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Molecular data infers the involvement of a marine aurantiactinomyxon in the life cycle of the myxosporean parasite Paramyxidium giardi (Cnidaria, Myxozoa)

Published online by Cambridge University Press:  15 July 2019

S. Rocha Open the ORCID record for S. Rocha [Opens in a new window] ,
Â. Alves ,
C. Antunes ,
C. Azevedo  and
G. Casal
S. Rocha*
Affiliation:
Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Rua Jorge Viterbo Ferreira no. 228, 4050-313 Porto, Portugal Laboratory of Animal Pathology, Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Terminal de Cruzeiros de Leixões, Av. General Norton de Matos s/n, 4450-208 Matosinhos, Portugal
Â. Alves
Affiliation:
Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Rua Jorge Viterbo Ferreira no. 228, 4050-313 Porto, Portugal
C. Antunes
Affiliation:
Laboratory of Animal Pathology, Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Terminal de Cruzeiros de Leixões, Av. General Norton de Matos s/n, 4450-208 Matosinhos, Portugal Aquamuseu do Rio Minho, Parque do Castelinho, 4920-290 Vila Nova de Cerveira, Portugal
C. Azevedo
Affiliation:
Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Rua Jorge Viterbo Ferreira no. 228, 4050-313 Porto, Portugal Laboratory of Animal Pathology, Interdisciplinary Centre of Marine and Environmental Research (CIIMAR), University of Porto, Terminal de Cruzeiros de Leixões, Av. General Norton de Matos s/n, 4450-208 Matosinhos, Portugal
G. Casal
Affiliation:
University Institute of Health Sciences & Institute of Research and Advanced Training in Health Sciences and Technologies, CESPU, Rua Central da Gandra no. 1317, 4585-116 Gandra, Portugal
*
Author for correspondence: S. Rocha, E-mail: [email protected]
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Abstract

An aurantiactinomyxon type is described from the marine naidid Tubificoides pseudogaster (Dahl, 1960), collected from the lower estuary of a Northern Portuguese River. This type constitutes the first of its collective group to be reported from Portugal, and only the fourth described from a marine oligochaete worldwide. Extensive morphological comparisons of new aurantiactinomyxon isolates to all known types without available molecular data are proposed to be unnecessary, given the artificiality of the usage of morphological criteria for actinosporean differentiation and the apparent strict host specificity of the group. Recognition of naidid oligochaetes as the hosts of choice for marine types of aurantiactinomyxon and other collective groups, suggests that the family Naididae played a preponderant role in the myxosporean colonization of estuarine communities. Molecular analyses of the type in study further infer its involvement in the life cycle of Paramyxidium giardi (Cépède, 1906) Freeman and Kristmundsson, 2018, a species that infects the kidney of European eel Anguilla anguilla (Linnaeus, 1758) and that has been reported globally, including from Portuguese waters. The low intraspecific difference registered in relation to Icelandic isolates of P. giardi (0.6%) is hypothesized to result from the emergence of genotypically different subspecies due to geographic isolation.

