First report of three multivalvulid species (Cnidaria: Myxozoa: Myxosporea) in commercial fishes from Java Sea, Indonesia, with records of Unicapsula pyramidata and two new Kudoa spp.

Abstract

Commercial marine fishes caught locally in East Java, Indonesia, were examined for multivalvulid myxosporeans (Cnidaria: Myxozoa: Myxosporea). Plasmodia of Unicapsula pyramidata were detected in the trunk muscle of two fork-tailed threadfin breams (Nemipterus furcosus). Genetic comparisons of this sample to those collected in the Australian Coral Sea and South China Sea showed few nucleotide substitutions in the small subunit and large subunit ribosomal RNA gene (rDNA) with the species isolated in the Australian Coral Sea and South China Sea. Pseudocysts of two new Kudoa spp. with four shell valves and polar capsules were found in the trunk muscle of two shrimp scads Alepes djedaba and two flathead grey mullets Mugil cephalus. Kudoa javaensis n. sp. myxospores isolated from the shrimp scad were 5.1–7.2 (mean 6.2) μm thick, 6.2–7.9 (7.3) μm wide, and 4.6–6.3 (5.4) μm long, with polar capsules 1.9–2.5 (2.2) μm long and 1.1–1.4 (1.3) μm wide (n = 15). Kudoa surabayaensis n. sp. myxospores isolated from the flathead grey mullet were 5.8–6.7 (6.3) μm thick, 6.4–7.6 (6.9) μm wide, and 4.6–5.0 (4.7) μm long, with polar capsules 1.8–2.4 (2.1) μm long and 0.9–1.3 (1.1) μm wide (n = 25). These two Kudoa spp. showed critical differences in spore shapes (semiquadrate with unequal shell valves vs. equal shell valves), and absence vs. presence of uplifted shell valve termini. Nucleotide sequencing of rDNA supported the morphological differentiation of these two species. Furthermore, these two isolates were morphologically and phylogenetically distinct from any recorded Kudoa spp.

This is a preview of subscription content, access via your institution.

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

References

  1. Abdel-Baki AS, Abdel-Haleem HM, Al-Quraishy S, Azevedo C, Mansour L (2018) Ultrastructural and molecular characteristics of Kudoa crenimugilis n. sp. infecting intestinal smooth muscle of fringelip mullet Crenimugil crenilabis in the Red Sea. Dis Aquat Org 129:53–62

    CAS  Article  Google Scholar 

  2. Akaishi F, Easy R, St-Jeans S, Courtenary S, Ribeiro CA, Cone D (2004) Supplemental diagnosis of Kudoa funduli (Myxozoa) parasitizing Fundulus heteroclitus (Cyprinodontidae) from coastal northeastern North America. J Parasitol 90:477–480

    PubMed  Article  Google Scholar 

  3. Alama-Bermejo G, Cuadrado M, Raga JA, Holzer AS (2009) Morphological and molecular redescription of the myxozoan Unicapsula pflugfelderi Schubert, Sprague & Reinboth 1975 from two teleost hosts in the Mediterranean. A review of the genus Unicapsula Davis 1924. J Fish Dis 32:335–350

    CAS  PubMed  Article  Google Scholar 

  4. Al-Jufaili SH, Freeman MA, Machkevskyi VK, Al-Nabhani A, Palm HW (2016) Morphological, ultrastructural, and molecular description of Unicapsula fatimae n. sp. (Myxosporea: Trilosporidae) of whitespotted rabbitfish (Siganus canaliculatus) in Omani waters. Parasitol Res 115:1173–1184

    PubMed  Article  Google Scholar 

  5. Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552

    PubMed  Article  Google Scholar 

  6. Arai Y, Matsumoto K (1953) On a new sporozoa, Hexacapsula neothunni gen. et sp. nov., from the muscle of yellowfin tuna, Neothunnus macropterus. Bull Jpn Soc Sci Fish 18:293–299

