Advertisement

Parasitology Research

, Volume 115, Issue 11, pp 4129–4138 | Cite as

Morphology, seasonality and phylogeny of Zschokkella trachini n. sp. (Myxozoa, Myxosporea) infecting the gallbladder of greater weever Trachinus draco (L.) from Tunisian waters

  • Ramla Azizi
  • Luis F. Rangel
  • Ricardo Castro
  • Maria J. Santos
  • Sihem Bahri
Original Paper
  • 337 Downloads

Abstract

We describe a new myxosporean species, Zschokkella trachini n. sp., infecting the gallbladder of greater weever Trachinus draco Linnaeus 1758 from Tunisia. This is the first record of Zschokkella species in T. draco. Plasmodia were polysporic producing six to eight mature spores; they were attached to the gallbladder epithelium or free floating in the bile. Mature spores were sub-ovoid in the frontal view, measured 15.2 ± 0.6 (14.4–16.0) μm in length and 9.8 ± 0.7 (9.0–10.8) μm in width. Two equal spherical polar capsules 4.0 ± 0.4 (3.6–4.5) μm in diameter, were located separately at the spore’s extremities. The prevalence of infection ranged from 23.5 to 87.7 %. Morphological data and molecular analysis of the small subunit rDNA gene identified this parasite as a new species of Zschokkella. Neighbour joining clustered the parasite in a sub-clade containing other Zschokkella species parasiting the gallbladder of marine fish hosts, located within the coelozoic clade of the major freshwater clade. This is the second Zschokkella species reported from Tunisia.

Keywords

Myxosporean Zschokkella trachini n. sp. Trachinus draco Morphology Seasonality Phylogeny Tunisia 

Notes

Acknowledgments

The research was in part supported by a research scholarship provided to Ramla Azizi from the University Tunis El Manar. The molecular part was partially supported by the European Regional Development Fund (ERDF) through the COMPETE—Operational Competitiveness Programme, and national funds through FCT—Foundation for Science and Technology, under the project DIRDAMyx, reference FCOMP-01-0124-FEDER-020726/FCT-PTDC/MAR/116838/2010; by the Structured Program of R&D&I INNOVMAR—Innovation and Sustainability in the Management and Exploitation of Marine Resources, reference NORTE-01-0145-FEDER-000035, namely within the Research Line INSEAFOOD Innovation and valorization of seafood products: meeting local challenges and opportunities, within the R&D Institution CIIMAR (InterdisciplinaryCentre of Marine and Environmental Research), supported by the Northern Regional Operational Programme (NORTE2020), through the European Regional Development Fund (ERDF); and the PhD fellowship grant SFRH/BD/82237/2011 attributed to L. Rangel through the programme POPH/FSE QREN.