Keywords

Actinosporemarine oligochaeteMyxosporeaPortugalRiver MinhoSSU rDNA geneTubificoides pseudogaster
Type
Research Article
Information
Parasitology , Volume 146 , Issue 12 , October 2019 , pp. 1555 - 1563
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Copyright © Cambridge University Press 2019 

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References

Atkinson, SD and Bartholomew, JL (2009) Alternate spore stages of Myxobilatus gasterostei, a myxosporean parasite of three-spined sticklebacks (Gasterosteus aculeatus) and oligochaetes (Nais communis). Parasitology Research 104, 1173–1181.Google Scholar
Atkinson, SD, Bartošová-Sojková, P, Whipps, CM and Bartholomew, JL (2015) Approaches for characterising Myxozoan species. In Okamura, B, Gruhl, A and Bartholomew, JL (eds), Myxozoan Evolution, Ecology and Development. Switzerland: Springer International Publishing, pp. 111–123.Google Scholar
Azevedo, C, Lom, J and Corral, L (1989) Ultrastructural aspects of Myxidium giardi (Myxozoa, Myxosporea), parasite of the European eel Anguilla Anguilla. Diseases of Aquatic Organisms 6, 55–61.Google Scholar
Bartholomew, JL, Whipple, MJ, Stevens, DG and Fryer, JL (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.Google Scholar
Bartholomew, JL, Atkinson, SD and Hallett, SL (2006) Involvement of Manayunkia speciosa (Annelida: Polychaeta: Sabellidae) in the life cycle of Parvicapsula minibicornis, a myxozoan parasite of Pacific salmon. Journal of Parasitology 92, 742–748.Google Scholar
Benajiba, MH and Marques, A (1993) The alternation of actinomyxidian and myxosporidian sporal forms in the development of Myxidium giardi (parasite of Anguilla Anguilla) through oligochaetes. Bulletin of the European Association of Fish Pathologists 13, 100–103.Google Scholar
Cépède, C (1906) Myxidium giardi Cépède, et la prétendue immunité des Anguilles a l’ègard des infections myxosporidiennes. Comptes Rendus des Séances de la Société de Biologie et de ses Filiales 6, 170–173.Google Scholar
Copland, JW (1981) The occurrence and distribution of Myxidium giardi Cépède, 1906 in wild and cultured European eels, Anguilla Anguilla L., in England. Journal of Fish Diseases 4, 231–242.Google Scholar
Dias, E, Morais, P, Cotter, AM, Antunes, C and Hoffman, JC (2016) Estuarine consumers utilize marine, estuarine and terrestrial organic matter and provide connectivity among these food webs. Marine Ecology Progress Series 554, 21–34.Google Scholar
Eiras, JC (2016) Parasites of marine, freshwater and farmed fishes of Portugal: a review. Brazilian Journal of Veterinary Parasitology 25, 259–278.Google Scholar
El-Mansy, A, Székely, C and Molnár, K (1998) Studies on the occurrence of actinosporean stages of fish myxosporeans in a fish farm of Hungary, with the description of triactinomyxon, raabeia, aurantiactinomyxon and neoactinomyxon types. Acta Veterinaria Hungarica 46, 259–284.Google Scholar
Erséus, C, Wetzel, MJ and Gustavsson, L (2008) ICZN rules – a farewell to Tubificidae (Annelida, Clitellata). Zootaxa 1744, 66–68.Google Scholar
Eszterbauer, E, Székely, C, Molnár, K and Baska, F (2000) Development of Myxobolus bramae (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. Journal of Fish Diseases 23, 19–25.Google Scholar
Eszterbauer, E, Marton, S, Rácz, OZ, Letenyei, M and Molnár, K (2006) Morphological and genetic differences among actinosporean stages of fish-parasitic myxosporeans (Myxozoa): difficulties of species identification. Systematic Parasitology 65, 97–114.Google Scholar
Eszterbauer, E, Atkinson, S, Diamant, A, Morris, D, El-Matbouli, M and Hartikainen, H (2015) Myxozoan life cycles: practical approaches and insights. In Okamura, B, Gruhl, A and Bartholomew, JL (eds). Myxozoan Evolution, Ecology and Development. Switzerland: Springer International Publishing, pp. 175–198.Google Scholar
Fiala, I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology 36, 1521–1534.Google Scholar
