Abstract
First parasitological surveys of Myxozoa are performed on the sparid saddled seabream Oblada melanura (Linnaeus, 1758) and the serranid painted comber Serranus scriba (Linnaeus, 1758) caught from the Bay of Bizerte and the Gulf of Tunis respectively in Northeast Tunisia, Western Mediterranean. In this study, 6 bivalvulid myxosporean species belonging to the 3 genera Ceratomyxa Thélohan, 1892, Myxodavisia Zhao, Zhou, Kent & Whipps, 2008 and Zschokkella Auerbach, 1910, are isolated infecting their hosts. Two species Ceratomyxa sp. 1 ex O. melanura (Prevalence (P) = 36%) and Ceratomyxa sp. 2 ex O. melanura (P = 13%) infected the saddled seabream and four species Ceratomyxa sp. 1 ex S. scriba (P = 11.7%), Ceratomyxa sp. 2 ex S. scriba (P = 6.7%), Myxodavisia sp. (P = 8.3%) and Zschokkella sp. (P = 5.6%) infected the painted comber. These myxosporeans differ, in vegetative stages and/or in mature spores, from all the previously known congeneric species, and are described here on the basis of their morphological and morphometric features, their host and tissue specificities and their biogeographical distribution. This is the first report of myxosporean infections in O. melanura and S. scriba. The occurrence of two ceratomyxid species in each host species supports that the genus Ceratomyxa is host-specific not only in sparids but also in serranids, which agrees with data previously obtained from Sparidae in Mediterranean Sea and from Serranidae in GBR, Australia. A member of the myxosporean genus Myxodavisia is recorded from the Mediterranean Sea for the first time, and Zschokkella spp. infections have not previously been recorded from a host in Serranidae. During the examination, a several cases of Co-infection among myxosporeans, both with two and three species, are provided and statistically studied. Indeed, 5% of the breams and 9.4% of the combers are infected with more than one myxosporean parasite. The relationship between myxosporean infections and some biological parameters are pointed out. A higher prevalence of myxosporean infection is coincided with the peak period of spawning activity in May-June for S. scriba. For both hosts, analysis using Fulton’s condition factor (K) has revealed no significant difference between infected and non-infected fishes. Clinically, no external signs of disease have been occurred in infected hosts, but some changes in the bile fluid, colour, and viscosity and in the gall bladder ’s tissue are examined in S. scriba.
References
Abdel-Baki, A.S., Mansour, L., Al-Qahtani, H.A., Al Omar, S.Y. & Al-Quraishy, S. (2015) Morphology, seasonality and phylogenetic relationships of Ceratomyxa husseini n. sp. from the gall-bladder of Cephalopholis hemistiktos (Rüppell) (Perciformes: Serranidae) in the Arabian Gulf off Saudi Arabia. Systematic Parasitology, 91, 91–99.
https://doi.org/10.1007/s11230-015-9554-3Abdel-Ghaffar, F., Ali, M.A., Al-Quraishy, S., Al-Rasheid, K., Al-Farraj, S., Abdel-Baki, A.S. & Bashtar, A.R. (2008a) Four new species of Ceratomyxa Thélohan 1892 (Myxozoa: Myxosporea: Ceratomyxidae) infecting the gall bladder of some Red Sea fishes. Parasitology Research, 103, 559–565.
https://doi.org/10.1007/s00436-008-1010-8Abdel-Ghaffar, F., Ali, M.A., Al-Quraishy, S., Entzeroth, R., Abdel-Baki, A.S., Al-Farraj, S. & Bashtar, A.R. (2008b) Zschokkella helmii n. sp (Myxozoa: Myxosporea), a new parasite of marbled spinefoot Siganus rivulatus (Forsskal, 1775), Red Sea, Egypt: light and transmission electron microscopy. Parasitology Research, 102, 83–192.
https://doi.org/10.1007/s00436-007-0732-3Abdel-Ghaffar, F., El-Toukhy, A., Al-Quraishy, S., Al-Rasheid, K., Abdel-Baki, A.S., Hegazy, A. & Bashtar, A.R. (2008c) Five new myxosporean species (Myxozoa: Myxosporea) infecting the Nile tilapia Oreochromis niloticus in Bahr Shebin, Nile Tributary. Nile Delta Egypt. Parasitology Research, 103, 1197–1205.
https://doi.org/10.1007/s00436-008-1116-zAdlard, R.D., Cribb, T.H., Beveridge, I. & Miller,T. (2010) Biodiversity and genetic relatedness of internalparasites of coral reef fishes collected under the CReefs program. Museum ofTropical Queensland. Availablefrom: http://www.mtq.qm.qld.gov.au/Research/Projects/Projects/Biodiversity/Parasitology/Internal+parasites+of+coral+reef+fishes#.WOTHStKLTIV(accessed 3 April 2017)
Alama-Bermejo, G., Raga, J.A. & Holzer, A.S. (2011) Host-parasite 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. Veterinary Parasitology, 182, 181–192.
https://doi.org/10.1016/j.vetpar.2011.05.012Alama-Bermejo, G., Šima, R., Raga, J.A. & Holzer, A.S. (2013) Understanding myxozoan infection dynamics in the sea: Seasonality and transmission of Ceratomyxa puntazzi. International Journal for Parasitology, 43 (9), 771–780.
https://doi.org/10.1016/j.ijpara.2013.05.003Ali, M., Abdel-Baki, A.A. & Sakran, T. (2006) Myxidium elmatboulii n. sp. and Ceratomyxa ghaffari n. sp. (Myxozoa: Myxosporea) parasitic in the gall bladder of the Red Sea houndfish Tylosurus choram (Ruppell 1837) (Teleostei: Belonidae) from the Red Sea, Egypt. Acta Protozoologica, 45, 97–103.
