Skip to main content
SpringerLink
Log in

Myxozoan Life Cycles: Practical Approaches and Insights

  • Chapter
  • First Online:
Myxozoan Evolution, Ecology and Development

Abstract

This chapter summarises the collective knowledge of myxozoan life cycles gained through experimental studies and observations. We review myxozoan life cycles, factors that influence parasite development and the conditions required for laboratory maintenance of invertebrate hosts. Unusual modes of transmission, including fish-to-fish and vertical transmission in invertebrate hosts are highlighted. We close by summarizing attempts to propagate myxozoans in vitro.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abd-Elfattah A, Fontes I, Kumar GL et al (2014) Vertical transmission of Tetracapsuloides bryosalmonae (Myxozoa), the causative agent of salmonid proliferative kidney disease. Parasitology 141:482–490

    PubMed  Google Scholar 

  • Alama-Bermejo G, Šima 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

    PubMed  Google Scholar 

  • Alvarez-Pellitero P, Palenzuela O, Sitjà-Bobadilla A (2008) Histopathology and cellular response in Enteromyxum leei (Myxozoa) infections of Diplodus puntazzo (Teleostei). Parasitol Int 57:110–120

    Google Scholar 

  • Anderson CL, Canning EU, Schäfer SM et al (2000) Molecular confirmation of the life cycle of Thelohanellus hovorkai Achmerov, 1960 (Myxozoa: Myxosporea). Bull Eur Assoc Fish Pathol 20:111–115

    Google Scholar 

  • Antonio DB, El-Matbouli M, Hedrick RP (1999) Detection of early developmental stages of Myxobolus cerebralis in fish and tubificid oligochaete hosts by in situ hybridization. Parasitol Res 85:942–944

    CAS  PubMed  Google Scholar 

  • Aston RJ (1984) The culture of Branchiura sowerbyi (Oligochaeta, Tubificidae) using cellulose substrate. Aquaculture 40:89–94

    Google Scholar 

  • Aston RJ, Sadler K, Milner AGP (1982) The effects of temperature on the culture of Branchiura sowerbyi (Oligochaeta, Tubificidae) on activated sludge. Aquaculture 29:137–145

    Google Scholar 

  • Atkinson SD (2011) Diversity, life cycles and population genetics of freshwater Myxozoa from the Pacific Northwest of North America. Ph.D. thesis, The University of Queensland

    Google Scholar 

  • Atkinson SD, Bartholomew JL (2009) Alternate spore stages of Myxobilatus gasterostei, a myxosporean parasite of three-spined sticklebacks (Gasterosteus aculeatus) and oligochaetes (Nais communis). Parasitol Res 104:1173–1181

    PubMed  Google Scholar 

  • Atkinson SD, Bartholomew JL (2010) Disparate infection patterns of Ceratomyxa shasta (Myxozoa) in rainbow trout (Oncorhynchus mykiss) and Chinook salmon (Oncorhynchus tshawytscha) correlate with internal transcribed spacer-1 sequence variation in the parasite. Int J Parasitol 40:599–604

    CAS  PubMed  Google Scholar 

  • Atkinson SD, Hallett SL, Bartholomew JL (2007) The life cycle of Chloromyxum auratum (Myxozoa) from goldfish, Carassius auratus (L.), involves an antonactinomyxon actinospore. J Fish Dis 30:149–156

    CAS  PubMed  Google Scholar 

  • Baerwald MR, Welsh AB, Hedrick RP, May B (2008) Discovery of genes implicated in whirling disease infection and resistance in rainbow trout using genome-wide expression profiling. BMC Genom 9:37

    Google Scholar 

  • Bartholomew JL, Whipple MJ, Stevens DG, Fryer JL (1997) The life cycle of Ceratomyxa shasta, a myxosporean parasite of salmonids, requires a freshwater polychaete as an alternate host. J Parasitol 83:859–868

    CAS  PubMed  Google Scholar 

  • Bartholomew JL, Atkinson SD, Hallett SL (2006) Involvement of Manayunkia speciosa (Annelida: Polychaeta: Sabellidae) in the life cycle of Parvicapsula minibicornis, a myxozoan parasite of Pacific salmon. J Parasitol 92:742–748

    PubMed  Google Scholar 

  • Baxa DV, Kelley GO, Mukkatira KS et al (2008) Arrested development of the myxozoan parasite, Myxobolus cerebralis, in certain populations of mitochondrial 16S lineage III Tubifex tubifex. Parasitol Res 102:219–228

    CAS  PubMed  Google Scholar 

  • Beauchamp KA, Kathman RD, McDowell TS, Hedrick RP (2001) Molecular phylogeny of tubificid oligochaetes with special emphasis on Tubifex tubifex (Tubificidae). Mol Phylogenet Evol 19:216–224

    CAS  PubMed  Google Scholar 

  • Beauchamp KA, El-Matbouli M, Gay M et al (2006) The effect of cohabitation of Tubifex tubifex (Oligochaeta: Tubificidae) populations on infections to Myxobolus cerebralis (Myxozoa: Myxobolidae). J Invertebr Pathol 91:1–8

    PubMed  Google Scholar 

  • Bechara IJ, Youssef NN, Roberts DW (2002) Study of the tail fin rays of rainbow trout (Oncorhynchus mykiss) infected with the parasite Myxobolus cerebralis. J Submicrosc Cytol Pathol 34:299–304

    CAS  PubMed  Google Scholar 

  • Bely AE, Wray GA (2004) Molecular phylogeny of naidid worms (Annelida: Clitellata) based on cytochrome oxidase I. Mol Phylogenet Evol 30:50–63

    CAS  PubMed  Google Scholar 

  • Benajiba MH, Marques A (1993) The alternation of actinomyxidian and myxosporidian sporal forms in the development of Myxidium giardi (parasite of Anguilla anguilla) through oligochaetes. Bull Eur Assoc Fish Pathol 13:100–103