Freeman, MA and Kristmundsson, A (2018) Studies of Myxidium giardi Cépède, 1906 infections in Icelandic eels identifies a genetically diverse clade of myxosporeans that represents the Paramyxidium n. g. (Myxosporea: Myxidiidae). Parasites and Vectors 11, 551.Google Scholar
Fujita, T (1927) Studies on Myxosporidia of Japan. Journal of the Faculty of Agriculture of the Hokkaido Imperial University 16, 229–247.Google Scholar
Grossheider, G and Körting, W (1992) First evidence that Hoferellus cyprini (Doflein, 1898) is transmitted by Nais sp. Bulletin of the European Association of Fish Pathologists 12, 17–20.Google Scholar
Hallett, SL and 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. Diseases of Aquatic Organisms 46, 197–212.Google Scholar
Hallett, SL and Lester, RJ (1999) Actinosporeans (Myxozoa) with four developing spores within a pansporocyst: Tetraspora discoidea n. g. n. sp. and Tetraspora rotundum n. sp. International Journal of Parasitology 29, 419–427.Google Scholar
Hallett, SL, Erséus, C and Lester, RJ (1997) Actinosporea from Hong Kong marine oligochaeta. In Morton, B (ed.), Proceedings of the Eight International Marine Biological Workshop: The Marine Flora and Fauna of Hong Kong and Southern China. Hong Kong: Hong Kong University Press, pp. 1–7.Google Scholar
Hallett, SL, O'Donoghue, PJ and Lester, RJG (1998) Structure and development of a marine actinosporean, Sphaeractinomyxon ersei n. sp. (Myxozoa). Journal of Eukaryotic Microbiology 45, 142–150.Google Scholar
Hallett, SL, Erséus, C and Lester, RJ (1999) Actinosporeans (Myxozoa) from marine oligochaetes of the Great Barrier Reef. Systematic Parasitology 44, 49–57.Google Scholar
Hallett, SL, Erséus, C, O'Donoghue, PJ and Lester, RJG (2001) Parasite fauna of Australian marine oligochaetes. Memoirs of the Queensland Museum 46, 555–576.Google Scholar
Hallett, SL, Atkinson, SD and El-Matbouli, M (2002) Molecular characterisation of two aurantiactinomyxon (Myxozoa) phenotypes reveals one genotype. Journal of Fish Diseases 57, 1–14.Google Scholar
Hallett, SL, Atkinson, SD, Erséus, C and El-Matbouli, M (2004) Molecular methods clarify morphometric variation in triactinomyxon spores (Myxozoa) released from different oligochaete hosts. Systematic Parasitology 57, 1–14.Google Scholar
Hallett, SL, Atkinson, SD, Erséus, C and El-Matbouli, M (2006) Myxozoan parasites disseminated via oligochaete worms as live food for aquarium fishes: descriptions of aurantiactinomyxon and raabeia actinospore types. Diseases of Aquatic Organisms 69, 213–225.Google Scholar
Hermida, M, Saraiva, A and Cruz, C (2008) Metazoan parasite community of a European eel (Anguilla Anguilla) population from an estuary in Portugal. Bulletin of the European Association of Fish Pathologists 28, 35–40.Google Scholar
Hillis, DM and Dixon, MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. The Quarterly Review of Biology 66, 411–453.Google Scholar
Hine, PM (1975) Three new species of Myxidium (protozoa: Myxosporidia) parasitic in Anguilla australis Richardson, 1848 and A. dieffenbachii gray, 1842 in New Zealand. Journal of the Royal Society of New Zealand 5, 153–161.Google Scholar
Hine, PM (1978) Variations in the spores of Myxidium zealandicum Hine, 1975 (Protozoa: Myxosporidia). New Zealand Journal of Marine and Freshwater Research 12, 189–195.Google Scholar
Hine, PM (1980) A review of some species of Myxidium bütschli, 1882 (Myxosporea) from eels (Anguilla spp.). The Journal of Protozoology 27, 260–267.Google Scholar
Holzer, AS, Sommerville, C and 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.Google Scholar
Holzer, AS, Sommerville, C and Wootten, R (2006) Molecular identity, phylogeny and life cycle of Chloromyxum schurovi Shul'man & Ieshko 2003. Parasitology Research 99, 90–96.Google Scholar