    Article  Google Scholar 

  7. Atkinson SD, Bartošová-Sojková P, Whipps CM, Bartholomew JL (2015) Approaches for characterising myxozoan species. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer International Publishing Switzerland, Cham, pp 111–123

    Google Scholar 

  8. Bartošová-Sojková P, Kodádková A, Peckova H, Kuchta R, Reed CC (2015) Morphology and phylogeny of two new species of Sphaeromyxa Thélohan, 1892 (Cnicaria: Myxozoa) from marine fish (Clinidae and Trachichthyidae). Parasitology 142:660–674

    PubMed  Article  Google Scholar 

  9. Burger MAA, Adlard RD (2010a) Four new species of Kudoa Meglitsch, 1947 (Myxosporea: Multivalvulida) from Australia with recommendations for species descriptions in the Kudoidae. Parasitology 137:793–814

    CAS  PubMed  Article  Google Scholar 

  10. Burger MAA, Adlard RD (2010b) Phenotypic variation in a significant spore character in Kudoa (Myxosporea: Multivalvulida) species infecting brain tissue. Parasitology 137:1759–1772

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. Burger MAA, Adlard RD (2011) Low host specificity in the Kudoidae (Myxosporea: Multivalvulida) including seventeen new host records for Kudoa thalassomi. Folia Parasitol 58:1–16

    Article  Google Scholar 

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  13. Burger MAA, Barnes AC, Adlard RD (2008) Wildlife as reservoirs for parasites infecting commercial species: host specificity and a redescription of Kudoa amamiensis from teleost fish in Australia. J Fish Dis 31:835–844

    CAS  PubMed  Article  Google Scholar 

  14. Cardim J, Araújo-Neto J, da Silva DT, Hamoy I, Matos E, Abrunhosa F (2020) Kudoa yasai n. sp. (Multivalvulida: Kudoidae) from the skeletal muscle of Macrodon ancylodon (Sciaenidae) on the northern Atlantic coast, Brazil. Parasitol Res (in press). https://doi.org/10.1007/s00436-020-06679-3

  15. Casal G, Soares EC, Rocha S, Silva TJ, Santos EL, Nascimento R, Oliveira E, Zaevedo C (2019) Description of a new myxozoan Kudoa eugerres n. sp. and reclassification of two Sphaerospora sensu lato species. Parasitol Res 118:1719–1730

    PubMed  Article  Google Scholar 

  16. Davis HS (1924) A new myxosporidian parasite, the cause of “wormy” halibut. Report of the U. S. Commercial Fisheries for 1923. Appendix 8:1–5

    Google Scholar 

  17. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie J-M, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:465–469

    Article  CAS  Google Scholar 

  18. Diamant A, Ucko M, Paperna I, Colorni A, Lipshitz A (2005) Kudoa iwatai (Myxosporea: Multivalvulida) in wild and cultured fish in the Red Sea: redescription and molecular phylogeny. J Parasitol 91:1175–1189

    CAS  PubMed  Article  Google Scholar 

  19. Dyková I, Lom J, Overstreet RM (1994) Myxosporean parasites of the genus Kudoa Meglitsch, 1947 from some Gulf of Mexico fishes: description of two new species and notes on their ultrastructure. Eur J Protistol 30:316–323

    Article  Google Scholar 

  20. Dyková I, de Buron I, Fiala I, Roumillat WA (2009) Kudoa inornata sp. n. (Myxosporea: Multivalvulida) from the skeletal muscles of Cynoscion nebulosus (Teleostei: Sciaenidae). Folia Parasitol 56:91–98

    Article  Google Scholar 

  21. Egusa S (1986) The order Multivalvulida Shulman, 1959 (Myxozoa: Myxosporea): a review. Fish Pathol 21:261–274 (in Japanese with English summary)

