK2012240, BK2011182), Special Fund for Basic Scientific Research of Central Institutes, FFRC (6-115080), Young Scientist Award of the Knowledge Innovation Program of the Chinese Academy of Sciences, and Huai’an Science and Technology Bureau (SN12099, SN13095).


  1. Abdel-Ghaffar F, Morsy K, Bashtar AR, El-Ganainy S, Gamal S (2013) Thelohanellus niloticus sp. nov. (Myxozoa: Myxosporea), a parasite of the Nile carp Labeo niloticus from the River Nile, Egypt. Parasitol Res 112:379–383PubMedCrossRefGoogle Scholar
  2. Adriano EA, Carriero MM, Maia AAM, Silva MRM, Naldoni J, Ceccarelli PS, Arana S (2012) Phylogenetic and host–parasite relationship analysis of Henneguya multiplasmodialis n. sp. infecting Pseudoplatystoma spp. in Brazilian Pantanal wetland. Vet Parasitol 185:110–120PubMedCrossRefGoogle Scholar
  3. Azevedo C, Samuel N, Saveia AP, Delgado F, Casal G (2011) Light and electron microscopical data on the spores of Thelohanellus rhabdalestus n. sp. (Myxozoa: Myxosporea), a parasite of a freshwater fish from the Kwanza River, Angola. Syst Parasitol 78:19–25PubMedCrossRefGoogle Scholar
  4. Bartosova P, Fiala I, Hypsa V (2009) Concatenated SSU and LSU rDNA data confirm the main evolutionary trends within myxosporeans (Myxozoa: Myxosporea) and provide an effective tool for their molecular phylogenetics. Mol Phylogenet Evol 53:81–93PubMedCrossRefGoogle Scholar
  5. Chen QL, Ma CL (1998) Myxozoa: Myxosporea. Science Press, BeijingGoogle Scholar
  6. Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534PubMedCrossRefGoogle Scholar
  7. Griffin MJ, Goodwin AE (2011) Thelohanellus toyamai (Syn. Myxobolus toyamai) infecting the gills of koi Cyprinuscarpio in the Eastern United States. J Parasitol 97:493–502PubMedCrossRefGoogle Scholar
  8. Gui JF, Zhou L (2010) Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploidy Carassius auratus gibelio. Sci China Life Sci 53:409–415PubMedCrossRefGoogle Scholar
  9. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321PubMedCrossRefGoogle Scholar
  10. Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS et al (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395–413PubMedCrossRefGoogle Scholar
  11. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  12. Liu Y, Whipps CM, Gu ZM, Zeng C, Huang MJ (2012) Myxobolus honghuensis n. sp. (Myxosporea: Bivalvulida) parasitizing the pharynx of allogynogenetic gibel carp Carassius auratus gibelio (Bloch) from Honghu Lake, China. Parasitol Res 110:1331–1336PubMedCrossRefGoogle Scholar
  13. Liu Y, Jia L, Huang MJ, Gu ZM (2014a) Thelohanellus testudineus n. sp. (Myxosporea: Bivalvulida) infecting the skin of allogynogenetic gibel carp Carassius auratus gibelio (Bloch) in China. J Fish Dis 37:535–542PubMedCrossRefGoogle Scholar
  14. Liu Y, Yuan JF, Jia L, Huang MJ, Zhou ZG, Gu ZM (2014b) Supplemental description of Thelohanellus wuhanensis Xiao & Chen, 1993 (Myxozoa: Myxosporea) infecting the skin of Carassius auratus gibelio (Bloch): ultrastructural and histological data. Parasitol Int 63:489–491PubMedCrossRefGoogle Scholar
  15. Lom J, Arthur JR (1989) A guideline for preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156CrossRefGoogle Scholar
  16. Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36PubMedCrossRefGoogle Scholar
  17. Luo YZ, Lin L, Wu ZX, Liu Y, Gu ZM, Li LJ, Yuan JF (2013) Haematopoietic necrosis of cultured Prussian carp, Carassius gibelio (Bloch), associated with Cyprinid herpesvirus 2. J Fish Dis 36:1035–1039PubMedCrossRefGoogle Scholar
  18. Molnár K (2002) Site preference of fish myxosporeans in the gill. Dis Aquat Organ 48:197–207PubMedCrossRefGoogle Scholar
  19. Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358PubMedGoogle Scholar
  20. Posada D (2008) JModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256PubMedCrossRefGoogle Scholar
  21. Shin SP, Nguyen VG, Jeong JM, Jun JW, Kim JH, Han JE, Baeck GW, Park SC (2014) The phylogenetic study of Thelohanellus species (Myxosporea) in relation to host specificity and infection site tropism. Mol Phylogenet Evol 72:31–34PubMedCrossRefGoogle Scholar
  22. Suo D, Zhao YJ (2010) Morphological redescription of Thelohanellus nikolskii Achmerov, 1955 (Myxozoa, Bivalvulida) and phylogenetic analysis of Thelohanellus nikolskii inferred from 18S rDNA. Acta Zootax Sin 35:90–95Google Scholar
  23. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (* and other methods), v. 4.0 beta 10. Sinauer Associates, SunderlandGoogle Scholar