Holzer, AS, Bartošová-Sojková, P, Born-Torrijos, A, Lövy, A, Hartigan, A and Fiala, I (2018) The joint evolution of the Myxozoa and their alternate hosts: a cnidarian recipe for success and vast biodiversity. Molecular Ecology 27, 1651–1666.Google Scholar
Ishii, S (1915) Myxosporidiosis of the Japanese eel. Zoological Magazine of Tokyo 27, 372–382.Google Scholar
Kallert, DM, Eszterbauer, E, El-Matbouli, M, Erséus, C and Haas, W (2005) The life cycle of Henneguya nuesslini Schuberg & Schroder, 1905 (Myxozoa) involves a triactinomyxon-type actinospore. Journal of Fish Diseases 28, 71–79.Google Scholar
Karlsbakk, E and Køie, M (2012) The marine myxosporean Sigmomyxa sphaerica (Thélohan, 1895) gen. n., comb. n. (syn. Myxidium sphaericum) from garfish (Belone belone (L.)) uses the polychaete Nereis pelagica L. as invertebrate host. Parasitology Research 110, 211–218.Google Scholar
Kent, ML, Whitaker, DJ and Margolis, L (1993) Transmission of Myxobolus arcticus Pugachev and Khokhlov, 1979, a myxosporean parasite of Pacific salmon, via a triactinomyxon from the aquatic oligochaete Stylodrilus heringianus (Lumbriculidae). Canadian Journal of Zoology 71, 1207–1211.Google Scholar
Køie, M, Whipps, CM and Kent, ML (2004) Ellipsomyxa gobii (Myxozoa: Ceratomyxidae) in the common goby Pomatoschistus microps (Teleostei: Gobiidae) uses Nereis spp. (Annelida: Polychaeta) as invertebrate hosts. Folia Parasitologica 51, 14–18.Google Scholar
Køie, M, Karlsbakk, E and 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, 1459–1467.Google Scholar
Køie, M, Karlsbakk, E and Nylund, A (2008) The marine herring myxozoan Ceratomyxa auerbachi (Myxozoa: Ceratomyxidae) uses Chone infundibuliformis (Annelida: Polychaeta: Sabellidae) as invertebrate host. Folia Parasitologica 55, 100–104.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Kvist, S, Sarkar, IN and Erséus, C (2010) Genetic variation and phylogeny of the cosmopolitan marine genus Tubificoides (annelida: Clitellata: Naididae: Tubificinae). Molecular Phylogenetics and Evolution 57, 687–702.Google Scholar
Lin, D, Hanson, LA and Pote, LM (1999) Small subunit ribosomal RNA sequence of Henneguya exilis (class Myxosporea) identifies the actinosporean stage from an oligochaete host. Journal of Eukaryotic Microbiology 46, 66–68.Google Scholar
Lom, J and Dyková, I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 1–36.Google Scholar
Lom, J, McGeorge, J, Feist, SW, Morris, D and Adams, A (1997) Guidelines for the uniform characterisation of the actinosporean stages of parasites of the phylum Myxozoa. Diseases of Aquatic Organisms 30, 1–9.Google Scholar
Marcucci, C, Caffara, M and Goretti, E (2009) Occurrence of actinosporean stages (Myxozoa) in the Nera River system (Umbria, central Italy). Parasitology Research 105, 1517–1530.Google Scholar
Marques, A (1984) Contribution à la connaissance des Actinomyxidies: ultrastructure, cycle biologique, systématique (PhD thesis). Université des Sciences et Techniques de Languedoc, Montepellier, France, pp. 218.Google Scholar
Marton, S and Eszterbauer, E (2011) The development of Myxobolus pavlovskii (Myxozoa: Myxobolidae) includes an echinactinomyxon-type actinospore. Folia Parasitologica 58, 157–163.Google Scholar
McGeorge, J, Sommerville, C and Wootten, R (1997) Studies of actinosporean myxozoan stages parasitic in oligochaetes from the sediments of a hatchery where Atlantic salmon harbour Sphaerospora truttae infection. Diseases of Aquatic Organisms 30, 107–119.Google Scholar
Milanin, T, Atkinson, SD, Silva, MR, Alves, RG, Maia, AA and Adriano, EA (2017) Occurrence of two novel actinospore types (Cnidaria: Myxosporea) in Brazilian fish farms, and the creation of a novel actinospore collective group, Seisactinomyxon. Acta Parasitologica 62, 121–128.Google Scholar
Molnár, K, Marton, S, Székely, C and Eszterbauer, E (2010) Differentiation of Myxobolus spp. (Myxozoa: Myxobolidae) infecting roach (Rutilus rutilus) in Hungary. Parasitology Research 107, 1137–1150.Google Scholar