Ali, M., Abdel-Baki, A.A.S. & 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. Parasitology Research, 100, 625−628.
https://doi.org/10.1007/s00436-006-0319-4Alonso-Fernández, A., Alós, J., Grau, A., Domínguez-Petit, R. & Saborido-Rey, F. (2011) The use of histological techniques to study the reproductive biology of the hermaphroditic Mediterranean fishes Coris julis, Serranus scriba and Diplodus annularis. Marine Coast Fisheries, 3, 145–159.
Alós, J., Alonso-Fernández, A., Catalán, I.A., Palmer, M. & Lowerre-Barbieri, S. (2013) Reproductive output traits of the simultaneous hermaphrodite Serranus scriba in the western Mediterranean. Scientia Marina, 77 (2), 331–340.
Alvarez-Pellitero, P. & Sitjá-Bobadilla, A. (1993a). Ceratomyxa spp. (Protozoa: Myxosporea) infections in wild and cultured sea bass (Dicentrarchus labrax) from the Spanish Mediterranean area. Journal of Fish Biology, 42, 889–901.
https://doi.org/10.1111/j.1095-8649.1993.tb00398.xAlvarez-Pellitero, P. & Sitjá-Bobadilla, A. (1993b) Pathology of myxosporea in marine fish culture. Diseases of Aquatic Organisms, 17, 229–238.
https://doi.org/10.3354/dao017229Alvarez-Pellitero, P., Sitjá-Bobadilla, A. & Franco-Sierra, A. (1992) Protozoan parasites of wild and cultured sea bass (Dicentrarchus labrax) from the Mediterranean area. Aquaculture and Fisheries Management, 24, 101–108.
Aseeva, N.L. (1992) Myxosporidia from Lepidopsetta bilineata of the Avachinskaya bay. Parasitologiya, 26, 161–165. [in Russian]
Aseeva, N.L. (2002) New species of myxosporeans (Myxozoa, Myxosporea) from sculpins of the Northern Japan Sea. Acta Parasitologica, 47, 179–189.
Aseeva, N.L. (2003) New species of myxosporeans (Myxozoa, Myxosporea) from flounders in the Sea of Japan. Zoologicheskii Zhurnal, 82, 1168–1178.
Atkinson, S.D., Foott, J.S. & Bartholomew, J.L. (2014) Erection of Ceratonova n. gen. (Myxosporea: Ceratomyxidae) to encompass freshwater species C. gasterostea n. sp. from threespine stickleback (Gasterosteus aculeatus) and C. shasta n. comb. from salmonid fishes. Journal of Parasitology, 100, 640‒645.
https://doi.org/10.1645/13-434.1Atz, J.W. (1965) Hermaphroditic Fish. Science, 150, 789–797.
https://doi.org/10.1126/science.150.3697.789Auerbach, M. (1910) Biologische und morphologische Bemerkungen uber Myxosporidien. Zoologischer Anzeiger, 3557–3563.
Awakura, T., Nagasawa, K. & Urawa, S. (1995) Occurence of Myxobolus arcticus and M. neurobius (Myxozoa: Myxosporea) in masu salmon (Oncorhynchus masou) from northern Japan. Reports of the Hokkaido Salmon Hatchery, 49, 35–40.
Azizi, R., Rangel, L., Castro, R., Santos, J.M. & Bahri, S. (2016) Morphology, seasonality and phylogeny of Zschokkella trachini n. sp. (Myxozoa, Myxosporea) infecting the gallbladder of greater weever Trachinus draco (L.) from Tunisian waters. Parasitology Research, 115, 4129–4138. https://doi.org/10.1007/s00436-016-5187-y
Bartholomew, J.L., Whipple, M.J., Stevens, D.G. & Fryer, J.L. (1997) The life cycle of Ceratomyxa shasta, a myxosporean parasite of salmonids, requires a freshwater polychaete as an alternate host. Journal of Parasitology, 83, 859–868.
https://doi.org/10.2307/3284281Bartošová, P. & Fiala, I. (2011) Molecular evidence for the existence of cryptic species assemblages of several myxosporeans (Myxozoa). Parasitolology Research, 108, 573–583. https://doi.org/10.1007/s00436-010-2100-y
Bartošová-Sojková, P., Kodádková, A., Pecková, H., Kuchta, R. & Reed, C.C. (2014) Morphology and phylogeny of two new species of Sphaeromyxa Thélohan, 1892 (Cnidaria: Myxozoa) from marine fish (Clinidae and Trachichthyidae). Parasitology, 142 (5), 660–674.
https://doi.org/10.1017/S0031182014001723Bauchot, M.L. (1987) Serranidae. In: Fischer, W., Bauchot, M.L. & Schneider M. (Eds.), Fiches FAO d’identification des espèces pour les besoins de la pêche (Révision 1). Méditerranée et Mer Noire. (Zone de Pêche 37). Vol. 2. Rome, FAO, pp. 1301–1319.
Bauchot, M.L. & Hureau, J.C. (1986) Sparidae. In: Fishes of the North Eastern Atlantic and the Mediterranean. Vol. II. UNESCO, Paris, pp. 883–907.
Bouain, A. (1981) Les serrans (Téléostéens, Serranidés) des côtes sud de la Tunisie. Taille de première maturité, période de reproduction. Cybium, 4, 65–75.
Bradai, M.N., Quignard, J.P., Bouain, A., Jarboui, O., Ouannes-Ghorbel, A., Benabdallah, L., Zaouali, J. & Bensalem, S. (2004) Ichtyofaune autochtone et exotique des côtes tunisiennes : recensement et biogéographie. Cybium, 28 (4), 315–328
Bush, A.O., Lafferty, K.D., Lotz, J.F. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms. Margolis et al. revisited. Journal of Parasitology, 83, 575–583.
https://doi.org/10.2307/3284227Chen, B.S. (1996) An overview of the disease situation, diagnostic techniques, preventatives and treatment for cage-cultured, high-value marine fishes in China. In: Main, K.L. & Rosenfeld, C. (Eds.), Aquaculture Health Management Strategies for Marine Fishes. Proceedings of a Workshop in Honolulu, Hawaii, October 9–13, 1995. The Oceanic Institute, Hawaii, pp. 109–116.