  24. Székely C, El-Mansy A, Molnár K, Baska F (1998) Development of Thelohanellus hovorkai and Thelohanellus nikolskii (Myxosporea: Myxozoa) in oligochaete alternate hosts. Fish Pathol 33:107–114CrossRefGoogle Scholar
  25. Székely C, Shaharom-Harrison F, Cech G, Mohamed K, Molnár K (2009) Myxozoan pathogens of Malaysian fishes cultured in ponds and net-cages. Dis Aquat Org 83:49–57PubMedCrossRefGoogle Scholar
  26. 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
  27. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTRAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882CrossRefGoogle Scholar
  28. Wang GT, Yao WJ, Wang JG, Lu YS (2001) Occurrence of thelohanellosis caused by Thelohanellus wuhanensis (Myxosporea) in juvenile allogynogenetic silver crucian carp, Carassius auratus gibelio (Bloch), with an observation on the efficacy of fumagillin as a therapeutant. J Fish Dis 4:57–60CrossRefGoogle Scholar
  29. Wang ZW, Zhu HP, Wang D, Jiang FF, Zhou L, Gui JF (2011) A novel nucleo-cytoplasmic hybrid clone formed via androgenesis in polyploidy gibel carp. BMC Res Notes 4:82PubMedCentralPubMedCrossRefGoogle Scholar
  30. Xi BW, Xie J, Zhou QL, Pan LK, Ge XP (2011) Mass mortality of pond-reared Carassius gibelio caused by Myxobolus ampullicapsulatus in China. Dis Aquat Org 93:257–260PubMedCrossRefGoogle Scholar
  31. Xi BW, Zhang JY, Xie J, Pan LK, Xu P, Ge XP (2013) Three actinosporean types (Myxozoa) from the oligochaete Branchirua sowerbyi in China. Parasitol Res 112:1575–1582PubMedCrossRefGoogle Scholar
  32. Xiao CH (1988) Study of epidemiology and myxosporean fauna from silver crucian carp (Carassius auratus gibelio Bloch) (in Chinese with English summary). Master dissertation, Institute of Hydrobiology, Chinese Academy of SciencesGoogle Scholar
  33. Ye LT, Li WX, Wang WW, Wu SG, Wang GT (2014) Updated morphology, histopathology and molecular phylogeny of Myxobolus hearti, cardiac myxosporea in gibel carp, Carassius gibelio (Bloch). J Fish Dis 37:11–20PubMedCrossRefGoogle Scholar
  34. Yokoyama H, Liyanage YS, Sugai A, Wakabayashi H (1998) Hemorrhagic thelohanellosis of color carp caused by Thelohanellus hovorkai (Myxozoa: Myxosporea). Fish Pathol 33:85–89CrossRefGoogle Scholar
  35. Yokoyama H, Grabner D, Shirakashi S (2012) Transmission biology of the myxozoa, health and environment in aquaculture. In: Carvalho E (ed) InTech, Available from: 
  36. Zhang JY, Wang JG, Li AH, Gong XN, Cai TZ (2006) Redescription of Myxobolus pyramidis Chen, 1958 (Myxosporea: Bivalvulida). Parasitol Res 99:65–69PubMedCrossRefGoogle Scholar
  37. Zhang JY, Wang JG, Li AH, Gong XN (2010a) Infection of Myxobolus turpisrotundus n. sp. in allogynogenetic gibel carp, Carassius auratus gibelio (Bloch), with revision of Myxobolus rotundus (s. l.) Nemeczek reported from C. auratus auratus (L.). J Fish Dis 33:625–638PubMedCrossRefGoogle Scholar
  38. Zhang JY, Yokoyama H, Wang JG, Li AH, Gong XN, Ryu-hasegawa A, Iwashita M, Ogawa K (2010b) Utilization of tissue habitats by Myxobolus wulii Landsberg and 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
  39. Zhang JY, Gu ZM, Kalavati C, Eiras JC, Liu Y, Guo QY, Molnár K (2013) Synopsis of the species of Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida). Syst Parasitol 86:235–256PubMedCrossRefGoogle Scholar
  40. Zhao YJ, Sun CY, Kent ML, Deng JL, Whipps CM (2008) Description of a new species of Myxobolus (Myxozoa: Myxobolidae) based on morphological and molecular data. J Parasitol 94:737–742PubMedCrossRefGoogle Scholar
  41. Zhao YJ, Zhao YJ, Li NN, Tang FH, Dong JL (2013) Remarks on the validity of Myxobolus ampullicapsulatus and Myxobolus honghuensis (Myxozoa: Myxosporea) based on SSU rDNA sequences. Parasitol Res 112: 3817–3823Google Scholar
  42. Zhu YT, Lu HD, Cai SJ (2012) Redescription of Thelohanellus wuhanensis Xiao et Chen (Myxozoa, Myxosporea) infecting allogynogenetic crucian carp (Carassius auratus gibelio) and phylogenetic analysis based on 18S rDNA sequence. Acta Zootax Sin 37:681–686Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • S. Yuan
    • 1
    • 2
  • B. W. Xi
    • 3
  • J. G. Wang
    • 1
  • J. Xie
    • 3
  • J. Y. Zhang
    • 1
  1. 1.Fish Diseases Laboratory, State Key Laboratory of Freshwater Ecology and BiotechnologyInstitute of Hydrobiology, Chinese Academy of SciencesWuhanChina
  2. 2.Jiangsu Agri-Animal Husbandry Vocational CollegeTaizhouChina
  3. 3.Freshwater Fisheries Research CenterChinese Academy of Fishery SciencesWuxiChina

Personalised recommendations