    Google Scholar 

  • Bettge K, Segner H, Burki R et al (2009a) Proliferative kidney disease (PKD) of rainbow trout: temperature- and time-related changes of Tetracapsuloides bryosalmonae DNA in the kidney. Parasitology 136:615–625

    CAS  PubMed  Google Scholar 

  • Bettge K, Wahli T, Segner H, Schmidt-Posthaus H (2009b) Proliferative kidney disease in rainbow trout: time-and temperature-related renal pathology and parasite distribution. Dis Aquat Org 83:67–76

    PubMed  Google Scholar 

  • Bjork SJ, Bartholomew JL (2009a) The effects of water velocity on the Ceratomyxa shasta infectious cycle. J Fish Dis 32:131–142

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bjork SJ, Bartholomew JL (2009b) Effects of Ceratomyxa shasta dose on a susceptible strain of rainbow trout and comparatively resistant Chinook and coho salmon. Dis Aquat Org 86:29–37

    PubMed  Google Scholar 

  • Bjork SJ, Bartholomew JL (2010) Invasion of Ceratomyxa shasta (Myxozoa) and comparison of migration to the intestine between susceptible and resistant fish hosts. Int J Parasitol 40:1087–1095

    PubMed  Google Scholar 

  • Blazer VS, Waldrop TB, Schill WB et al (2003) Effects of water temperature and substrate type on spore production and release in eastern Tubifex tubifex worms infected with Myxobolus cerebralis. J Parasitol 89:21–26

    PubMed  Google Scholar 

  • Borkhanuddin MH, Cech G, Molnár K, Székely C (2013) In: 16th EAFP international conference on diseases of fish and shellfish, Tampere, Finland. O-038, 2–6 September 2013

    Google Scholar 

  • Caffara M, Raimondi E, Florio D, Marcer F, Quaglio F, Fioravanti ML (2009) The life cycle of Myxobolus lentisuturalis (Myxozoa: Myxobolidae), from goldfish (Carassius auratus auratus), involves a Raabeia-type actinospore. Folia Parasitol 56:6–12

    CAS  PubMed  Google Scholar 

  • Carroll JH Jr, Dorris TC (1972) The Life History of Branchiura sowerbyi. Am Midl Nat 87:413–422

    Google Scholar 

  • Cheng LL, Bowser PR, Spitsbergen JM (1993) Development of cell cultures derived from lake trout liver and kidney in a hormone-supplemented, serum-reduced medium. J Aquatic Animal Health 5:119–126

    Google Scholar 

  • China M, Nakamura H, Hamakawa K et al (2013) Occurrence of the myxosporean emaciation disease caused by Enteromyxum leei in cultured Malabar grouper Epinephelus malabaricus. Fish Pathol 48:88–96

    Google Scholar 

  • Clifton-Hadley RS, Richards RH, Bucke D (1986) Proliferative kidney disease (PKD) in rainbow trout Salmo gairdneri: further observations on the effects of water temperature. Aquaculture 55:165–171

    Google Scholar 

  • Csaba G (1976) An unidentifiable extracellular sporozoan parasite from the blood of the carp. Parasitol Hung 9:21–24

    Google Scholar 

  • Diamant A (1997) Fish to fish transmission of a marine myxosporean. Dis Aquat Org 30:99–105

    Google Scholar 

  • Diamant A (1998) Red drum Sciaenops ocellatus (Sciaenidae), a recent introduction to Mediterranean mariculture, is susceptible to Myxidium leei (Myxosporea). Aquacultre 162:33–39

    Google Scholar 

  • Diamant A, Wajsbrot N (1997) Experimental transmission of Myxidium leei in gilthead sea bream Sparus aurata. Bull Eur Assoc Fish Pathol 17:99–103

    Google Scholar 

  • Diamant A, Palenzuela O, Álvarez-Pellitero P et al. (2006a) Epizootiology of Enteromyxum leei (Myxozoa: Myxosporea) in Mediterranean mariculture systems. In: 5th international symposium on aquatic animal health, (Myxozoa: Myxosporea) in Mediterranean mariculture systems, San Francisco, p. 94

    Google Scholar 

  • Diamant A, Ram S, Paperna I (2006b) Experimental transmission of Enteromyxum leei to freshwater fish. Dis Aquat Org 72:171–178

    CAS  PubMed  Google Scholar 

  • El-Matbouli M, Hoffmann RW (1993) Myxobolus carassii Klokaceva, 1914 also requires an aquatic oligochaete, Tubifex tubifex as intermediate host in its life cycle. Bull Eur Assoc Fish Pathol 13:189–192

    Google Scholar 

  • El-Mansy A, Molnár K (1997a) Extrapiscine development of Myxobolus drjagini Akhmerov, 1954 (Myxosporea, Myxobolidae) in oligochaete alternative hosts. Acta Vet Hung 45:427–438

    CAS  PubMed  Google Scholar 

  • El-Mansy A, Molnár K (1997b) Development of Myxobolus hungaricus (Myxosporea: Myxobolidae) in oligochaete alternate hosts. Dis Aquat Org 31:227–232

    Google Scholar 

  • El-Mansy A, Molnár K, Székely Cs (1998) Development of Myxobolus portucalensis Saraiva (Molnár, 1990 (Myxosporea: Myxobolidae) in the oligochaete Tubifex tubifex (Müller). Syst Parasitol 41:95–103

    Google Scholar 

  • El-Matbouli M, Hoffmann RW (1989) Experimental transmission of two Myxobolus spp. developing bisporogeny via tubificid worms. Parasitol Res 75:461–464

