Skip to main content
SpringerLink
Log in

Morphological description and phylogeny of Ceratomyxa scorpaeni n. sp. (Myxosporea: Ceratomyxidae) infecting the gallbladder of Scorpaena porcus (L.) (Scorpaeniformes: Scorpaenidae) from the bay of Bizerte in Tunisia

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

A new marine myxosporean species Ceratomyxa scorpaeni n. sp. is described using morphological characteristics and small subunit ribosomal DNA (rDNA) sequence data. The parasite was found infecting the gallbladder of Scorpaena porcus Linnaeus, 1758 collected from the Bay of Bizerte. Mature plasmodia were disporous free floating in the bile. Spores were transversely elongated and crescent-shaped with unequal shell valves and measured 7.6 ± 0.2 (7.2–8.0) μm in length and 32.8 ± 0.3 (21.6–44.0) μm in thickness. Two sub-spherical polar capsules equal in size, situated at the same level and measured 3.0 ± 0.2 (3.0–3.2) μm in length and 2.4 ± 0.3 (2.3–3.3) μm in width. The infection with C. scorpaeni n. sp. was prevalent throughout the year with a maximum prevalence of infection during spring and summer. Molecular analysis of the SSU rRNA gene confirmed the parasite as a new member of the genus Ceratomyxa and showed close relationship with the species of Ceratomyxa infecting the gallbladders of Sparidae from the Mediterranean Sea. This is the first report of Ceratomyxa species from the gallbladder of S. porcus in Tunisian coastal waters.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdel-Ghaffar F, Ali MA, Al-Quraishy SA, Rasheid KA, Farraj SA, Abdel-Baki AS, Bashtar A-R (2008) Four new species of Ceratomyxa Thélohan, 1892 (Myxozoa: Myxosporea: Ceratomyxidae) infecting the gallbladder of some Red Sea fishes. Parasitol Res 103:559–565

    Article  CAS  PubMed  Google Scholar 

  • Akif ER, Kayis S (2015) Intensity and prevalence of some crustacean fish parasites in Turkey and their molecular identification. Turk J Zool 39:1142–1150

    Article  Google Scholar 

  • Alama-Bermejo G, Raga JA, Holzer AS (2011) Host parasite relationship of Ceratomyxa puntazzi n. sp. (Myxozoa: Myxosporea) and sharpsnout seabream Diplodus puntazzo (Walbaum, 1792) from the Mediterranean with first data on ceratomyxid host specificity in sparids. Vet Parasitol 182:181–192

    Article  CAS  PubMed  Google Scholar 

  • Alama-Bermejo G, Síma 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 M, Abdel-Baki A, Sakran T (2006) Myxidium elmatboulii n. sp. and Ceratomyxa ghaffari n. sp. (Myxozoa: Myxosporea) Parasitic in the Gallbladder of the Red Sea Houndfish Tylosurus choram (Rüppell, 1837) (Teleostei: Belonidae) from the Red Sea, Egypt. Acta Protozool 45:97–103

    Google Scholar 

  • Arculeo M, Hristosvki N, Riggio S (1997) Helminth infestation of three fishes (Serranus scriba, Mullus surmuletus, Scorpaena porcus) from a coastal seaground in the Gulf of Palermo (Tyrrhenian Sea). Ital J Zool 64:283–286

    Article  Google Scholar 

  • Barta JR, Martin DS, Liberator PA, Dshkevicz 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 83:262–271

    Article  CAS  PubMed  Google Scholar 

  • Bartoli P, Gibson DI (1991) On Podocotyle scorpaenae, Poracanthium furcatum and Derogenes latus, three poorly known digenean parasites of eastern Mediterranean teleosts. Syst Parasitol 20:29–46

    Article  Google Scholar 

  • Burger MAA, Cribb TH, Adlard RD (2007) Patterns of relatedness in the Kudoidae with descriptions of Kudoa chaetodoni sp. n. and K. lethrini sp. n. (Myxosporea: Multivalvulida). Parasitol 134:669–681

    Article  CAS  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  • Canning EU, Okamura B (2004) Biodiversity and evolution of the Myxozoa. Adv Parasitol 56:44–130

    Google Scholar 

  • Çelik ES, Aydin S (2006) Effect of Trachelobdella lubrica (Hirudinea: Piscicolidae) on biochemical and haematological characteristics of black Scorpion fish (Scorpaena porcus, Linnaeus, 1758). Fish Physiol Biochem 32:255–260