    Article  Google Scholar 

  22. Egusa S, Nakajima K (1980) Kudoa amamiensis n. sp. (Myxosporea: Multivalvulida) found in cultured yellowtails and wild damselfishes from Amami-Ohshima and Okinawa, Japan. Bull Jpn Soc Sci Fish 46:1193–1198

    Article  Google Scholar 

  23. Egusa S, Shiomitsu T (1983) Two new species of the genus Kudoa (Myxosporea: Multivalvulida) from marine cultured fishes in Japan. Fish Pathol 18:163–171 (in Japanese with English summary)

    Article  Google Scholar 

  24. Eiras JC, Saraiva A, Cruz C (2014) Synopsis of the species of Kudoa Meglitsch, 1947 (Myxozoa: Myxosporea: Multivalvulida). Syst Parasitol 87:153–180

    PubMed  Article  PubMed Central  Google Scholar 

  25. Fiala I, Bartošová-Sojková P, Whipps CM (2015) Classification and phylogenetics of Myxozoa. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer International Publishing Switzerland, Cham, pp 85–110

    Google Scholar 

  26. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    PubMed  Article  PubMed Central  Google Scholar 

  27. Heiniger H, Cribb TH, Adlard RD (2013) Intra-specific variation of Kudoa spp. (Myxosporea: Multivalvulida) from apogonid fishes (Perciformes), including the description of two new species, K. cheilodipteri n. sp. and K. cookii n. sp., from Australian waters. Syst Parasitol 84:193–215

    PubMed  Article  PubMed Central  Google Scholar 

  28. Hervio DML, Khattra J, Devlin RH, Kent ML, Sakanari J, Yokoyama H (1997) Taxonomy of Kudoa species (Myxosporea), using a small-subunit ribosomal DNA sequence. Can J Zool 75:2112–2119

    CAS  Article  Google Scholar 

  29. Hsieh S, Chen C (1984) Septemcapsula yasunagai gen. et sp. nov., representative of a new family of the class Myxosporea. Acta Zootax Sin 9:225–227 (in Chinese with English summary)

    Google Scholar 

  30. Jirků M, Vartošová P, Kodádková A, Mutschmann F (2011) Another chloromyxid lineage: molecular phylogeny and redescription of Chloromyxum careni from the Asian horned frog Megophrys nasuta. J Eukaryot Microbiol 58:50–59

    PubMed  Article  Google Scholar 

  31. Joy JE (1972) A new species of Kudoa (Myxosporidea: Chloromyxidae) from the spot, Leiostomus xanthurus Lacépede, in Clear Lake, Texas. J Protozool 19:264–265

    CAS  PubMed  Article  Google Scholar 

  32. Kabata Z, Whitaker DJ (1981) Two species of Kudoa (Myxosporea: Multivalvulida) parasitic in the flesh of Merluccius productus (Ayres, 1855) (Pisces: Teleostei) in the Canadian Pacific. Can J Zool 59:2085–2091

    Article  Google Scholar 

  33. Kasai A, Li Y-C, Setsuda A, Mafie E, Sato H (2015) Genetic characterization of Kudoa iwatai and Kudoa trachuri in commercial marine fish (Platycephalus sp. and Trachurus japonicus) for human consumption. Jpn J Vet Parasitol 14:22–30

    Google Scholar 

  34. Kasai A, Li Y-C, Mafie E, Sato H (2016a) Morphological and molecular genetic characterization of two Kudoa spp., K. musculoliquefaciens, and K. pleurogrammi n. sp. (Myxosporea: Multivalvulida), causing myoliquefaction of commercial marine fish. Parasitol Res 115:1883–1892

    PubMed  Article  Google Scholar 

  35. Kasai A, Li Y-C, Mafie E, Sato H (2016b) New host records of monacanthid fish for three Kudoa spp. (K. septempunctata, K. thyrsites, and K. shiomitsui) prevalent in the olive flounder (Paralichthys olivaceus), with the description of K. parathyrsites n. sp. from a black scraper (Thamnaconus modestus). Parasitol Res 115:2741–2755