    CAS  PubMed  Google Scholar 

  • El-Matbouli M, Hoffmann RW (1998) Light and electron microscopic studies on the chronological development of Myxobolus cerebralis to the actinosporean stage in Tubifex tubifex. Int J Parasitol 28:195–217

    CAS  PubMed  Google Scholar 

  • El-Matbouli M, Hoffmann RW (2002) Influence of water quality on the outbreak of proliferative kidney disease—field studies and exposure experiments. J Fish Dis 25:459–467

    Google Scholar 

  • El-Matbouli M, Fischer-Scherl T, Hoffmann RW (1992a) Present knowledge of the life cycle, taxonomy, pathology, and therapy of some Myxosporea spp. important for freshwater fish. Ann Rev Fish Dis 3:367–402

    Google Scholar 

  • El-Matbouli M, Fischer-Scherl T, Hoffmann RW (1992b) Transmission of Hoferellus carassii Achmerov, 1960 to goldfish Carassius auratus via an aquatic oligochaete. Bull Eur Assoc Fish Pathol 12:54–56

    Google Scholar 

  • El-Matbouli M, Hoffmann RW, Shoel H et al (1999a) Whirling disease: host specificity and interaction between the actinosporean stage of Myxobolus cerebralis and rainbow trout (Oncorhynchus mykiss) cartilage. Dis Aquat Org 35:1–12

    CAS  PubMed  Google Scholar 

  • El-Matbouli M, McDowell TS, Antonio DB et al (1999b) 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

    CAS  PubMed  Google Scholar 

  • Estensoro I, Bermúdez R, Losada AP et al (2009) Effect of Enteromyxum leei (Myxozoa) on gastrointestinal neuromodulators and cell apoptosis of gilthead sea bream (Sparus aurata). In: 14th European association of fish pathologists international conference, Prague, Czech Republic

    Google Scholar 

  • Estensoro I, Redondo MJ, Álvarez-Pellitero P, Sitjà-Bobadilla A (2010) Novel horizontal transmission route for Enteromyxum leei (Myxozoa) by anal intubation of gilthead sea bream Sparus aurata. Dis Aquat Org 92:51–58

    PubMed  Google Scholar 

  • Estensoro I, Benedito-Palos L, Palenzuela O et al (2011) The nutritional background of the host alters the disease course in a fish–myxosporean system. Vet Parasitol 175:141–150

    PubMed  Google Scholar 

  • Estensoro I, Álvarez-Pellitero P, Sitjà-Bobadilla A (2013) Antigenic characterization of Enteromyxum leei (Myxozoa: Myxosporea). Dis Aquat Org 106:149–162

    CAS  PubMed  Google Scholar 

  • Eszterbauer E (2002) Developmental and molecular biological studies on fish-parasitic myxozoans. Ph.D. dissertation, Eötvös Loránd University

    Google Scholar 

  • Eszterbauer E, Székely C, Molnár K, Baska F (2000) Development of Myxobolus bramae (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. J Fish Dis 23:19–25

    Google Scholar 

  • Eszterbauer E, Marton Sz, Rácz OZ, Letenyei M, Molnár K (2006) Morphological and genetic differences among actinosporean stages of fish-parasitic myxosporeans (Myxozoa): difficulties of species identification. Syst Parasitol 65:97–114

    Google Scholar 

  • Eszterbauer E, Kallert DM, Grabner D, El-Matbouli M (2009) Differentially expressed parasite genes involved in host recognition and invasion of the triactinomyxon stage of Myxobolus cerebralis (Myxozoa). Parasitology 136:367–377

    CAS  PubMed  Google Scholar 

  • Feist SW, Longshaw M, Canning EU, Okamura B (2001) Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae. Dis Aquat Org 45:61–68

    CAS  PubMed  Google Scholar 

  • Fetherman ER, Winkelman DL, Schisler GJ, Myrick CA (2011) The effects of Myxobolus cerebralis on the physiological performance of whirling disease resistant and susceptible strains of rainbow trout. J Aquat Anim Health 23:169–177

    PubMed  Google Scholar 

  • Fleurance R, Sauvegrain C, Marques A et al (2008) Histopathological changes caused by Enteromyxum leei infection in farmed sea bream Sparus aurata. Dis Aquat Org 79:219–228

    CAS  PubMed  Google Scholar 

  • Golomazou E, Athanassopoulou F, Karagouni E, Tsagozis P, Tsantilas H, Vagianou S (2006) Experimental transmission of Enteromyxum leei Diamant, Lom and Dyková, 1994 in sharpsnout sea bream, Diplodus puntazzo C. and the effect on some innate immune parameters. Aquaculture 260:44–53

    Google Scholar 

  • Grabner DS, El-Matbouli M (2008) Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) to Fredericella sultana (Bryozoa: Phylactolaemata) by various fish species. Dis Aquat Org 79:133–139

    Google Scholar 

  • Grabner DS, El-Matbouli M (2010) Experimental transmission of malacosporean parasites from bryozoans to common carp (Cyprinus carpio) and minnow (Phoxinus phoxinus). Parasitology 137:629-639

    Google Scholar 

  • Grossheider G, Körting W (1992) First evidence that Hoferellus cyprini (Doflein, 1898) is transmitted by Nais sp. Bull Eur Assoc Fish Pathol 12:17–20

    Google Scholar 

  • Hahn CW (1917) On the sporozoon parasites of the fishes of Woods Hole and vicinity. J Parasitol 3:91–104

    Google Scholar 

  • Hallett SL, Bartholomew JL (2006) Application of a real-time PCR assay to detect and quantify the myxozoan parasite Ceratomyxa shasta in river water samples. Dis Aquat Org 71:109–118

    CAS  PubMed  Google Scholar 

  • Hallett SL, Bartholomew JL (2008) Effects of water flow on the infection dynamics of Myxobolus cerebralis. Parasitology 135:371–384