Cone, D., Marcogliese, D.J. & Russell, R. (2004) The myxozoan fauna of spottail shiner in the great lakes basin: membership, richness, and geographical distribution. Journal of
Parasitology, 90 (5), 921–932.
https://doi.org/10.1645/GE-3313Cuyás, C., Castro, J.J., Santa-Ortega, A.T. & Carbonell, E. (2004) Insular stock identification of Serranus atricauda (Pisces: Serranidae) through the presence of Ceratothoa steindachneri (Isopoda: Cymothoidae) and Pentacapsula cutanea (Myxozoa: Pentacapsulidae) in the Canary Islands. Scientia Marina, 68 (1), 159–163.
https://doi.org/10.3989/scimar.2004.68n1159Davis, H.S. (1917) The Myxosporidia of the Beaufort region, a systematic and biological study. Bulletin of the United States Bureau of Fisheries, 35, 199–252.
Diamant, A., Lom, J. & Dyková, I. (1994) Myxidium leei n. sp., a pathogenic myxosporean of cultured sea bream Sparus aurata. Diseases of Aquatic Organisms, 20, 137–141. https://doi.org/10.3354/dao020137
Eiras, J.C. (2006) Synopsis of the species of Ceratomyxa Thélohan, 1892 (Myxozoa: Myxosporea: Ceratomyxidae). Systematic Parasitology, 65 (1), 49–71.
https://doi.org/10.1007/s11230-006-9039-5El-Matbouli, M., McDowell, T.S., Antonio, D.B., Andree, K.B. & Hedrick, R.P. (1999) Effect of water temperature on the development, release and survival of the triactinomyxon stage of Myxobolus cerebralis, the causative agent of whirling disease, in its oligochaete host. International Journal for Parasitology, 29, 627–641.
https://doi.org/10.1016/S0020-7519(99)00009-0Feng, J.M., Xiong, J., Zhang, J.Y., Yang, Y.L., Yao, B., Zhou, Z.G. & Miao, W. (2014) New phylogenomic and comparative analyses provide corroborating evidence that Myxozoa is Cnidaria. Molecular Phylogenetics and Evolution, 81, 10–18.
https://doi.org/10.1016/j.ympev.2014.08.016Fiala, I. (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology, 36, 1521−1534. https://doi.org/10.1016/j.ijpara.2006.06.016
Fioravanti, M.L., Caffara, M., Florio, D., Gustinelli, A. & Marcer, F. (2006) A parasitological survey of European seabass (Dicentrarchus labrax) and gilthead seabream (Sparus aurata) cultured in Italy. Veterinary Research Communications, 30 (1), 249–252.
https://doi.org/10.1007/s11259-006-0053-5Fischer, W. & Petersen, C.W. (1987) The evolution of sexual patterns in the sea basses. Space use and behavior can predict whether a species has harems or is monogamous and hermaphroditic. Bio Science., 37, 482−489.
Fischer, W., Schneider, M. & Bauchot, M.L. (1987) Fiches FAO d’identification des espèces pour les besoins de la pêche. Méditerranée et Mer Noire (zone de pêche 37). FAO, Rome, 1529 pp.
Froese, R. (2006) Cube law, condition factor and Length-Weight relationships: history, meta-analysis and recommendations. Journal of Applied Ichthyology, 22, 241–253.
https://doi.org/10.1111/j.1439-0426.2006.00805.xFroese, R. & Pauly, D. (2000) FishBase 2000: Concepts, design and data sources. ICLARM, Manila, 344 pp.
Froese, R. & Pauly, D. (2009) FishBase. World Wide Web electronic publication. Version 08/2009. Available from: http://www.fishbase.org (accessed 4 April 2017)
Fujita, T. (1923) Studies on Myxosporidia of Japan. Journal of the College of Agriculture, Hokkaido Imperial University, 16, 191–248.
Georgévitch, J. (1916) Note sur les Myxosporidies recueillies a Roscoff. Bulletin de la société zoologique de France, 41, 86–95.
https://doi.org/10.5962/bhl.part.26340Gleeson, R. & Adlard, R. (2011) Morphological and genetic analysis of three new species of Ceratomyxa Thélohan, 1892 (Myxozoa: Myxosporea) from carcharhinid sharks off Australia. Systematic Parasitology, 80, 117–124.
https://doi.org/10.1007/s11230-011-9316-9Guidetti, P. (2000) Differences among fish assemblages associated with nearshore Posidonia oceanica seagrass beds, rocky-algal reefs and unvegetated sand habitats in the Adriatic Sea. Estuarine, Coastal and Shelf Science, 50, 515–529.
https://doi.org/10.1006/ecss.1999.0584Gunter, N. & Adlard, R. (2010) The demise of Leptotheca Thélohan, 1895 (Myxozoa: Myxosporea: Ceratomyxidae) and assignment of its species to Ceratomyxa Thélohan 1892 (Myxosporea: Ceratomyxidae), Ellipsomyxa Køie, 2003 (Myxosporea: Ceratomyxidae), Myxobolus Butschli, 1882 and Sphaerospora Thélohan, 1892 (Myxosporea: Sphaerosporidae). Systematic Parasitology, 75, 81–104.
https://doi.org/10.1007/s11230-009-9227-1Gunter, N.L. & Adlard, R.D. (2008) Bivalvulidan (Myxozoa: Myxosporea) parasites of damselfishes with description of twelve novel species from Australia’s Great Barrier Reef. Parasitology, 135, 1165–1178.