    Article  CAS  Google Scholar 

  • Cho JB, Kwon SR, Kim SK, Nam YK, Kim KH (2004) Ultrastructure and development of Ceratomyxa protopsettae Fujita, 1923 (Myxosporea) in the gallbladder of cultured olive flounder, Paralichthys olivaceus. Acta Protozool 43:241–250

    Google Scholar 

  • 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 

  • Ferri J, Petric M, Matic-skoko S, Dulcic J (2008) New host record, black scorpionfish Scorpaena porcus (Pisces, Scorpaenidae) for Nerocila orbigny and Ceratothoa parallela (Crustacea, Isopoda, Cymothoidae). Acta Adriat 49(3):255–258

    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, Hlavnickova M, Kodadkova A, Freeman MA, Bartošova-Sojkova P, Atkinson SD (2015) Evolutionary origin of Ceratonova shasta and phylogeny of the marine myxosporean lineage. Mol Biol Evol 86:75–89

    Google Scholar 

  • Fujita T (1923) Studies on Myxosporidia of Japan. 1. Parasites of flatfishes in Hokkaido. J Coll Agric Hokkaido Imp Univ 10:191–248

    Google Scholar 

  • Gunter NL, Whipps CM, Adlard RD (2009) Ceratomyxa (Myxozoa:Bivalvulida) robusta taxon or genus of convenience? Int J Parasitol 39:1395–1405

    Article  PubMed  Google Scholar 

  • 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 46:197–212

    Article  CAS  PubMed  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 

  • Hmissi J (2014) Contribution à l’étude de la parasitofaune de trois espèces de poissons Scorpaenidés provenant de Bizerte et de Mahdia. Mémoire de Mastère, Faculté des Sciences de Tunis, pp 1–89

    Google Scholar 

  • Kalavati C, MacKenzie K (1999) The genera Ceratomyxa Thélohan, 1892, Leptotheca Thélohan, 1895 and Sphaeromyxa Thélohan, 1892 (Myxosporea: Bivalvulida) in gadid fish of the Northeast Atlantic. Syst Parasitol 43:209–216

    Article  CAS  PubMed  Google Scholar 

  • Kalavati C, Raman AV, Vaidehi J, Bharathi VR (1997) Effects of pollution on planktonic ciliates in Visakhapatnam harbor. Indian J Mar Sci 26:68–73

    Google Scholar 

  • Katharios P, Garaffo M, Sarter K, Athanassopoulou F, Mylonas CC (2007) A case of high mortality due to heavy infestation of Ceratomyxa diplodae in sharpsnout sea bream (Diplodus puntazzo) treated with reproductive steroids. Bull Eur Ass Fish Pathol 27:43–47

    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, Dykova I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36

    Article  PubMed  Google Scholar 

  • Lubat V, Radujkovic B, Marques A, Bouix G (1989) Parasites des poissons marins du Montenegro: Myxosporidies. Acta Adriat 30:31–50

    Google Scholar 

  • Mansour L, Al-Qahtani HA, Al-Quraishy S, Abdel-Baki AS (2014) 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 

  • Oğuz MC, Bray RA (2006) Digenetic trematodes of some teleost fish off the Mudanya Coast (Sea of Marmara, Turkey). Helminthol 43:161–167

    Google Scholar 

  • Öktener A, Trilles JP (2004) Report on Cymothoids (Crustacea, Isopoda) collected from marine fishes in Turkey. Acta Adriat 45(2):145–154

    Google Scholar 

  • Rocha S, Casal G, Rangel L, Severino R, Castro R, Azevedo C, Santos MJ (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 

  • Rocha S, Casal G, Rangel L, Castro R, Severino R, Azevedo C, Santos MJ (2015) Ultrastructure and phylogeny of Ceratomyxa auratae n. sp. (Myxosporea: Ceratomyxidae), a parasite infecting the gilthead sea bream Sparus aurata (Teleostei: Sparidae). Parasitol Int 64:305–313

    Article  CAS  PubMed  Google Scholar 

  • Sağlam N, Oğuz MC, Celik ES, Doyuk SA, Usta A (2003) Pontobdella muricata and Trachelobdella lubrica (Hirudinea: Piscicolidae) on some marine fish in the Dardanelles, Turkey. J Mar Biol Ass UK 83:1315–1316