    CAS  PubMed  Google Scholar 

  • Hallett SL, Atkinson SD, Erséus C, El-Matbouli M (2005) Dissemination of triactinomyxons (Myxozoa) via oligochaetes used as live food for aquarium fishes. Dis Aquat Org 65:137–152

    PubMed  Google Scholar 

  • Halliday MM (1976) The biology of Myxosoma cerebralis: the causative organism of whirling disease of salmonids. J Fish Biol 9:339–357

    Google Scholar 

  • Hartikainen H, Okamura B (2012) Castrating parasites and colonial hosts. Parasitology 139:547–556

    CAS  PubMed  Google Scholar 

  • Hartikainen H-L, Fontes I, Okamura B (2013) Parasitism and phenotypic change in colonial hosts. Parasitology 140:1403–1412

    PubMed  Google Scholar 

  • Hedrick RP, Baxa DV, De Kinkelin P, Okamura B (2004) Malacosporean-like spores in urine of rainbow trout react with antibody and DNA probes to Tetracapsuloides bryosalmonae. Parasitol Res 92:81–88

    CAS  PubMed  Google Scholar 

  • Hedrick RP, MacConnell E, De Kinkelin P (1993) Proliferative kidney disease of salmonid fish. Ann Rev Fish Dis 3:277–290

    Google Scholar 

  • Hedrick RP, El-Matbouli M, Adkison MA, MacConnell E (1998) Whirling disease: re-emergence among wild trout. Immunol Rev 166:365–376

    CAS  PubMed  Google Scholar 

  • Hedrick RP, McDowell TS, Marty GD et al (2003) Susceptibility of two strains of rainbow trout (one with suspected resistance to whirling disease) to Myxobolus cerebralis infection. Dis Aquat Org 55:37–44

    PubMed  Google Scholar 

  • Hill SLL, Okamura B (2007) Endoparasitism in colonial hosts: patterns and processes. Parasitology 134:841–852

    CAS  PubMed  Google Scholar 

  • Hoffman GL (1990) Myxobolus cerebralis, a worldwide cause of salmonid whirling disease. J Aquat Anim Health 2:30–37

    Google Scholar 

  • Hoffman GL, Putz RE (1969) Host susceptibility and the effect of aging, freezing, heat and chemicals on spores of Myxosoma cerebralis. Prog Fish-Cult 31:35–37

    Google Scholar 

  • Holzer AS, Sommerville C, Wootten R (2004) Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. Int J Parasitol 34:1099–1111

    CAS  PubMed  Google Scholar 

  • Holzer AS, Sommerville C, Wootten R (2006) Molecular identity, phylogeny and life cycle of Chloromyxum schurovi Shulman and Ieshko 2003. Parasitol Res 99:90–96

    PubMed  Google Scholar 

  • Hurst CN, Bartholomew JL (2012) Ceratomyxa shasta genotypes cause differential mortality in their salmonid hosts. J Fish Dis 35:725–732

    CAS  PubMed  Google Scholar 

  • Johnson KA (1980) Host susceptibility, histopathologic and transmission studies on Ceratomyxa shasta, a myxosporidan parasite of salmonid fish. Fish Pathol 14:183–184

    Google Scholar 

  • Kallert DM, Eszterbauer E, El-Matbouli M et al (2005a) The life cycle of Henneguya nuesslini Schuberg & Schröder 1905 (Myxozoa) involves a triactinomyxon-type actinospore. J Fish Dis 28:71–79

    CAS  PubMed  Google Scholar 

  • Kallert DM, Eszterbauer E, Erséus C et al (2005b) Life cycle studies of Myxobolus parviformis sp. n. (Myxozoa, Myxobolidae) from bream. Dis Aquat Org 66:233–243

    CAS  PubMed  Google Scholar 

  • Kallert DM, Eszterbauer E, Grabner D, El-Matbouli M (2009) In vivo exposure of susceptible and non-susceptible fish species to Myxobolus cerebralis actinospores reveals non-specific invasion behaviour. Dis Aquat Org 84:123–130

    CAS  PubMed  Google Scholar 

  • Kallert DM, Ponader S, Eszterbauer E, El-Matbouli M, Haas W (2007) Myxozoan transmission via actinospores: new insights in mechanisms and adaptations for host invasion. Parasitology 134:1741–1750

    CAS  PubMed  Google Scholar 

  • Karlsbakk E, 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. Parasitol Res 110:211–218

    PubMed Central  PubMed  Google Scholar 

  • Kelemen O, Ostoros G, Cech G, Székely C (2009) Study of the development of fish-parasitic myxosporeans in oligochaete alternative hosts in Lake Balaton. In: 14th EAFP international conference on diseases of fish and shellfish, Prague, Czech Republic. P-082, 14–19 Sept 2009

    Google Scholar 

  • Kelley GO, Zagmutt-Vergara FJ, Leutenegger CM, Myklebust KA, Adkison MA, McDowell TS, Marty GD, Kahler AL, Bush AL, Gardner IA, Hedrick RP (2004) Evaluation of five diagnostic methods for the detection and quantification of Myxobolus cerebralis. J Vet Diagn Invest 16:202–211

    PubMed  Google Scholar 

  • Kent ML, Hedrick RP (1985) PKX, the causative agent of proliferative kidney disease (PKD) in Pacific salmonid fishes and its affinities with the Myxozoa. J Protozool 32:254–260

    CAS  PubMed  Google Scholar 

  • Kent ML, Whitaker DJ, 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). Can J Zool 71:1207–1211

    Google Scholar 

  • Kerans BL, Stevens RI, Lemmon JC (2005) Water temperature affects a hostparasite interaction: Tubifex tubifex and Myxobolus cerebralis. J Aquat Anim Health 7:216–221