https://doi.org/10.1017/S0031182008004733Gunter, N.L. & Adlard, R.D. (2009) Seven new species of Ceratomyxa Thélohan, 1892 (Myxozoa) from the gall-bladders of serranid fishes from the Great Barrier Reef, Australia. Systematic Parasitology, 73, 1–11.
https://doi.org/10.1007/s11230-008-9162-6Gunter, N.L., Burger, M.A. & Adlard, R.D. (2010) Morphometric and molecular characterisation of four new Ceratomyxa species (Myxosporea: Bivalvulida: Ceratomyxidae) from fishes off Lizard Island, Australia. Folia Parasitologica, 57, 1–10
Gunter, N.L., Whipps, C.M. & Adlard, R.D. (2009) Ceratomyxa (Myxozoa: Bivalvulida): robust taxon or genus of convenience?. International Journal for Parasitology, 39, 1395–1405. https://doi.org/10.1016/j.ijpara.2009.04.008
Harikrishnan, R., Balasundaram, C. & Heo, M. (2010) Molecular studies, disease status and prophylactic measures in grouper aquaculture: economic importance, disease and immunology. Aquaculture, 309, 1–14.
https://doi.org/10.1016/j.aquaculture.2010.09.011Hartikainen, H., Gruhl, A. & Okamura, B. (2014) Diversification and repeated morphological transitions in endoparasitic cnidarians (Myxozoa: Malacosporea). Molecular Phylogenetics and Evolution, 76, 261–269.
https://doi.org/10.1016/j.ympev.2014.03.010Heiniger, H. & Adlard, R.D. (2013) Molecular identification of cryptic species of Ceratomyxa Thélohan, 1892 (Myxosporea: Bivalvulida) including the description of eight novel speciesfrom apogonid fishes (Perciformes: Apogonidae) from Australian waters. Acta Parasitologica, 58 (3), 342–360.
https://doi.org/10.2478/s11686-013-0149-3Heiniger, H. & Adlard, R.D. (2014) Relatedness of novel species of Myxidium Bütschli, 1882, Zschokkella Auerbach, 1910 and Ellipsomyxa Køie, 2003 (Myxosporea: Bivalvulida) from the gall bladders of marine fishes (Teleostei) from Australian waters. Systematic Parasitology, 87, 47–72. https://doi.org/10.1007/s11230-013-9454-3
Heiniger, H., Gunter, N.L. & Adlard, R.D. (2008) Relationships between four novel ceratomyxid parasites from the gall bladders of labrid fishes from Heron Island, Australia. Parasitology International, 57, 158–165.
https://doi.org/10.1016/j.parint.2007.11.006Holzer, A.S., Sommerville, C. & Wootten, R. (2004) Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. International Journal of Parasitology, 34, 1099–1111.
https://doi.org/10.1016/j.ijpara.2004.06.002Holzer, A.S., Stewart, S., Tildesley, A., Wootten, R. & Sommerville, C. (2010) Infection dynamics of two renal myxozoans in hatchery reared fry and juvenile Atlantic cod Gadus morhua L. Parasitology, 137, 1501–1513.
https://doi.org/10.1017/S0031182010000247Ishizaki, H. (1960). A new myxosporidian parasite of the genus Leptotheca. Bulletin of Fukuoka Gakugei University, 10, 113–116.
Jameson, A.P. (1913) A note on some Myxosporidia collected at Monaco. Bulletin de l’Institut Océanographique de Monaco, 273, 1–4.
Jameson, A.P. (1929) Myxosporidia from Californian fishes. Journal of Parasitology, 16, 59–68.
Jardas, I. (1996) Jadranska ihtiofauna. S Ï kolska knjiga, Zagreb, 533 pp. [in Croatian]
Kabata, Z. (1962) Five new species of myxosporidia from marine fishes. Journal of Parasitology, 52, 177–186.
https://doi.org/10.2307/3271910Kalatzis, P.G., Kokkari, C. & Katharios, P. (2013) Description and relationships of two novel species of Ceratomyxa Thélohan, 1892 infecting the gall bladders of Aulopiformes: Atlantic lizardfish Synodus saurus Linnaeus, 1758 and royal flagfin Aulopus filamentosus Bloch, 1792 from Cretan Sea, Greece. Parasitology Research, 112, 2055–2061.
https://doi.org/10.1007/s00436-013-3366-7
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. Systematic Parasitology, 43, 209–216.
https://doi.org/10.1023/A:1006144721096Katharios, P., Garaffo, M., Sarter, K., Athanassopoulou, F. & Mylonas, C.C. (2007) A case of high mortality due to heavy infestation of Ceratomyxa diplodae in sharpsnout sea bream (Diplodus puntazzo) treated with reproductive steroids. Bulletin of the European Association of Fish Pathologists, 27, 43–47.
Kaur, H. & Katoch, A. (2016) Prevalence, site and tissue preference of myxozoan parasites infecting gills of cultured fish in Punjab (India). Diseases of Aquatic Organisms, 118, 129–137.
https://doi.org/10.3354/dao02959Kent, M.L., Andree, K.B., Bartholomew, J.L., El-Matbouli, M., Desser, S.S., Devlin, R.H., Feist, S.W., Hedrick, R.P., Hoffmann, R.W., Khattra, J., Hallett, S.L., Lester, R.J., Longshaw, M., Palenzuela, O., Siddal, M.E. & Xiao, C. (2001) Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology, 48 (4), 395–413.
https://doi.org/10.1111/j.1550-7408.2001.tb00173.xKent, M.L., Watral, V.G. & Whipps, C.M. (2004) A Digenean Metacercaria (Apophallus sp.) and a Myxozoan (Myxobolus sp.) associated with vertebral deformities in cyprinid fishes from the Willamette River, Oregon. Journal of Aquatic Animal Health, 16, 116–129.