Compliance with ethical standards

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Abdel-Baki AA, Sakran T, Zayed E, Al-Quraishy S (2014) Seasonal fluctuation and histopathology of Henneguya ghaffari (Myxozoa: Myxosporea) infection in the gills of the Nile perch, Lates niloticus, in the River Nile: a new locality record. Parasitol Res 113:1459–1463CrossRefPubMedGoogle Scholar
  2. Abdel-Ghaffar F, Ali MA, Al Q, Entzeroth R, Abdel-Baki AS, Al Farraj S, Bashtar AR (2008) Zschokkella helmi n.sp. (Myxozoa: Myxosporea), a new parasite of marble spinefoot Siganus rivulatus (Forsskal 1775), Red Sea, Egypt: light and transmission electron microscopy. Parasitol Res 102:183–192CrossRefPubMedGoogle Scholar
  3. Akmirza A (2004) Parasite fauna of greater weever Trachinus draco (Linnaeus, 1758). Acta Adriat 45:35–41Google Scholar
  4. Alama-Bermejo G, Sima R, Raga JA, Holzer AS (2013) Understanding myxozoan infection dynamics in the sea: seasonality and transmission of Ceratomyxa puntazzi. Int J Parasitol 43:771–780CrossRefPubMedGoogle Scholar
  5. Ali MA, Abdel-Baki AS, Abdel-Ghaffar F (2007) Zschokkella egyptica n. sp. (Myxosporea: Bivalvulida) infecting the gall bladder of the eel catfish Plotosus lineatus Thunberg, 1787 and the freckled goatfish Upeneus tragula Richardson, 1846 in the Red Sea, Egypt. Parasitol Res 100:625–628CrossRefPubMedGoogle Scholar
  6. Azizi R (2014) Contribution à l’étude de la parasitofaune de trois espèces de poissons Trachinidés provenant de Bizerte et de Mahdia. Faculté des sciences de Tunis, pp. 1–92Google Scholar
  7. Bartošová P, Fiala I, Hypša V (2009) Concatenated SSU andLSU rDNA data confirm the main evolutionary trends within myxosporeans (Myxozoa: Myxosporea) and provide an effective tool for their molecular phylogenetics. Mol Phylogenet Evol 53:81–93Google Scholar
  8. Bucher F, Hofer L, El-Matbouli M (1992) Prevalence and pathology of Zschokkella nova (Myxosporea) in the liver of bullhead Cottus gobio from a polluted river. Dis Aquat Org 14:137–143CrossRefGoogle Scholar
  9. Canning EU, Okamura B (2004) Biodiversity and evolution of the Myxozoa. Adv Parasitol 56:43–131CrossRefPubMedGoogle Scholar
  10. Canning EU, Curry A, Anderson CL, Okamura B (1999) Ultrastructure of Myxidium trachinorum sp. nov. from the gallbladder of the lesser weever fish Echiichthys vipera. Parasitol Res 85:910–919CrossRefPubMedGoogle Scholar
  11. Carreras-Aubets M, Montero FE, Kostadinova A, Gibson DI, Carrasson M (2012) Redescriptions of two frequently recorded but poorly known hemiurid digeneans, Lecithochirium musculus (Looss, 1907) (Lecithochiriinae) and Ectenurus Lepidus (Looss, 1907) (Dinurinae), based on material from the western Mediterranean. Syst Parasitol 82:185–199CrossRefPubMedGoogle Scholar
  12. Dillon WA, Hargis WJ (1965) Monogenetic trematodes from the southern Pacific Ocean 2. Polyopisthocotyleids from New Zealand fishes: the families Discocotylidae, Micrococotylidae, Axinidae, and Gastrococotylidae. In: Biology of the Antractic seas II. Antractic Research series. American Geophysical Union 5:251–280Google Scholar
  13. Dorothy KP, Kalavati C (1992) Two new myxosporean parasites of the mullet Liza macrolepis (Smith). Unar Pradesh. J Zool 12:15–19Google Scholar
  14. El-Matbouli M, McDowell TS, Antonio DB, Andree KB, Hedrick RP (1999) Effect of water temperature on the development, release and survival of the triactinomyxon stage of Myxobolus cerebralis in its oligochaete host. Int J Parasitol 29:627–641CrossRefPubMedGoogle Scholar
  15. Farjallah S, Slimane BB, Busi M, Paggi L, Amor N, Blel H, Said K, D’Amelio S (2008) Occurrence and molecular identification of Anisakis spp. from the North African coasts of Mediterranean Sea. Parasitol Res 102:371–379CrossRefPubMedGoogle Scholar