    Google Scholar 

  • Køie 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. J Parasitol 93:1459–1467

    PubMed  Google Scholar 

  • Køie M, Karlsbakk E, Nylund A (2008) The marine herring myxozoan Ceratomyxa auerbachi (Myxozoa: Ceratomyxidae) uses Chone infundibuliformis (Annelida: Polychaeta: Sabellidae) as invertebrate host. Folia Parasitol 55:100–104

    PubMed  Google Scholar 

  • Körting W, Kruse P, Steinhagen D (1989) Development of “Csaba cells” in experimentally infected Cyprinus carpio. Angew Parasitol 30:185–188

    PubMed  Google Scholar 

  • Køie M, Whipps CM, Kent ML (2004) Ellipsomyxa gobii (Myxozoa: Ceratomyxidae) in the common goby Pomatoschistus microps (Teleostei: Gobiidae) uses Nereis spp. (Annelida: Polychaeta) as invertebrate hosts. Folia Parasitol 51:14–18

    PubMed  Google Scholar 

  • Kumar G, Abd-Elfattah A, Saleh M, El-Matbouli M (2013a) Fate of Tetracapsuloides bryosalmonae (Myxozoa) after infection of brown trout (Salmo trutta) and rainbow trout (Oncorhynchus mykiss). Dis Aquat Org 107:9–18

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kumar G, Abd-Elfattah A, Soliman H, El-Matbouli M (2013b) Establishment of medium for laboratory cultivation and maintenance of Fredericella sultana for in vivo experiments with Tetracapsuloides bryosalmonae (Myxozoa). J Fish Dis 36:81–88

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lin D, Hanson LA, Pote LM (1999) Small subunit ribosomal RNA sequence of Henneguya exilis (class Myxosporea) identifies the actinosporean stage from an oligochaete host. J Eukaryot Microbiol 46:66–68

    CAS  PubMed  Google Scholar 

  • Liyanage YS, Yokoyama H, Wakabayashi H (2003) Dynamics of experimental production of Thelohanellus hovorkai (Myxozoa: Myxozoa) in fish and oligochaete alternate hosts. J Fish Dis 26:575–582

    CAS  PubMed  Google Scholar 

  • Lom J, Dyková I (2006) Myxozoan genera: definiton and notes on taxonomy, life cycles, terminology and pathogenic species. Folia Parasitol 53:1–36

    PubMed  Google Scholar 

  • Longshaw M, Le Deuff R-M, Harris AF, Feist SW (2002) Development of proliferative kidney disease in rainbow trout Oncorhynchus mykiss (Walbaum), following short-term exposure to Tetracapsula bryosalmonae infected bryozoans. J Fish Dis 25:443–449

    Google Scholar 

  • MacConnell E, Vincent ER (2002) Review: the effects of Myxobolus cerebralis on the salmonid host. In: Bartholomew JL, Wilson JC (eds) Whirling disease: reviews and current topics. American Fisheries Society, Symposium 29, Bethesda, Maryland, pp 95–107

    Google Scholar 

  • Markiw ME (1991) Whirling disease: earliest susceptible age of rainbow trout to the triactinomyxid of Myxobolus cerebralis. Aquaculture 92:1–6

    Google Scholar 

  • Markiw ME (1992) Experimentally induced whirling disease. I. Dose response of fry and adults of rainbow trout exposed to the triactinomyxon stage of Myxobolus cerebralis. J Aquat Anim Health 4:40–43

    Google Scholar 

  • Marton Sz, Eszterbauer E (2011) The development of Myxobolus pavlovskii (Myxozoa: Myxobolidae) includes an echinactinomyxon-type actinospore. Folia Parasitol 58:157–163

    Google Scholar 

  • Marton Sz, Eszterbauer E (2012) The susceptibility of diverse species of cultured oligochaetes for the fish parasite Myxobolus pseudodispar Gorbunova (Myxozoa). J Fish Dis 35:303–314

    Google Scholar 

  • McGurk C (2005) Culture of malacosporeans (Myxozoa) and development of control strategies for proliferative kidney disease, Ph.D. dissertation. University of Stirling, Stirling, pp 295

    Google Scholar 

  • McGurk C, Morris DJ, Auchinachie NA, Adams A (2006) Development of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) in bryozoan hosts (as examined by light microscopy) and quantitation of infective dose to rainbow trout (Oncorhynchus mykiss). Vet Parasitol 135:249–257

    PubMed  Google Scholar 

  • Meaders MD, Hendrickson GL (2009) Chronological development of Ceratomyxa shasta in the polychaete host Manayunkia speciosa. J Parasitol 95:1397–1407

    PubMed  Google Scholar 

  • Mischke CC, Griffin MJ (2011) Laboratory mass culture of the freshwater oligochaete dero digitata. N Am J Aquacult 73:13–16

    Google Scholar 

  • Molnár K (1979) Myxobolus pavlovskii (Achmerov, 1954) (Myxosporidia) infection in the silver carp and bighead. Acta Vet Acad Sci H 27:207–216

    Google Scholar 

  • Molnár K (1984) Experimental evidence that protozoans causing swimbladder inflammation in common carp Cyprinus carpio L. are stages of Sphaerospora renicola. Bull Eur Ass Fish Pathol 4:14–15

    Google Scholar 

  • Molnár K, Kovács-Gayer É (1986) Experimental induction of Sphaerospora renicola (Myxosporea) infection in common carp (Cyprinus carpio) by transmission of SB-protozoans. J Appl Ichthyol 2:86–94

    Google Scholar 

  • Molnár K, Székely C (1999) Myxobolus infection of the gills of common bream (Abramis brama) in Lake Balaton and in the Kis-Balaton Reservoir, Hungary. Acta Vet Hung 47:419–432