https://doi.org/10.1577/H04-004.1Kim, W.S., Kim, J.H. & Oh, M.J. (2013) Morphologic and Genetic Evidence for Mixed Infection with Two Myxobolus Species (Myxozoa: Myxobolidae) in Gray Mullets, Mugil cephalus, from Korean Waters. Korean journal of Parasitology, 51 (3), 369–373.
https://doi.org/10.3347/kjp.2013.51.3.369Kodádková, A., Dyková, I, Tyml T., Ditrich, O. & Fiala, I. (2014) Myxozoa in high Arctic: Survey on the central part of Svalbard archipelago. International Journal for Parasitology: Parasites and Wildlife, 3 (1), 41–56.
https://doi.org/10.1016/j.ijppaw.2014.02.001Køie, M. & Karlsbakk, E. (2009) Ellipsomyxa syngnathi sp. n. (Myxozoa, Myxosporea) in the pipefish Syngnathustyphle and S. rostellatus (Teleostei, Syngnathidae) from Denmark. Parasitology Research, 105, 1611−1616.
https://doi.org/10.1007/s00436-009-1598-3Køie M., Karlsbakk E. & Nylund A. (2007) A new genus Gadimyxa with three new species (Myxozoa, Parvicapsulidae) parasitic in marine fish (Gadidae) and the two–host life cycle of Gadimyxa atlantica n. sp. Journal of Parasitology 93, 1456–1467.
https://doi.org/10.1645/GE-1256.1Køie, M., Steffensen, J.F., Moller, P.R. & Christiansen, J.S. (2008) The parasite fauna of Arctogadus glacialis (Peters) (Gadidae) from western and eastern Greenland. Polar Biololgy, 31, 1017–1021.
https://doi.org/10.1007/s00300-008-0440-1
Koprivnikar, J., Koehler, A., Rodd, F.H. & Desser, S.S. (2002) Environmental factors affecting the distribution and abundance of cyst-forming myxobolus spp. and their cyprinid hosts in 3 lakes in algonquin park, Ontario. Journal of Parasitology, 88(3), 467–473.
https://doi.org/10.1645/0022-3395(2002)088[0467:EFATDA]2.0.CO;2
Kovaljova, A.A. & Gaevskaya, A.V. (1983) New data on fish Myxosporidia from open waters of the southeastern Pacific Ocean. Vestnik Zoologii, 1, 6–11. [in Russian]
Kpatcha, T.K., Diebakate, C. & Toguebaye, B.S. (1996) Myxosporidia (Myxozoa, Myxosporea) of the genera Sphaeromyxa Thelohan,1892, Myxidium Buetschli, 1882, Zschokkella Auerbach, 1910, Bipteria Kovaljova, Zubtchenko & Krasin, 1983 and Leptotheca Thélohan, 1895 parasites of fish from the coast of Senegal (West Africa). Journal of African Zoology, 110, 309–317
Kudo, R. (1920) Studies on Myxosporidia. A synopsis of genera and species of myxosporidia. Illinois Biological Mongraphs, 5, 1–265.
Laamiri, S. (2014) New observations on Myxozoa of the goldline sea bream Sarpa salpa L. 1758 (Teleostei : Sparidae) from the Mediterranean coast of Tunisia. Zootaxa, 3887 (2), 157–190.
https://doi.org/10.11646/zootaxa.3887.2.3
Laird, M. (1953) The Protozoa of New Zealand intertidal zone fishes. Transactions of the Royal Society of New Zealand, 81, 79–143.
Lenfant, P. & Olive, C. (1998) Changements graduels du régime alimentaire des juvéniles d’oblade (Oblada melanura, Sparidae) lors du recrutement. Cybium, 22, 203–211.
Lom, J. & Arthur, R. (1989) A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases, 12, 151–156.
https://doi.org/10.1111/j.1365-2761.1989.tb00287.xLom, J. & Dyková, I. (1992) Protozoan Parasites of Fishes. Elsevier, New York, 315 pp.
Lom, J. & Dyková, I. (1993) Scanning electron microscopic revision of common species of the genus Chloromyxum (Myxozoa: Myxosporea) infecting European freshwater fishes. Folia Parasitologica, 40, 161−174
Lom, J. & Dykova, I. (1995) New species of the genera Zschokkella and Ortholinea (Myxozoa) from the Southeast Asian teleost fish, Telraodon fluviatilis. Folia Parasitologica, 42, 161–168.
Lom, J. & Dyková, I. (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica, 53 (1), 1–36.
Lubat, V., Radujkovic, B., Marques, A. & Bouix, G. (1989) Parasites de poissons marins du Montenegro: Myxosporidies. Acta Adriatica, 30, 31–50
Mackenzie, K. & Kalavati, C. (2014) Myxosporean parasites of marine fishes: their distribution in the world’s oceans. Parasitology, 141, 1709–1717.
https://doi.org/10.1017/S0031182014001425MacKenzie, K., Kalavati, C., Gaard, M. & Hemmingsen, W. (2005) Myxosporean gall bladder parasites of gadid fishes in the North Atlantic: Their geographical distributions and an assessment of their economic importance in fisheries and mariculture. Fish Research, 76 (3), 454–465.
https://doi.org/10.1016/j.fishres.2005.07.014Maigret, J. & Ly, B. (1986) Les poissons de mer de Mauritanie (Fishes of Mauritania). Science Nature, 213 pp.
Mansour, L., Al-Qahtani, H.A., Al-Quraishy, S. & Abdel-Baki A.A.S. (2014) Molecular and Morphometric Characteristics of Ceratomyxa hamour n. sp. (Myxosporea: Bivalvulida) Infecting the Gall bladder of the Orange-spotted Grouper Epinephelus coioides from the Arabian Gulf, Saudi Arabia. Journal of Eukaryotic Microbiology, 62, 95–101.
https://doi.org/10.1111/jeu.12148-4521Meglitsch, P.A. (1960) Some coelozoic myxosporidia from New Zealand fishes. I. General and family Ceratomyxidae. Transactions of the Royal Society of New Zealand, 88, 265–356.
