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

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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.

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References

  • 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 113:1459–1463

    Article  PubMed  Google Scholar 

  • 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 102:183–192

    Article  CAS  PubMed  Google Scholar 

  • Akmirza A (2004) Parasite fauna of greater weever Trachinus draco (Linnaeus, 1758). Acta Adriat 45:35–41

    Google Scholar 

  • 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 43:771–780

    Article  PubMed  Google Scholar 

  • 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 100:625–628

    Article  PubMed  Google Scholar 

  • 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. 1–92

  • 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 53:81–93

  • 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 14:137–143

    Article  Google Scholar 

  • Canning EU, Okamura B (2004) Biodiversity and evolution of the Myxozoa. Adv Parasitol 56:43–131

    Article  PubMed  Google Scholar 

  • 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 85:910–919

    Article  CAS  PubMed  Google Scholar 

  • 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 82:185–199

    Article  PubMed  Google Scholar 

  • 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 5:251–280

    Google Scholar 

  • Dorothy KP, Kalavati C (1992) Two new myxosporean parasites of the mullet Liza macrolepis (Smith). Unar Pradesh. J Zool 12:15–19

  • 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 29:627–641

    Article  CAS  PubMed  Google Scholar 

  • 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 102:371–379

    Article  PubMed  Google Scholar 

  • Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534

    Article  CAS  PubMed  Google Scholar 

  • Fiala I, Bartošová P (2010) History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evol Biol 10:228

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 31:921–930

    Article  CAS  PubMed  Google Scholar 

  • Georges V (1982) Helminthes parasites des Poissons de mer des côtes du Sénégal. Bulletin de l’1.F.A.N. T. 44, 8:1–2

  • 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 46:197–212

    Article  CAS  PubMed  Google Scholar 

  • 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 987:47–72

    Article  Google Scholar 

  • Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66:411–453

    Article  CAS  PubMed  Google Scholar 

  • 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 34:1099–1111

    Article  CAS  PubMed  Google Scholar 

  • Holzer AS, Wootten R, Sommerville C (2010) Zschokkella hildae Auerbach, 1910: phylogenetic position, morphology, and location in cultured Atlantic cod. Parasitol Int 59:133–140

  • Horton T (2000) Cerathothoa Steindachneri (Isopoda: Cymotoidae) new to British waters with a key to north-east and Meditterranean Cerathothoa. J Mar Biol 80:1041–1052

    Article  Google Scholar 

  • 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 92:211–218

    Article  PubMed  Google Scholar 

  • 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 48:395–413

    Article  CAS  PubMed  Google Scholar 

  • Lom J, Arthur JR (1989) A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156

    Article  Google Scholar 

  • Lom J, Dyková I (2006) Myxozoan genera: definition and note on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36

    Article  PubMed  Google Scholar 

  • 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 31:189–193

    Article  Google Scholar 

  • 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 62:95–101

    Article  PubMed  Google Scholar 

  • Moser M, Kent ML, Dennis D (1989) Gall bladder Myxosporea in coral reef fishes from Heron Island, Australia. Aust J Zool 37:1–13

    Article  Google Scholar 

  • Okamura B, Gruhl A, Bartholomew JL (eds) (2015) Myxozoan evolution, ecology and development. Springer International Publishing, Switzerland, p 441

    Google Scholar 

  • Öktner A, Trilles JP (2004) Report on the Cymothoids (Crustacea, Isopoda) collected from marine fishes in Turkey. Acta Adriat 45:15–23

    Google Scholar 

  • 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 20:73–89

    CAS  Google Scholar 

  • Petter JA, Maillard C (1988) Larves d’Ascarides parasites de Poissons en Méditerranée Occidentale. Bull Mus Natl Hist Nat 10:347–369

    Google Scholar 

  • 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 107:19–30

    Article  CAS  PubMed  Google Scholar 

  • 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 7:172–177

    Google Scholar 

  • 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 147:1–9

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thélohan P (1895) Recherches sur les myxosporidies. Bull Sci France Belgique 5:100–394

  • Trilles JP, Radujkovic BM, Romestand B (1989) Parasites des poisons marins du Monténégro: Isopodes. Acta Adriat 30:279–306

    Google Scholar 

  • Tripathi YR (1948) Some new Myxosporidia from Plymouth with a proposed new classification of the order. Parasitol 39:110–118

    Article  CAS  Google Scholar 

  • 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 89:168–173

  • 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 29:561–567

    Article  CAS  PubMed  Google Scholar 

  • 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 36:871–879

    CAS  PubMed  Google Scholar 

  • Yokoyama H (2003) A review: gaps in our knowledge on myxozoan parasites of fishes. Fish Pathol 38:125–136

    Article  Google Scholar 

  • 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 48:125–130

    Article  CAS  PubMed  Google Scholar 

  • 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 33:939–946

    Article  CAS  PubMed  Google Scholar 

  • 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. 42

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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.

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Authors and Affiliations

  1. Research Unit of Integrative Biology and Evolutionary and Functional Ecology of Aquatic Systems, Faculty of Science of Tunis, University of Tunis El Manar, El Manar I 2092, Tunis, Tunisia

    Ramla Azizi & Sihem Bahri

  2. Laboratory of Animal Pathology, Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), Biology Department, Faculty of Sciences (FCUP), University of Porto, Porto, Portugal

    Luis F. Rangel, Ricardo Castro & Maria J. Santos

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  1. Ramla Azizi
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Correspondence to Ramla Azizi.

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Azizi, R., Rangel, L.F., Castro, R. et al. Morphology, seasonality and phylogeny of Zschokkella trachini n. sp. (Myxozoa, Myxosporea) infecting the gallbladder of greater weever Trachinus draco (L.) from Tunisian waters. Parasitol Res 115, 4129–4138 (2016). https://doi.org/10.1007/s00436-016-5187-y

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