  16. Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534CrossRefPubMedGoogle Scholar
  17. Fiala I, Bartošová P (2010) History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evol Biol 10:228CrossRefPubMedPubMedCentralGoogle Scholar
  18. Freeman MA, Yokoyama H, Ogawa K (2008) Description and phylogeny of Ceratomyxa anko sp. n. and Zschokkella lophii sp. n. from the Japanese angler fish, Lophius litulon (Jordan). J Fish Dis 31:921–930CrossRefPubMedGoogle Scholar
  19. Georges V (1982) Helminthes parasites des Poissons de mer des côtes du Sénégal. Bulletin de l’1.F.A.N. T. 44, 8:1–2Google Scholar
  20. Hallett SL, Diamant A (2001) Ultrastructure and small-subunit ribosomal DNA sequence of Henneguya lesteri n. sp. (Myxosporea), a parasite of sand whiting Silla goanalis (Sillaginidae) from the coast of Queensland, Australia. Dis Aquat Org 46:197–212CrossRefPubMedGoogle Scholar
  21. Heiniger H, Adlard RD (2014) Relatedness of novel species of Myxidium Bütshli, 1882, Zschokkella Auerbach, 1910 and Ellipsomyxa (Koie, 2003) (Myxosporea: Bivalvulida) from the gall bladders of marines fishes (Teleostei) from Australian waters. Syst parasitol 987:47–72CrossRefGoogle Scholar
  22. Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453CrossRefPubMedGoogle Scholar
  23. 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 34:1099–1111CrossRefPubMedGoogle Scholar
  24. Holzer AS, Wootten R, Sommerville C (2010) Zschokkella hildae Auerbach, 1910: phylogenetic position, morphology, and location in cultured Atlantic cod. Parasitol Int 59:133–140Google Scholar
  25. Horton T (2000) Cerathothoa Steindachneri (Isopoda: Cymotoidae) new to British waters with a key to north-east and Meditterranean Cerathothoa. J Mar Biol 80:1041–1052CrossRefGoogle Scholar
  26. Kalatzis PG, Kokkari C, Katharios P (2015) Morphological characterisation and phylogenetic relationships of Zschokkella candia n. sp. from the gallbladder of Sparisoma cretense (L.) (Perciformes: Scaridae) in the Sea of Crete off Greece. Syst Parasitol 92:211–218CrossRefPubMedGoogle Scholar
  27. Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Delvin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJG, Longshaw M, Palenzuela O, Siddall ME, Xizo CX (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395–413CrossRefPubMedGoogle Scholar
  28. Lom J, Arthur JR (1989) A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156CrossRefGoogle Scholar
  29. Lom J, Dyková I (2006) Myxozoan genera: definition and note on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36CrossRefPubMedGoogle Scholar
  30. Maeno Y, Sorimachi M, Ogawa K, Kearn GC (1995) Myxobolus spirosulcatus n. sp. (myxosporea, bivalvulida) infecting the bile-duct of the yellowtail Seriola quinqueradiata from japan. Syst Parasitol 31:189–193CrossRefGoogle Scholar
  31. Mansour L, Al-Qahtani HA, Al-Quraishy S, Abdel-Baki AA (2015) Molecular and morphometric characteristics of Ceratomyxa hamour n. sp. (Myxosporea: Bivalvulida) infecting the gallbladder of the orange-spotted grouper Epinephelus coioides from the Arabian Gulf, Saudi Arabia. J Eukaryot Microbiol 62:95–101CrossRefPubMedGoogle Scholar
  32. Moser M, Kent ML, Dennis D (1989) Gall bladder Myxosporea in coral reef fishes from Heron Island, Australia. Aust J Zool 37:1–13CrossRefGoogle Scholar
  33. Okamura B, Gruhl A, Bartholomew JL (eds) (2015) Myxozoan evolution, ecology and development. Springer International Publishing, Switzerland, p 441Google Scholar
  34. Öktner A, Trilles JP (2004) Report on the Cymothoids (Crustacea, Isopoda) collected from marine fishes in Turkey. Acta Adriat 45:15–23Google Scholar
  35. Orecchia P, Paggi L (1978) Aspetti di sistematica e di ecologia degli elminti parassiti di pesci marini studiati presso l’Istituto di Parassitologia dell’Università di Roma. Parasitol 20:73–89Google Scholar