    PubMed  Google Scholar 

  • Molnár K, El-Mansy A, Székely C, Baska F (1999) Development of Myxobolus dispar (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. Folia Parasit 46:15–21

    Google Scholar 

  • Molnár K, Eszterbauer E, Székely C et al (2002) Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. J Fish Dis 25:643–652

    Google Scholar 

  • Molnár K, Marton Sz, Székely Cs, Eszterbauer E (2010) Differentiation of Myxobolus spp. (Myxozoa: Myxobolidae) infecting roach (Rutilus rutilus) in Hungary. Parasitol Res 107:1137–1150

    Google Scholar 

  • Moran JDW, Whitaker DJ, Kent ML (1999) Natural and laboratory transmission of the marine myxozoan parasite Kudoa thyrsites to Atlantic salmon. J Aquat Anim Health 11:110–115

    Google Scholar 

  • Morris DJ (2012) Towards an in vitro culture method for the rainbow trout pathogen Tetracapsuloides bryosalmonae. J Fish Dis 35:941–944

    CAS  PubMed  Google Scholar 

  • Morris DJ, Adams A (2006a) Transmission of freshwater myxozoans during the asexual propagation of invertebrate hosts. Int J Parasitol 36:371–377

    CAS  PubMed  Google Scholar 

  • Morris DJ, Adams A (2006b) Proliferative, presaccular stages of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) within the invertebrate host Fredericella sultana (Bryozoa: Phylactolaemata). J Parasitol 92:984–989

    PubMed  Google Scholar 

  • Morris DJ, Adams A (2006c) Transmission of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea), the causative organism of salmonid proliferative kidney disease, to the freshwater bryozoan Fredericella sultana. Parasitology 133:701–709

    CAS  PubMed  Google Scholar 

  • Morris DJ, Freeman MA (2010) Hyperparasitism has wide-ranging implications for studies on the invertebrate phase of myxosporean (Myxozoa) life cycles. Int J Parasitol 40:357–369

    CAS  PubMed  Google Scholar 

  • Morris DJ, Morris DC, Adams A (2002) Development and release of a malacosporean (Myxozoa) from Plumatella repens (Bryozoa: Phylactolaemata). Folia Parasit 49:25–34

    Google Scholar 

  • Muñoz P, Cuesta A, Athanassopoulou F, Golomazou E et al. (2007) Sharpsnout sea bream (Diplodus puntazzo) humoral immune response against the parasite Enteromyxum leei (Myxozoa). Fish Shellfish Immunol 23:636–645

    Google Scholar 

  • Palenzuela O, Sitjà-Bobadilla A, Alvarez-Pellitero P (1994) In vitro sporulation of Ceratomyxa sp. (Myxosporea: Bivavulida) from Sparus aurata L. (Teleostei: Sparidae). ICOPA VIII. Abstracts book (vol 1), p 195. Turkish Society for Parasitology Izmir

    Google Scholar 

  • Pote L, Bellerud MB, Lin TL, Chenney EF (1994) The isolation and propagation of Dero digitata infected with Aurantiactinomyxon sp. J World Aquacult Soc 25:303–307

    Google Scholar 

  • Rácz OZ (2004) Experimental study of intrapiscin and intraoligochaete developmental stages of fish-parasitic myxozoans. Ph.D. dissertation, Szent István University

    Google Scholar 

  • Rácz OZ, Székely Cs, Molnár K (2004) Intraoligochaete development of Myxobolus intimus (Myxosporea: Myxobolidae), a gill myxosporean of the roach (Rutilus rutilus). Folia Parasitol 51:199–207

    Google Scholar 

  • Rácz O, Székely C, Molnár K (2006) The role of copepods (Cyclops spp.) in eliminating the actinospore stages of fish-parasitic myxozoans. Acta Vet Hung 54:61–70

    PubMed  Google Scholar 

  • Rangel LF, Santos MJ, Cech G, Székely C (2009) Morphology, molecular data, and development of Zschokkella mugilis (Myxosporea, Bivalvulida) in a polychaete alternate host, Nereis diversicolor. J Parasitol 95:561–569

    CAS  PubMed  Google Scholar 

  • Ray AR, Holt RA, Bartholomew JL (2012) Relationship between temperature and Ceratomyxa shasta-induced mortality in Klamath River salmonids. J Parasitol 98:520–526

    PubMed  Google Scholar 

  • Redondo MJ, Palenzuela O, Riaza et al (2002) Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. J Parasitol 88:482–488

    Google Scholar 

  • Redondo MJ, Palenzuela O, Alvarez-Pellitero P (2003) In vitro studies on viability and proliferation of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of cultured turbot Scophthalmus maximus. Dis Aquat Org 55:133–144

    PubMed  Google Scholar 

  • Redondo MJ, Palenzuela O, Alvarez-Pellitero P (2004) Studies on transmission and life cycle of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. Fol Parasitol 51:188–198

    Google Scholar 

  • Redondo MJ, Cortadellas N, Palenzuela O, Alvarez-Pellitero P (2008) Enteromyxum scophthalmi (Myxozoa) and possible interactions with its fish host Psetta maxima. Parasitol Res 102:1257–1267

    CAS  PubMed  Google Scholar 

  • Rigos G, Christophilogiannis P, Yiagnisi M et al (1999) Myxosporean infections in Greek mariculture. Aquacult Int 7:361–364

    Google Scholar 

  • Ryce EKN, Zale AV, MacConnell E (2004) Effects of fish age and parasite dose on the development of whirling disease in rainbow trout. Dis Aquat Org 59:225–233

    PubMed  Google Scholar 

  • Severin VI, Soliman H, El-Matbouli M (2010) Expression of immune-regulatory genes, arginase-2 and inducible nitric oxide synthase (iNOS), in two rainbow trout (Oncorhynchus mykiss) strains following exposure to Myxobolus cerebralis. Parasitol Res 106:325–334