Negredo, C and Mulcahy, MF (2001) Actinosporean infections in oligochaetes in a river system in southwest Ireland with descriptions of three new forms. Diseases of Aquatic Organisms 46, 67–77.Google Scholar
Negredo, C, Dillane, E and Mulcahy, MF (2003) Small subunit ribosomal DNA characterization of an unidentified aurantiactinomyxon form and its oligochaete host Tubifex ignotus. Diseases of Aquatic Organisms 54, 229–241.Google Scholar
Oumouna, M, Hallett, SL, Hoffmann, RW and El-Matbouli, M (2003) Seasonal occurrence of actinosporeans (Myxozoa) and oligochaetes (Annelida) at a trout hatchery in Bavaria, Germany. Parasitology Research 89, 170–184.Google Scholar
Özer, A, Wootten, R and Shinn, AP (2002) Survey of actinosporean types (Myxozoa) belonging to seven collective groups found in a freshwater salmon farm in Northern Scotland. Folia Parasitologica 49, 189–210.Google Scholar
Palumbi, S, Martin, A, Romano, S, McMillan, WO, Stice, L and Grabowski, G (2002) The Simple Fools Guide to PCR, Version 2.0. Honolulu: University of Hawaii. Available at http://palumbi.stanford.edu/SimpleFoolsMaster.Google Scholar
Rangel, LF, Santos, MJ, Cech, G and Székely, C (2009) Morphology, molecular data, and development of Zschokkella mugilis (Myxosporea, Bivalvulida) in a polychaete alternate host, Nereis diversicolor. Journal of Parasitology 95, 561–569.Google Scholar
Rangel, LF, Cech, G, Székely, C and Santos, MJ (2011) A new actinospore type Unicapsulactinomyxon (Myxozoa), infecting the marine polychaete, Diopatra neapolitana (Polychaeta: Onuphidae) in the Aveiro estuary, Portugal. Parasitology 138, 698–712.Google Scholar
Rangel, LF, Rocha, S, Castro, R, Severino, R, Casal, G, Azevedo, C, Cavaleiro, F and Santos, MJ (2015) The life cycle of Ortholinea auratae (Myxozoa: Ortholineidae) involves an actinospore of the triactinomyxon morphotype infecting a marine oligochaete. Parasitology Research 114, 2671–2678.Google Scholar
Rangel, LF, Castro, R, Rocha, S, Cech, G, Casal, G, Azevedo, C, Székely, C, Cavaleiro, F and Santos, MJ (2016 a) Description of new types of sphaeractinomyxon actinospores (Myxozoa: Myxosporea) from marine tubificid oligochaetes, with a discussion on the validity of the tetraspora and the endocapsa as actinospore collective group names. Parasitology Research 115, 2341–2351.Google Scholar
Rangel, LF, Castro, R, Rocha, S, Severino, R, Casal, G, Azevedo, C, Cavaleiro, F and Santos, MJ (2016 b) Tetractinomyxon stages genetically consistent with Sphaerospora dicentrarchi (Myxozoa: Sphaerosporidae) found in Capitella sp. (Polychaeta: Capitellidae) suggest potential role of marine polychaetes in parasite's life cycle. Parasitology 143, 1067–1073.Google Scholar
Rangel, LF, Rocha, S, Casal, G, Castro, R, Severino, R, Azevedo, C, Cavaleiro, F and Santos, MJ (2017) Life cycle inference and phylogeny of Ortholinea labracis n. sp. (Myxosporea: Ortholineidae), a parasite of the European seabass Dicentrarchus labrax (Teleostei: Moronidae), in a Portuguese fish farm. Journal of Fish Diseases 40, 243–262.Google Scholar
Rocha, S, Casal, G, Rangel, L, Castro, R, Severino, R, Azevedo, C and Santos, MJ (2015) Ultrastructure and phylogeny of Ceratomyxa auratae n. sp. (Myxosporea: Ceratomyxidae), a parasite infecting the gilthead seabream Sparus aurata (Teleostei: Sparidae). Parasitology International 64, 305–313.Google Scholar
Rocha, S, Alves, Â, Fernandes, P, Antunes, C, Azevedo, C and Casal, G (2019 a) Description of a new actinosporean prompts union of the raabeia and echinactinomyxon collective groups (Cnidaria, Myxozoa), due to overlap in actinospore morphology. Diseases of Aquatic Organisms (In press).Google Scholar
Rocha, S, Rangel, LF, Castro, R, Severino, R, Azevedo, C, Santos, MJ and Casal, G (2019 b) The potential role of the sphaeractinomyxon collective group (Cnidaria, Myxozoa) in the life cycle of mugiliform-infecting myxobolids, with the morphological and molecular description of three new types from the oligochaete Tubificoides insularis. Journal of Invertebrate Pathology 160, 33–42.Google Scholar