    PubMed  Article  PubMed Central  Google Scholar 

  36. Kasai A, Setsuda A, Sato H (2017a) Morphological and genetic characterization of Kudoa whippsi (Myxosporea: Multivalvulida) from Cheilodactylus zonatus in the western Pacific Ocean off Japan, and two new Kudoa spp. (K. akihitoi n. sp. and K. empressmichikoae n. sp.) from Acanthogobius hasta in the Sea of Ariake, Japan. Parasitol Res 116:647–659

    PubMed  Article  PubMed Central  Google Scholar 

  37. Kasai A, Tsuduki H, Jimenez LA, Li Y-C, Tanaka S, Sato H (2017b) Incidence of three Kudoa spp., K. neothunni, K. hexapunctata, and K. thunni (Myxosporea: Multivalvulida), in Thunnus tunas distributed in the western Pacific Ocean. Parasitol Res 116:1137–1150

    PubMed  Article  PubMed Central  Google Scholar 

  38. Kawai T, Sekizuka T, Yahata Y, Kuroda M, Kumeda Y, Iijima Y, Kamata Y, Sugita-Konishi Y, Ohnishi T (2012) Identification of Kudoa septempunctata as the causative agent of novel food poisoning outbreaks in Japan by consumption of Paralichthys olivaceus in raw fish. Clin Infect Dis 54:1046–1052

    PubMed  Article  PubMed Central  Google Scholar 

  39. Kovaleva AA, Shulman SS, Yakovlev VN (1979) Myxosporidia of the genus Kudoa (Myxosporidia, Multivalvulida) from the basin of the Atlantic Ocean. In: Systematics and ecology of sporozoans and cnidosporidians. Tr Zool Inst Akad Nauk SSSR 87:42–64 (in Russian) [Cited by Whipps and Diggles, 2006]

  40. Lester RJG (1982) Unicapsula seriolae n. sp. (Myxosporea, Multivalvulida) from Australian yellowtail kingfish Seriola lalandi. J Protozool 29:584–587

    Article  Google Scholar 

  41. Li Y-C, Sato H, Tanaka S, Ohnishi T, Kamata Y, Sugita-Konishi Y (2013) Characterization of the ribosomal RNA gene of Kudoa neothunni (Myxosporea: Multivalvulida) in tunas (Thunnus spp.) and Kudoa scomberi n. sp. in a chub mackerel (Scomber japonicus). Parasitol Res 112:1991–2003

    PubMed  Article  Google Scholar 

  42. Li Y-C, Tamemasa S, Zhang J-Y, Sato H (2020a) Phylogenetic characterisation of seven Unicapsula spp. (Myxozoa: Myxosporea: Multivalvulida) from commercial fish in southern China and Japan. Parasitology 147:448–464

    CAS  PubMed  Article  Google Scholar 

  43. Li Y-C, Inoue K, Zhang J-Y, Sato H (2020b) Phylogenetic relationships of three Kudoa spp. with morphologically similar myxospores (K. iwatai, K. lutjanus, and K. bora), with the redescription of K. uncinata and K. petala and description of a new species (K. fujitai n. sp.) in fishes in the South China Sea. Parasitol Res 119:1221–1236

    PubMed  Article  Google Scholar 

  44. Li Y-C, Inoue K, Tanaka S, Zhang J-Y, Sato H (2020c) Identification of four new Kudoa spp. (Myxozoa: Myxosporea: Multivalvulida) in commercial fishes collected from South China Sea, Atlantic Ocean, and Bering Sea by integrated taxonomic approach. Parasitol Res 119:2113–2128

    PubMed  Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  47. Lom J, Dyková I, Lhotáková Š (1983) Kudoa lunata n. sp. (Myxozoa, Myxosporea) and notes on the nature of muscular “cysts” of the genus Kudoa. Arch Protistenkd 127:387–397