    Article  Google Scholar 

  • Sitjà-Bobadilla A, Álvarez-Pellitero P (1993) Light and electron microscopical description of Ceratomyxa labracis n. sp. and a redescription of C. diplodae (Myxosporea: Bivalvulida) from wild and cultured Mediterranean sea bass Dicentrarchus labrax (L.) (Teleostei: Serranidae). Syst Parasitol 26:215–223

    Article  Google Scholar 

  • Sitjà-Bobadilla A, Palenzuela O, Álvarez-Pellitero P (1995) Ceratomyxa sparusaurati n. sp (Myxosporea: Bivalvulida), a new parasite from cultured gilthead seabream (Sparus aurata L.) (Teleostei: Sparidae): light and electron microscopic description. J Eukaryot Microbiol 42:529–539

    Article  Google Scholar 

  • Shulman SS (1966) Miksosporidii Fauny SSSR. Nauka Publishers, Moscow. (English translation 1990)

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tepe Y, Oğuz MC (2013) Nematode and acanthocephalan parasites of marine fish of the eastern Black Sea coasts of Turkey. Turk J Zool 37:753–760

    Article  Google Scholar 

  • Thabet A, Mansour L, Al-Omar SY, Tlig-Zouari S (2015) Ceratomyxa tunisiensis n. sp. (Myxosporea: Bivalvulida) from the gallbladders of two Carangid fish caught off the Coast of Tunisia. J Eukaryot Microbiol 63(1):86–92

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gilson TJ, Clustal W (1994) Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whipps CM, Adlard RD, Bryant MS, Lester RJG, Findlav V, Kent ML (2003) First report of three Kudoa species from Eastern Australia: Kudoa thyrsites from Mahi mahi (Coryphaena hippurus), Kudoa amamiensis and Kudoa minithyrsites n. sp. from sweeper (Pempheris ypsilychnus). J Eukaryotic Microbiol 50:215–219

    Article  Google Scholar 

  • Yemmen C, Marton S, Eszterbauer E, Bahri S (2012) Ceratomyxa aegyptiaca n. sp. (Myxozoa: Myxosporea) from the gall-bladder of Solea aegyptiaca Chabanaud (Pleuronectiformes: Soleidae) in a Tunisian coastal lagoon. Syst Parasitol 83:21–28

    Article  PubMed  Google Scholar 

  • Yokoyama H, Fukuda Y (2001) Ceratomyxa seriolae n. sp. and C. buri n. sp. (Myxozoa: Myxosporea) from the gall-bladder of cultured yellow tail Seriola quinqueradiata. Syst Parasitol 48:125–130

    Article  CAS  PubMed  Google Scholar 

  • Yurakhno VM (1997) Influence of environmental factors on myxosporean infestation of Black Sea fish in coastal waters. Oceanol Stud 1:75–85

    Google Scholar 

Download references

Acknowledgments

This research was in part supported by a research scholarship provided to Ms. Myriam Garbouj from the University of Tunis El Manar. We thank Dr. Yemmen, a member of our laboratory at the Faculty of Sciences of Tunis, for his assistance on the phylogenetic analysis. 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 BPEst-C/MAR/LA0015/2013 and the project DIRDAMyx, reference FCOMP-01-0124-FEDER-020726/FCT-PTDC/MAR/116838/2010, was also partially supported 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 (Interdisciplinary Centre of Marine and Environmental Research), supported by the Northern Regional Operational Programme (NORTE2020), through the European Regional Development Fund (ERDF), and the Ph.D. fellowship grant SFRH/BD/82237/2011 attributed to L.F. Rangel.

Author information

Authors and Affiliations

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

    Myriam Garbouj, Jihene Hmissi & Sihem Bahri

  2. Laboratory of Animal Pathology, Department of Biology, Faculty of Sciences, University of Porto, Porto, Portugal

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

  3. Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto, Porto, Portugal

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

Authors
  1. Myriam Garbouj
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luís F. Rangel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ricardo Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jihene Hmissi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maria J. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sihem Bahri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Myriam Garbouj.

Ethics declarations

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

Conflict of interests

The authors declare that they have no conflict of interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Garbouj, M., Rangel, L.F., Castro, R. et al. Morphological description and phylogeny of Ceratomyxa scorpaeni n. sp. (Myxosporea: Ceratomyxidae) infecting the gallbladder of Scorpaena porcus (L.) (Scorpaeniformes: Scorpaenidae) from the bay of Bizerte in Tunisia. Parasitol Res 115, 4495–4502 (2016). https://doi.org/10.1007/s00436-016-5236-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-016-5236-6

Keywords

Search

Navigation