Merella P., Garippa G. & Salati F. (2006). Parasites of cage cultured European seabass Dicentrarchus labrax and gilthead seabream Sparus aurata from Sardinia (western Mediterranean): first results. Parassitologia, 48, 290.
Mladineo, I. (2003) Myxosporidean infections in Adriatic cage reared. Bulletin of the European Association of Fish Pathologists, 23 (3), 113–122.
Mladineo, I. (2006a). Parasites of Adriatic cage reared fish. Acta Adriatica, 47, 23–28.
Mladineo, I. (2006b) Check list of the parasitofauna in Adriatic Sea cage-reared fish. Acta Veterinaria, 56 (2–3), 285–292.
https://doi.org/10.2298/AVB0603285MUDK619:639.2.09Moran, J.D.W. & Kent, M.L. (1999) Kudoa thyrsites (Myxozoa: Myxosporea) infections in pen-reared Atlantic salmon in the eastern North Pacific Ocean, with a survey of potential non salmonid reservoir hosts. Journal of Aquatic Animal Health, 11, 101–109.
https://doi.org/10.1577/1548-8667(1999)011<0101:KTMMII>2.0.CO;2Moran, J.D.W., Whitaker, D.J. & Kent, M.L. (1999) Natural and laboratory transmission of the marine myxosporean parasite Kudoa thyrsites (Gilchrist, 1924) to Atlantic salmon. Journal of Aquatic Animal Health, 11, 110–115.
https://doi.org/10.1577/1548-8667(1999)011<0110:NALTOT>2.0.CO;2Morrison, C.M., Martell, D.J., Leggiadro, C. & O’Neil, D. (1996) Ceratomyxa drepanopsettae in the gall bladder of Atlantic halibut, Hippoglossus hippoglossus, from the northwest Atlantic Ocean. Folia Parasitologica, 43, 20–36.
Moser, M., Kent, L. & Dennis, D. (1989) Gall bladder myxosporea in coral reef fishes from Heron Island, Australia. Australian Journal of Zoology, 37, 1–13.
https://doi.org/10.1071/ZO9890001Moser, M. & Noble, E.R. (1975) The myxosporidian genus Davisia in two deep-sea fishes. Journal of Parasitology, 61, 691–694.
https://doi.org/10.2307/3279466Moser, M. & Noble, E.R. (1977) Zschokkella (Protozoa: Myxosporida) in Macrourid fishes. International Journal of Parasitology, 7, 97–100.
https://doi.org/10.1016/0020-7519(77)90073-XNandi, N.C., Kalavati, C., Das, A.K. & Nandi, R. (2004) State fauna series 5: Fauna of Andhra Pradesh-Part 6 (Protozoa). Zoological Survey of India, Kolkata, 422 pp.
Padma Dorothy, K., Kalavati, C. & Vaidchi, J. (1998) Three new species of myxozoans from teleosts of Bay of Bengal. Rivista di Parassitologia, 15, 67–72.
Padrós, F., Palenzuela, O., Hispano, C., Tosas, O., Zarza, C., Crespo, S. & Alvarez-Pellitero, P. (2001) Myxidium leei (Myxozoa) infections in aquarium-reared Mediterranean fish species. Diseases of Aquatic Organisms, 47, 57–62.
https://doi.org/10.3354/dao047057Palenzuela, O., Sitjá-Bobadilla, A. & Alvarez-Pellitero, P. (1997) Ceratomyxa sparusaurati (Protozoa: Myxosporea) infections in cultured gilthead sea bream Sparus aurata (Pisces: Teleostei) from Spain: aspects of the host–parasite relationship. Parasitology Research, 83, 539–548.
https://doi.org/10.1007/s004360050295Pallaoro, A., Santic, M. & Jardas, I. (2003) Feeding habits of the saddled bream, Oblada melanura (Sparidae), in the Adriatic Sea. Cybium, 27 (4), 261–268.
Paperna, I. & Baudin-Laurencin, F. (1979) Parasitic infections of sea bass, Dicentrarchus labrax, and gilt head sea bream, Sparus aurata, in mariculture facilities in France. Aquaculture, 16, 173–175.
https://doi.org/10.1016/0044-8486(79)90148-0Parisi, B. (1912) Primo contributo alla distribusione geografica dei missosporidi in Italia. Atti della Societá Italiana de Scienza Naturalle, 50, 283–290.
Poulin, R. (1996). Sexual inequalities in helminth infections: a cost of being male? American Naturalist, 147, 287–295.
Rajendran, K.V. & Janardanan, K.P. (1992) Ceratomyxa etroplusi sp. n. (Protozoa, Myxozoa) from the gall bladder of the brackishwater fish, Etroplus maculatus (Bloch). Acta Protozoologica, 31, 177–180.
Ray, R.A., Holt, R.A. & Bartholomew, J.L. (2012) Relationship between temperature and Ceratomyxa shasta-induced mortality in Klamath River salmonids. Journal of Parasitology, 98, 520–526.
https://doi.org/10.1645/JP-GE-2737.1
Reed, C.C., Basson, L., Van As, L.L. & Dyková, I. (2007) Four new myxozoans (Myxosporea: Bivalvulida) from intertidal fishes along the south coast of Africa. Folia Parasitologica, 54, 283–292.
https://doi.org/10.14411/fp.2007.037Reiczigel, J. (2003) Confidence intervals for the binomial parameter: some new considerations. Statistics in Medicine, 22, 611–621.
https://doi.org/10.1002/sim.1320Reiczigel, J. & Rózsa, L. (2005) Quantitative Parasitology 3.0. Distributed by the authors, Budapest, 4 pp.