    Article  Google Scholar 

  48. Mateo-Salas E (1972) Investigación parasitológica de la merluza (Merluccius gayii peruanus). Instituto del Mar de Peru, Informe 40:5–13 (Spanish)

  49. Matsukane Y, Sato H, Tanaka S, Kamata Y, Sugita-Konishi Y (2010) Kudoa septempunctata n. sp. (Myxosporea: Multivalvulida) from an aquacultured olive flounder (Paralichthys olivaceus) imported from Korea. Parasitol Res 107:865–872

    PubMed  Article  Google Scholar 

  50. Matsumoto K (1954) On the two new Myxosporidia, Chloromyxum musculoliquefaciens sp. nov. and Neochloromyxum cruciformum gen. et sp. nov., from the jellied muscle of swordfish, Xiphias glandius Linné, and Lateolabrax japonicus (Temmink et Schlegel). Bull Jpn Soc Sci Fish 20:469–478

    Article  Google Scholar 

  51. Meglitsch PA (1947) Studies on Myxosporidia from the Beaufort Region. II. Observations of Kudoa clupeidae (Harn), gen. nov. J Parasitol 33:271–277

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  52. Miller TL, Adlard RD (2013) Unicapsula species (Myxosporea: Trilosporidae) of Australian marine fishes, including the description of Unicapsula andersenae n. sp. in five teleost families off Queensland, Australia. Parasitol Res 112:2945–2957

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  53. Moran JDW, Whitaker DJ, Kent ML (1999) A review of the myxosporean genus Kudoa Meglitsh, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172:163–196

    Article  Google Scholar 

  54. Mutschmann F (1999) A new myxozoan, Chloromyxum careni sp. n. (Myxosporea: Chloromyxidae) from the kidney of Megophrys nasuta Schlegel, 1858 (Anura: Pelobatidae) from Indonesia. Acta Protozool 38:83–86

    Google Scholar 

  55. Naidjenova NN, Zaika VE (1970) Three new genera of myxosporean parasites of fish from the Indian Ocean. Zool Zhournal 49:451–454 (in Russian with English summary)

    Google Scholar 

  56. Ohnishi T, Obara T, Arai S, Yoshinari T, Sugita-Konishi Y (2018) Quantitative analysis of Unicapsula seriolae in greater amberjack associated with unidentified food-borne disease. Food Hyg Safe Sci 59:24–29

    CAS  Article  Google Scholar 

  57. Özer A, Okkay S, Gürkanli CT, Çiftçi Y, Yurankhno V (2018) Two novel myxosporean parasites in Black Sea fishes: Kudoa niluferi sp. nov. and Kudoa anatolica sp. nov. (Cnidaria: Myxosporea). Dis Aquat Org 128:225–233

    Article  CAS  Google Scholar 

  58. Pampoulie C, Marques A, Rosecchi E, Crivelli AJ, Bouchereau J-L (1999) A new myxosporean parasite, Kudoa camarguensis n. sp., recorded on two goby species (Teleostei: Pisces) in the Rhône Delta (Mediterranean Sea, France). J Eukaryot Microbiol 46:304–310

    Article  Google Scholar 

  59. Parker JD, Warner MC (1970) Effects of fixation, dehydration and staining on dimensions of myxosporidian and microsporidian spores. J Wildl Dis 6:448–456

    CAS  PubMed  Article  Google Scholar 

  60. Pascual S, Abollo E, Yurakhno V, Gaevskaya A (2012) Molecular characterization of Kudoa nova (Myxosporea: Multivalvulida) infecting the round goby Neogobius melanostomus from the Sea of Azov. Azov Mar Ecol J 11:66–73

    Google Scholar 

  61. Reimschuessel R, Gieseker CM, Driscoll C, Baya A, Kane AS, Blazer VS, Evans JJ, Kent ML, Moran JDW, Poynton SL (2003) Myxosporean plasmodial infection associated with ulcerative lesions in young-of-the-year Atlantic menhaden in a tributary of the Chesapeake Bay, and possible links to Kudoa clupeidae. Dis Aquat Org 53:143–166