  36. Petter JA, Maillard C (1988) Larves d’Ascarides parasites de Poissons en Méditerranée Occidentale. Bull Mus Natl Hist Nat 10:347–369Google Scholar
  37. Rocha S, Casal G, Rangel L, Severino R, Castro R, Azevedo C, Joao-Santos M (2013) Ultrastructural and phylogenetic description of Zschokkella auratis sp. nov. (Myxozoa), a parasite of the gilthead seabream Sparus aurata. Dis Aquat Org 107:19–30CrossRefPubMedGoogle Scholar
  38. Sarkar NK (2012) Three new species of Myxosporea (Bivalvulida), parasites of the gallbladder of scombrid fish, from the Bay of Bengal (Indian Ocean), West Bengal, India. Protistol 7:172–177Google Scholar
  39. Schlegel M, Lom J, Stechmann A, Bernhard B, Leipe D, Dyková I, Sogin M (1996) Phylogenetic analysis of complete small subunit ribosomal RNAcoding region of Myxidium lieberkuehni: evidence that myxozoa are metazoa and related to the bilateria. Arch Protistenkunde 147:1–9CrossRefGoogle Scholar
  40. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  41. Thélohan P (1895) Recherches sur les myxosporidies. Bull Sci France Belgique 5:100–394Google Scholar
  42. Trilles JP, Radujkovic BM, Romestand B (1989) Parasites des poisons marins du Monténégro: Isopodes. Acta Adriat 30:279–306Google Scholar
  43. Tripathi YR (1948) Some new Myxosporidia from Plymouth with a proposed new classification of the order. Parasitol 39:110–118CrossRefGoogle Scholar
  44. Whipps CM, Adlard RD, Bryant MS, Kent ML (2003) Two unusual myxozoans, Kudoa quadricornis n. sp. (Multivalvulida) from the muscle of goldspotted trevally (Carangoides fulvoguttatus) and Kudoa permulticapsula n. sp. (Multivalvulida) from the muscle of Spanish mackerel (Scomberomorus commersoni) from the Great Barrier Reef. Aust J Parasitol 89:168–173Google Scholar
  45. Yanagida T, Sameshima M, Nasu H, Yokoyama H, Ogawa K (2006) Temperature effects on the development of Enteromyxum spp. (Myxozoa) in experimentally infected tiger puffer, Takifugur ubripes (Temminck & Schlegel). J Fish Dis 29:561–567CrossRefPubMedGoogle Scholar
  46. Yemmen C, Marton S, Bahri S, Eszterbauer E (2013) Morphology, seasonality and phylogeny of Zschokkella soleae sp. n. (Myxozoa, Myxosporea) parasite of Solea solea (L.) (Pleuronectiformes, Soleidae) from Ghar El Melh Lagoon, Tunisia. J Fish Dis 36:871–879PubMedGoogle Scholar
  47. Yokoyama H (2003) A review: gaps in our knowledge on myxozoan parasites of fishes. Fish Pathol 38:125–136CrossRefGoogle Scholar
  48. Yokoyama H, Fukuda Y (2001) Ceratomyxa seriolae n. sp. and C. buri n. sp. (Myxozoa: Myxosporea) from the gall-bladder of cultured yellowtail Seriola quinqueradiata. Syst Parasitol 48:125–130CrossRefPubMedGoogle Scholar
  49. Yokoyama H, Yanagida T, Freeman MA, Katagiri T, Hosokawa A, Endo M, Hirai M, Takagi S (2010) Molecular diagnosis of Myxobolus spirosulcatus associated with encephalomyelitis of cultured yellowtail, Seriola quinqueradiata Temminck & Schlegel. J Fish Dis 33:939–946CrossRefPubMedGoogle Scholar
  50. Yokoyama H, Grabner D, Shirakashi S (2012) Transmission biology of the Myxozoa. In: E. Carvalho., editor. Health and environment in aquaculture. InTech; Rijeka, Croatia. pp. 42Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Ramla Azizi
    • 1
  • Luis F. Rangel
    • 2
  • Ricardo Castro
    • 2
  • Maria J. Santos
    • 2
  • Sihem Bahri
    • 1
  1. 1.Research Unit of Integrative Biology and Evolutionary and Functional Ecology of Aquatic Systems, Faculty of Science of TunisUniversity of Tunis El ManarTunisTunisia
  2. 2.Laboratory of Animal Pathology, Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), Biology Department, Faculty of Sciences (FCUP)University of PortoPortoPortugal

Personalised recommendations