Roubal, FR, Hallett, SL and Lester, RJG (1997) First record of triactinomyxon actinosporean in marine oligochaete. Bulletin of the European Association of Fish Pathologists 17, 83–85.Google Scholar
Saraiva, A and Chubb, JC (1989) Preliminary observations on the parasites of Anguilla Anguilla (L.) from Portugal. Bulletin of the European Association of Fish Pathologists 9, 88–89.Google Scholar
Saraiva, A and Eiras, JC (1996) Parasite community of european eel Anguilla Anguilla (L.) in the river Este, northern Portugal. Research and Reviews in Parasitology 56, 179–183.Google Scholar
Styer, EL, Harrison, LR and Burtle, GJ (1991) Communications: experimental production of proliferative gill disease in channel catfish exposed to a myxozoan-infected oligochaete, Dero digitata. Journal of Aquatic Animal Health 3, 288–291.Google Scholar
Székely, C, Eiras, JC and Eszterbauer, E (2005) Description of a new synactinomyxon type from the River Sousa, Portugal. Diseases of Aquatic Organisms 66, 9–14.Google Scholar
Székely, C, Borkhanuddin, MH, Cech, G, Kelemen, O and Molnár, K (2014) Life cycles of three Myxobolus spp. from cyprinid fishes of Lake Balaton, Hungary involve triactinomyxon-type actinospores. Parasitology Research 113, 2817–2825.Google Scholar
Timm, T and Martin, PJ (2015) Clitellata: Oligochaeta. In Thorp, JH and Rogers, DC (eds), Thorp and Covich's Freshwater Invertebrates, 4th Edn. USA: Academic Press, pp. 529–549.Google Scholar
Treasurer, JW and Cox, D (1997) The occurrence of Myxidium giardi Cépède, in cultured eels, Anguilla Anguilla L., in West Scotland. Bulletin of the European Association of Fish Pathologists 17, 171–173.Google Scholar
Ventura, MT and Paperna, I (1984) Histopathology of Myxidium giardi Cépède, 1906 infection in European eels, Anguilla Anguilla L., in Portugal. Aquaculture 43, 357–368.Google Scholar
Whipps, CM, Adlard, RD, Bryant, MS, Lester, RJ, Findlay, V and 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). Journal of Eukaryotic Microbiology 50, 215–219.Google Scholar
Wolf, K and Markiw, ME (1984) Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 225, 1449–1452.Google Scholar
Xi, BW, Zhang, JY, Xie, J, Pan, LK, Xu, P and Ge, XP (2013) Three actinosporean types (Myxozoa) from the oligochaete Branchiura sowerbyi in China. Parasitology Research 112, 1575–1582.Google Scholar
Xi, BW, Zhou, ZG, Xie, J, Pan, LK, Yang, YL and Ge, XP (2015) Morphological and molecular characterization of actinosporeans infecting oligochaete Branchiura sowerbyi from Chinese carp ponds. Diseases of Aquatic Organisms 114, 217–228.Google Scholar
Xiao, CX and Desser, SS (1998) Actinosporean stages of myxozoan parasites of oligochaetes from Lake Sasajewun, Algonquin Park, Ontario: new forms of echinactinomyxon, neoactinomyxum, aurantiactinomyxon, guyenotia, synactinomyxon and antonactinomyxon. Journal of Parasitology 84, 1010–1019.Google Scholar
Yokoyama, H, Ogawa, K and Wakabayashi, H (1993) Involvement of Branchiura sowerbyi (Oligochaeta, Annelida) in the transmission of Hoferellus carassii (Myxosporea, Myxozoa), the causative agent of kidney enlargement disease (KED) of goldfish Carassius auratus. Fish Pathology 28, 135–139.Google Scholar
Zhao, D, Borkhanuddin, MH, Wang, W, Liu, Y, Cech, G, Zhai, Y and Székely, C (2016) The life cycle of Thelohanellus kitauei (Myxozoa: Myxosporea) infecting common carp (Cyprinus carpio) involves aurantiactinomyxon in Branchiura sowerbyi. Parasitology Research 115, 4317–4325.Google Scholar
Zhao, DD, Zhai, YH, Liu, Y, Wang, SJ and Gu, ZM (2017) Involvement of aurantiactinomyxon in the life cycle of Thelohanellus testudineus (Cnidaria: Myxosporea) from allogynogenetic gibel carp Carassius auratus gibelio, with morphological, ultrastructural, and molecular analysis. Parasitology Research 116, 2449–2456.Google Scholar