    CAS  Article  Google Scholar 

  62. Rukyani A (1990) Histopathological changes in the gills of common carp (Cyprinus carpio L.) infected with the myxosporean parasite Myxobolus koi Kudo, 1920. Asian Fish Sci 3:337–341

    Google Scholar 

  63. Sakai H, Kato E, Sakaguchi S, Setsuda A, Sato H (2018) Morphological and molecular genetic characterization of Kudoa konishiae n. sp. (Myxosporea: Multivalvulida) in the muscle of Japanese Spanish mackerel (Scomberomorus niphonius). Parasitol Res 117:893–904

    PubMed  Article  PubMed Central  Google Scholar 

  64. Sakai H, Kawai T, Zhang J, Sato H (2019) New host records of three Kudoa spp. (K. yasunagai, K. thalassomi, and K. igami) with notable variation in the number of shell valves and polar capsules in spores. Parasitol Res 118:143–157

    PubMed  Article  PubMed Central  Google Scholar 

  65. Sato H, Kasai A (2016) Kudoa species (Myxozoa: Myxosporea: Multivalvulida) recorded in Japan or its surrounding natural waters (1930–2016). Jpn J Vet Parasitol 15:111–138

    Google Scholar 

  66. Shin SP, Shirakashi S, Hamano S, Kato K, Lasso LT, Yokoyama H (2016) Phylogenetic study of the genus Kudoa (Myxozoa: Multivalvulida) with a description of Kudoa rayformis sp. nov. from the trunk muscle of Pacific sierra Scomberomorus sierra. Mol Phylogenet Evol 98:337–345

    PubMed  Article  PubMed Central  Google Scholar 

  67. Sugita-Konishi Y, Sato H, Ohnishi T (2014) Novel foodborne disease associated with consumption of raw fish, olive flounder (Paralichthys olivaceus). Food Safe 2:141–150

    Article  Google Scholar 

  68. Suzuki J, Murata R, Sadamasu K, Kai A (2012) Cases of food poisoning caused possibly by Kudoa spp. in the Tokyo metropolitan area. IASR 33:153–155 (in Japanese)

    Google Scholar 

  69. Suzuki J, Murata R, Yokoyama H, Sadamasu K, Kai A (2015) Detection rate of diarrhea-causing Kudoa hexapunctata in pacific Bluefin tuna Thunnus orientalis from Japanese waters. Int J Food Microbiol 194:1–6

    PubMed  Article  PubMed Central  Google Scholar 

  70. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  71. Tomochi H, Li Y-C, Tran BT, Yanagida T, Sato H (2014) Three Unicapsula species (Myxosporea: Trilosporidae) of Asian marine fishes, including the description of Unicapsula setoensis n. sp. in the yellowfin goby (Acanthogobius flavimanus) from the Inland Sea of Japan. Parasitol Res 113:3807–3816

    PubMed  Article  Google Scholar 

  72. Ward RD, Zemlak TS, Innes BH, Last PR, Hebert DN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc B (Biol Sci) 360:1847–1857

    CAS  Article  Google Scholar 

  73. Whipps CM, Kent ML (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J Eukaryot Microbiol 53:364–373

    CAS  PubMed  Article  Google Scholar 

  74. Whipps CM, Adlard RD, Bryant MS, Kent ML (2003a) Two unusual myxozoans, Kudoa quadricornis n. sp. (Multivalvulida) from the muscle of goldspotted trevally (Carangoides fulvoguttatus) and Kudoa permulticapsula n. sp. (Myltivalvulida) from the muscle of Spanish mackerel (Scomberomorus commerson) from the Great Barrier Reef, Australia. J Parasitol 89:168–173