    Google Scholar 

  • Shirakashi S, El-Matbouli M (2009) Effect of cadmium on the susceptibility of Tubifex tubifex to Myxobolus cerebralis (Myxozoa), the causative agent of whirling disease. Dis Aquat Org 89:63–70

    Google Scholar 

  • Siau Y, Grassé PP (1977) Premiers stades du dévelopement experimental en cultures, de spores de la Myxosporidié Myxobolus exiguous Thélohan, 1895. Comptes Rendus des Seances de l’Academie des Sciencés Paris serie D 285:681–683

    Google Scholar 

  • Sitjà-Bobadilla A, Palenzuela O (2012) Enteromyxum species. In: Woo PTK, Buchmann K (eds) Fish parasites: pathobiology and protection, Chapter 9, CABI Publishing, Wallingford, pp 163–176

    Google Scholar 

  • Sitjà-Bobadilla A, Diamant A, Palenzuela O, Alvarez-Pellitero P (2007) Effect of host factors and experimental conditions on the transmission of Enteromyxum leei (Myxozoa) to gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.). J Fish Dis 30:243–250

    PubMed  Google Scholar 

  • Steinbach Elwell LC, Stromberg KE, Ryce EKN, Bartholomew JL (2009) Whirling Disease in the United States. A summary of progress in research and management, Trout Unlimited and the Whirling Disease Foundation, Bozeman, p. 61

    Google Scholar 

  • Stevens R, Kerans BL, Lemmon JC, Rasmussen C (2001) The effects of Myxobolus cerebralis myxospore dose on triactinomyxon production and biology of Tubifex tubifex from two geographic regions. J Parasitol 87:315–321

    CAS  PubMed  Google Scholar 

  • Sturmbauer C, Opadiya GB, Neiderstätter H, Reidman A (1999) Mitochondrial DNA reveals cryptic oligochaete species differing in cadmium resistance. Mol Biol Evol 16:967–974

    CAS  PubMed  Google Scholar 

  • Styer EL, Harrison LR, Burtle GJ (1991) Experimental production of proliferative gill disease in channel catfish exposed to myxozoan-infected oligochaete Dero digitata. J Aquat Anim Health 4:288–291

    Google Scholar 

  • Székely C, El-Mansy A, Molnár K, Baska F (1998) Development of Thelohanellus hovorkai and Thelohanellus nikolskii (Myxosporea: Myxozoa) in oligochaete alternate hosts. Fish Pathol 33:107–114

    Google Scholar 

  • Székely C, Molnár K, Eszterbauer E, Baska F (1999) Experimental detection of the actinospores of Myxobolus pseudodispar (Myxosporea: Myxobolidae) in oligochaete alternate hosts. Dis Aquat Org 38:219–224

    PubMed  Google Scholar 

  • Székely C, Molnár K, Rácz O (2001) Complete developmental cycle of Myxobolus pseudodispar (Gorbunova) (Myxosporea: Myxobolidae). J Fish Dis 24:461–468

    Google Scholar 

  • Székely C, Rácz O, Molnár K, Eszterbauer E (2002) Development of Myxobolus macrocapsularis (Myxosporea: Myxobolidae) in an oligochaete alternate host, Tubifex tubifex. Dis Aquat Org 48:117–123

    PubMed  Google Scholar 

  • Székely C, Hallett SL, Atkinson SD, Molnár K (2009) Complete life cycle of Myxobolus rotundus (Myxosporea: Myxobolidae), a gill myxozoan of common bream Abramis brama. Dis Aquat Org 85:147–155

    PubMed  Google Scholar 

  • Tocher DR, Sargant JR, Frerichs GN (1988) The fatty acid composition of established fish cell lines after long term culture in mammalian sera. Fish Physiol Biochem 5:219–277

    CAS  PubMed  Google Scholar 

  • Tops S (2004) Ecology, life history and diversity of malacosporeans. In Animal and microbial sciences, University of Reading, pp 206

    Google Scholar 

  • Tops S, Lockwood W, Okamura B (2006) Temperature-driven proliferation of Tetracapsuloides bryosalmonae in bryozoan hosts portends salmonid declines. Dis Aquat Org 70:227–236

    CAS  PubMed  Google Scholar 

  • Tops S, Hartikainen HL, Okamura B (2009) The effects of infection by Tetracapsuloides bryosalmonae (Myxozoa) and temperature on Fredericella sultana (Bryozoa). Int J Parasitol 39:1003–1010

    PubMed  Google Scholar 

  • Trouillier A, El-Matbouli M, Hoffmann RW (1996) A new look at the life-cycle of Hoferellus carassii in the goldfish (Carassius auratus auratus) and its relation to kidney enlargement disease (KED). Folia Parasitol 43:173–187

    Google Scholar 

  • Tyutyaev PYu (2008) Organization of the chromosomal apparatus Myxozoa Tsitologiya 50:907–910

    Google Scholar 

  • Udey lR, Fryer JL, Pilcher KS 1975. Relation of water temperature to ceratomyxosis in rainbow trout (Salmo gairdneri) and coho salmon (Oncorhynchus kisutch). J Fish Res Board Canada 32:1545–1551

    Google Scholar 

  • Urawa S (1994) Life cycle of Myxobolus arcticus, a myxosporean parasite of salmonid fishes. Int Symp Aquat Anim Health, Program and Abstracts, Seattle, 4–8 Sept 1994, p. W-10.3

    Google Scholar 

  • Urawa S, Freeman MA, Johnson SC et al (2011) Geographical variation in spore morphology, gene sequences, and host specificity of Myxobolus arcticus (Myxozoa) infecting salmonid nerve tissues. Dis Aquat Org 96:229–237