Rigos, G., Christophilogiannis, P., Yiagnisi, M., Andriopoulou, A., Koutsodimou, M., Nengas, I. & Alexis, M. (1999) Myxosporean infections in Greek mariculture. Aquaculture International, 7, 361–364.
https://doi.org/10.1023/A:1009200732200Rocha, S., Casal, G., Rangel, L., Severino, R., Castro, R., Azevedo, C. & Santos, M.J. (2013) Ultrastructural and phylogenetic description of Zschokkella auratis sp. nov. (Myxozoa), a parasite of the gilthead seabream Sparus aurata. Diseases Of Aquatic Organisms, 107, 19–30. https://doi.org/10.3354/dao02661
Sakiti, N. (1982) Recherches ultrastructurales et biologiques sur quelques myxosporidies parasites de serranidés (Poissons, Téléostéens). Thèse de doctorat, Université des Sciences et Techniques du Languedoc, Montpellier, 222 pp.
Sarkar, N.K. (2010) Myxodavisia haldarae sp. n. and Ceratomyxa sardinellae sp. n. (Myxosporea, Bivalvulida) from the gall bladder of Indian Sardine Sardinella longiceps collected in the Bay of Bengal. Protistology, 6 (4), 290–296
Schärer, L. & Vizoso, D.B. (2003) Earlier sex change in infected individuals of the protogynous reef fish Thalassoma bifasciatum. Behaviour Ecology Sociobiology, 55, 137–143. https://doi.org/10.1007/s00265-003-0694-0
Shulman, S.S. (1966) Myxosporidia of the USSR. Nauka Publishers, Moscow-Leningrad, 631 pp.
Siau, Y. & Bouain, A. (1994) Variations in spawning of two species of coastal hermaphrodite fishes, genus Serranus, related to their bathymetric distribution. Oebalia, 10, 1–20.
Siau, Y. & Sakiti, N. (1981) The species Ceratomyxa (Myxosporidae) in Serranidae (fishes, Teleosta). Archives Institute Pasteur Tunis, 58 (3), 431–439.
Sitjá-Bobadilla, A. (2008) Fish immune response to myxozoan parasites. Parasite, 15, 420–425. https://doi.org/10.1051/parasite/2008153420
Sitjá-Bobadilla, A. (2009) Can myxosporean parasites compromise fish and amphibian reproduction? Proceedings of the Royal Society B: Biological Sciences, 276, 2861–2870. https://doi.org/10.1098/rspb.2009.0368
Sitjá-Bobadilla, A. & Alvarez-Pellitero, P. (1990) Sphaerospora testicularis sp. nov. (Myxosporea: Sphaerosporidae) in wild and cultured sea bass, Dicentrarchus labrax (L.), from the Spanish Mediterranean area. Journal of Fish Diseases, 13, 193–203.
https://doi.org/10.1111/j.1365-2761.1990.tb00774.xSitjá-Bobadilla, A. & Alvarez-Pellitero, P. (1992) Light and electron microscopic description of Sphaerospora dicentrarchi n. sp. (Myxosporea: Sphaerosporidae) from wild and cultured sea bass, Dicentrarchus labrax L. Journal of Protozoology, 39, 273–281.
https://doi.org/10.1111/j.1550-7408.1992.tb01314.xSitjá-Bobadilla, A. & Alvarez-Pellitero, P. (1993a) 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). Systematic Parasitology, 26, 215–223.
https://doi.org/10.1007/BF00009729Sitjá-Bobadilla, A. & Alvarez-Pellitero, P. (1993b) Pathologic effects of Sphaerospora dicentrarchi Sitjá-Bobadilla and Alvarez-Pellitero, 1992 and S. testicularis Sitjá-Bobadilla and Alvarez-Pellitero, 1990 (Myxosporea: Bivalvulida) parasitic in the Mediterranean sea bass Dicentrarchus labrax L.(Teleostei: Serranidae) and the cell-mediated immune reaction: a light and electron microscopy study. Parasitology Research, 79, 119–129.
https://doi.org/10.1007/BF00932257Sitjá-Bobadilla, A. & Alvarez-Pellitero, P. (1993c) Population dynamics of Sphaerospora dicentrarchi Sitjá-Bobadilla and Alvarez-Pellitero, 1992 and S. testicularis Sitjá-Bobadilla and Alvarez-Pellitero, 1990 (Myxosporea: Bivalvulida) infections in wild and cultured Mediterranean sea bass (Dicentrarchus labrax L.). Parasitology, 106, 39–45.
Sitjá-Bobadilla, A. & Alvarez-Pellitero, P. (1993d) Ultrastructural and cytochemical observations on the sporogenesis of Sphaerospora testicularis (Protozoa: Myxosporea) from Mediterranean Sea bass, Dicentrarchus labrax (L.). Europeen Journal of Protistology, 29, 219–229. https://doi.org/10.1016/S0932-4739(11)80276-2
Sitjá-Bobadilla, A. & Alvarez-Pellitero, P. (1993e) Zschokkella mugilis n. sp (Myxosporea: Bivalvulida) from mullets (Teleostei: Mugilidae) of Mediterranean waters: light and electron microscopic description. Journal of Eukaryotic Microbiology, 40, 755–764. https://doi.org/10.1111/j.1550-7408.1993.tb04471.x
Sitjá-Bobadilla, A. & Alvarez-Pellitero, P. (2001) Leptotheca sparidium n. sp. (Myxosporea: Bivalvulida), a parasite from cultured common dentex (Dentex dentex L.) and gilthead seabream (Sparus aurata L.) (Teleostei: Sparidae). Journal of Eukaryotic Microbiology, 48, 627–639. https://doi.org/10.1111/j.1550-7408.2001.tb00202.x
Sitjá-Bobadilla, A., Palenzuela, O. & Alvarez-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. Journal of Eukaryotic Microbiology, 42, 529–539.
https://doi.org/10.1111/j.1365-2761Skuratovskaya, E.N., Yurakhno, V.M. & Zavyalov, A.V. (2013) The influence of parasitic infection on the black sea whiting merlangius merlangus euxinus (Gadidae) morphophysiological and biochemical parameters. Vestnik zoologii, 47 (4), 309–317.
https://doi.org/10.2478/vzoo-2013-0032SPSS Inc. (2007) SPSS Base 16.0 User’s Guide. Chicago, IL, 527 pp.