    CAS  PubMed  Article  Google Scholar 

  75. Whipps CM, Adlard RD, Bryant MS, Lester RJG, Findlay V, Kent ML (2003b) 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 Eukaryot Microbiol 50:215–219

    PubMed  Article  Google Scholar 

  76. Whipps CM, Grossel G, Adlard RD, Yokoyama H, Bryant MS, Munday BL, Kent ML (2004) Phylogeny of the Multivalvulidae (Myxozoa: Myxosporea) based on comparative ribosomal DNA sequence analysis. J Parasitol 90:618–622

    CAS  PubMed  Article  Google Scholar 

  77. Whitaker DJ, Kent ML, Sakanari JA (1996) Kudoa minauriculata n. sp. (Myxozoa, Myxosporea) from the musculature of bocaccio (Sebastes paucispinis) from California. J Parasitol 82:312–315

    CAS  PubMed  Article  Google Scholar 

  78. Whipps CM, Diggles BK (2006) Kudoa alliaria in flesh of Argentinian hoki Macruronus magellanicus (Gadiformes; Merlucciidae). Dis Aquat Org 69:259–263

  79. Yokoyama H, Whipps CM, Kent ML, Mizuno K, Kawakami H (2004) Kudoa thyrsites from Japanese flounder and Kudoa lateolabracis n. sp. from Chinese Sea bass: causative myxozoans of post-mortem myoliquefaction. Fish Pathol 39:79–85

    Article  Google Scholar 

  80. Yokoyama H, Mekata T, Satoh J, Nishioka T, Mori K (2016) Morphological and molecular comparisons between Japanese and Korean isolates of Kudoa septempunctata (Myxozoa: Multivalvulida) in the olive flounder Paralichthys olivaceus. Fish Pathol 52:152–157

    Article  Google Scholar 

  81. Zhang JB, Hanner R (2011) DNA barcoding is a useful tool for the identification of marine fishes from Japan. Biochem Syst Ecol 39:31–42

    Article  CAS  Google Scholar 

  82. Zhou Y, Zhao Y-J (2008) Description of three new species of Kudoa (Myxosporea, Multivalvulida, Kudoiae) parasitic in marine fishes from the East China Sea. Acta Hydrobiol Sin 32(Suppl):51–56 (in Chinese with English summary)

    Google Scholar 

Download references

Acknowledgments

We thank the Faculty of Veterinary Medicine, Airlangga University, for supporting this international collaborative study with the Joint Faculty of Veterinary Medicine, Yamaguchi University, including provision of travelling funds to MY and LRY for travelling to Yamaguchi; the Ministry of Research, Technology and Higher Education of Indonesia (Career and Competency of Human Resources), for providing a travelling fund to DN; and the Organization for Research Initiatives, Yamaguchi University, for providing a travelling fund to SG for the international collaborative research at Yamaguchi University.

Funding

This study was partially supported by a Grant-in-Aid for Food Science and Research 2019 from the Toyo Suisan Foundation (HS), and JSPS KAKENHI grant number 18K05995 (HS). Special thanks are extended for the international research grants to LRY from Airlangga University (2 months), to SG from Yamaguchi University (1 month), and to DN from the Department of Career and Competency of Human Resources, Ministry of Research, Technology and Higher Education of Indonesia (2 months).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Hiroshi Sato.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Section Editor: Christopher Whipps

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yunus, M., Yustinasari, L.R., Natalia, D. et al. First report of three multivalvulid species (Cnidaria: Myxozoa: Myxosporea) in commercial fishes from Java Sea, Indonesia, with records of Unicapsula pyramidata and two new Kudoa spp.. Parasitol Res 120, 861–876 (2021). https://doi.org/10.1007/s00436-020-07030-6

Download citation

Keywords

  • Myxozoa
  • Unicapsula pyramidata
  • Kudoa javaensis n. sp.
  • Kudoa surabayaensis n. sp.
  • Morphology
  • rDNA
  • Java Sea