    PubMed  Google Scholar 

  • Uspenskaya AV (1957) The ecology and spreading of the pathogen of Myxosoma cerebralis of trout in the fish ponds of the Soviet Union. In: Petrushevski GK (ed) Parasites and diseases of fish. Bull Inst Freshw Fish 42. Leningrad

    Google Scholar 

  • Uspenskaya AV (1995) Alternation of actinosporean and myxosporean phases in the life cycle of Zschokkella nova (Myxozoa). J Eukaryot Microbiol 42:665–668

    CAS  PubMed  Google Scholar 

  • Wolf K, Markiw ME (1976) Myxosoma cerebralis: in vitro sporulation of the myxosporidian of salmonid whirling disease. J Protozool 23:425–427

    CAS  PubMed  Google Scholar 

  • Wolf K, Markiw ME (1984) Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 225:1449–1452

    CAS  PubMed  Google Scholar 

  • Wood TS (1971) Laboratory culture of freshwater Ectoprocta. Trans Amer Micros Soc 90:229–231

    Google Scholar 

  • Wood TS (1996) Aquarium culture of freshwater invertebrates. Am Biol Teach 58:46–50

    Google Scholar 

  • Yanagida T, Nomura Y, Kimura T et al (2004) Molecular and morphological redescriptions of enteric myxozoans, Enteromyxum leei (formerly Myxidium sp. TP) and Enteromyxum fugu comb. n. (syn. Myxidium fugu) from cultured tiger puffer. Fish Pathol 39:137–14

    CAS  Google Scholar 

  • Yanagida T, Sameshima M, Nasu H et al (2006) Temperature effects on the development of Enteromyxum spp. (Myxozoa) in experimentally infected tiger puffer, Takifugu rubripes (Temminck & Schlegel). J Fish Dis 29:561–567

    CAS  PubMed  Google Scholar 

  • Yanagida T, Palenzuela O, Hirae T et al (2008) Myxosporean emaciation disease of cultured red sea bream Pagrus major and spotted knifejaw Oplegnathus punctatus. Fish Pathol 43:45–48

    Google Scholar 

  • Yasuda H, Ooyama T, Iwata K et al (2002) Fish-to-fish transmission of Myxidium spp. (Myxozoa) in cultured tiger puffer suffering from emaciation disease. Fish Pathol 37:29–33

    Google Scholar 

  • Yokoyama H (1997) Transmission of Thelohanellus hovorkai Achmerov, 1960 (Myxosporea: Myxozoa) to common carp Cyprinus carpio through the alternate oligochaete host. Syst Parasitol 36:79–84

    Google Scholar 

  • Yokoyama H, Yutaka F (1999) In vitro sporulation of Myxobolus spirosulcatus and Ceratomyxa spp. (Myxozoa: Myxosporea) infecting the gallbladder of yellowtail Seriola quinqueradiata. In: 9th international conference diseases of fish and shellfish of European Association of Fish Pathologists, Rhodes, Greece, p 210

    Google Scholar 

  • Yokoyama H, Ogawa K, 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 Pathol 28:135–139

    Google Scholar 

  • Yasuda H, Ooyama T, Nakamura A, Iwata K, Palenzuela O, Yokoyama H (2005) Occurrence of the myxosporean emaciation disease caused by Enteromyxum lee, in cultured Japanese flounder Paralichthys olivaceus. Fish Pathol 40:175–180

    Google Scholar 

  • Yokoyama H, Ogawa K, Wakabayashi H (1995) Myxobolus cultus n. sp. (Myxosporea: Myxobolidae) in the goldfish Carassius auratus transformed from the actinosporean stage in the oligochaete Branchiura sowerbyi. J Parasitol 81:446–451

    CAS  PubMed  Google Scholar 

  • Yokoyama H, Danjo T, Ogawa K et al (1997) A vital staining technique with fluorescein-diacetate (FDA) and propidium iodide (PI) for the determination of viability of myxosporean and actinosporean spores. J Fish Dis 20:281–286

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungarian Academy of Sciences, P.O. Box 18, H-1581, Budapest, Hungary

    Edit Eszterbauer

  2. Department of Microbiology, Oregon State University, 226 Nash Hall, Corvallis, OR, 97331-3804, USA

    Stephen Atkinson

  3. National Center for Mariculture, Israel Oceanographic and Limnological Research, P.O. Box 1212, 88112, Eilat, Israel

    Arik Diamant

  4. Department of Mathematics and Statistics, University of Strathclyde, Glasgow, UK

    David Morris

  5. Clinical Unit of Fish Medicine, University of Veterinary Medicine, Veterinärplatz 1, 1210, Vienna, Austria

    Mansour El-Matbouli

  6. ETH Zürich and Eawag, Institute for Integrative Biology, Ueberlandstrasse 133, 8600, Duebendorf, Switzerland

    Hanna Hartikainen

Authors
  1. Edit Eszterbauer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen Atkinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arik Diamant
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David Morris
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mansour El-Matbouli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hanna Hartikainen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Edit Eszterbauer .

Editor information

Editors and Affiliations

  1. Department of Life Sciences, Natural History Museum, London, United Kingdom

    Beth Okamura

  2. Department of Life Sciences, Natural History Museum, London, United Kingdom

    Alexander Gruhl

  3. Department of Microbiology, Oregon State University, Corvallis, Oregon, USA

    Jerri L. Bartholomew

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Eszterbauer, E., Atkinson, S., Diamant, A., Morris, D., El-Matbouli, M., Hartikainen, H. (2015). Myxozoan Life Cycles: Practical Approaches and Insights. In: Okamura, B., Gruhl, A., Bartholomew, J. (eds) Myxozoan Evolution, Ecology and Development. Springer, Cham. https://doi.org/10.1007/978-3-319-14753-6_10

Download citation

Publish with us

Policies and ethics

Search

Navigation