Supamattaya, K., Fischer-Scherl, T., Hoffmann, R.W. & Boonyaratpalin, S. (1991) Sphaerospora epinepheli n. sp. (Myxosporea:Sphaerosporidae) observed in grouper (Epinephelus malabaricus). Journal of Eukaryotic Microbiology, 38, 448–454.
https://doi.org/10.1111/j.1550-7408.1991.tb04815.xSwearer, S.E. & Robertson, D.R. (1999) Life History, Pathology, and Description of Kudoa ovivora n. sp. (Myxozoa, Myxosporea): An Ovarian Parasite of Caribbean Labroid Fishes. Journal of Parasitology, 85 (2), 337–353.
https://doi.org/10.2307/3285645Thélohan, P. (1892) Myxosporidies de la vésicule biliaire des poissons. Compte Rendu Hebdomadaire des Séances de l’Académie des Sciences, 115, 1091–1094.
Thélohan, P. (1895) Recherches sur les myxosporidies. Bulletin Scientifique de la France et Belgique, 24 (5), 100–394.
Tops, S., Lockwood, W. & Okamura, B. (2006) Temperature-driven proliferation of Tetracapsuloides bryosalmonae in bryozoan hosts portends salmonid declines. Diseases of Aquatic Organisms, 70, 227–236.
https://doi.org/10.3354/dao040033
Tortonese, E. (1986) Serranidae. In: Whitehead, P.J.P., Bauchot, M.L., Hureau, J.C., Nielsen, J. & Tortonese, E. (Eds.), Fishes of the Northeastern Atlantic and the Mediterranean, Vol. 2. United Nations Educational, Scientific and Cultural Organization (UNESCO), Paris, pp. 780–792.
U-taynapun, K., Chirapongsatonkulb, N., Maneesaayc, P., Itamid, T. & Tantikitti, C. (2012) A new host record of Sphaerospora epinepheli (Myxosporea: Bivalvulida) occurring on orange-spotted grouper Epinephelus coioides from Thailand: epidemiology, histopathology and phylogenetic position. Veterinary Parasitology, 188, 215–224.
https://doi.org/10.1016/j.vetpar.2012.04.002Valtomen, E.T., Holmes, J.C. & Koskivaara, M. (1997) Eutrophisation, pollution and fragmentation: effects on parasite communities in roach (Rutilus rutilus) and perch (Perca fluviatilis) in four lakes in Central Finland. Canadian Journal of Fishes Aquatic Science, 54, 572–585.
https://doi.org/10.1139/f96-306Wu, Z., Wu, J. & Hua. D. (1993) A study on Myxosporidia of fishes from south China Sea, I: Five new species of Ceratomyxa. Tropic Oceanology, 12, 79–87.
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. Journal of Fish Diseases, 10, 871–879. https://doi.org/10.1111/jfd.12088
Yokoyama, H. (2003) A review: gaps in our knowledge on myxozoan parasites of fishes. Fish Pathology, 38, 125–136.
https://doi.org/10.3147/jsfp.38.125Yokoyama, H. & Fukuda, Y. (2001) Ceratomyxa seriolae n. sp. and C. buri n. sp. (Myxozoa: Myxosporea) from the gall bladder of cultured yellowtail Seriola quinqueradiata. Systematic Parasitology, 48, 125–130.
https://doi.org/10.1023/A:1006432526089Yokoyama, H., Grabner, D. & Shirakashi, S. (2012) Transmission biology of the Myxozoa. In: Carvalho, E., David, G.S. & Silva, R.J. (Eds.), Health and Environment in Aquaculture. InTech, Rijeka, Croatia, pp. 3–42.
https://doi.org/10.5772/29571Yokoyama, H., Abe, N., Maehara, T. & Suzuki, J. (2014) First record of Unicapsula seriolae (Myxozoa: Multivalvulida) from the muscle of Malabar grouper Epinephelus malabaricus in Japan. Parasitology International, 63 (3), 561–566.
https://doi.org/10.1016/j.parint.2014.03.002Yoshino, T.P. & Noble, E.R. (1973) Myxosporidia in macrourid fishes of the North Atlantic. Canadian Journal of Zoology, 51, 745–752.
https://doi.org/10.1139/z73-109Yurakhno, V. M. (2009) The Black Sea and the Sea of Azov fish diseases induced by myxosporeans (Myxozoa: Myxosporea). Ecologiya Morya, 77, 33–37.
Zhang, Z.Q. (2013) Animal biodiversity: An update of classification and diversity in 2013. In: Zhang, Z.-Q. (Ed.), Animal Biodiversity: An Outline of Higher-level Classification and Survey of Taxonomic Richness (Addenda 2013). Zootaxa, 3703 (1), 1–82.
https://doi.org/10.11646/zootaxa.3703.1.3Zhao, Y., Zhou, Y., Kent, M.L. & Whipps, C.M. (2008) Replacement of the preoccupied name Davisia Laird 1953 and Description of a new species (Myxosporea: Sinuolineidae) from Sebastiscus marmoratus (Cuvier 1829) in the east China Sea. Journal of Parasitology, 94, 269–279.
https://doi.org/10.1645/GE-1232.1