Skip to main content
SpringerLink
Log in

Myxozoans Exploiting Homeotherms

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

Abstract

Discoveries published in 2007 and 2008 expanded the known host range of myxozoans beyond poikilotherms to include mammals and birds. Here we review records of myxozoans from small terrestrial mammals, waterfowl and those associated with humans, and augment them with data from our ongoing studies. True myxosporean infections—those with active parasite development and sporogenesis—have been recorded for Soricimyxum spp. in central European shrews and Myxidium spp. in North American waterfowl. In all cases, bile ducts within the liver were the nidal tissue and complete life cycles are unknown. Incidental myxosporean infections—the presence of myxospores without parasite development—have been observed in humans, usually in association with the ingestion of infected fish. Clinical presentations of these cases range from no disease (e.g. Henneguya spp.), allergic responses (Kudoa sp.) or acute gastroenteritis (Kudoa septempunctata). Phylogenetically, myxosporean parasites of homeotherms cluster closely with Myxidium and Cystodiscus species known to infect other terrestrial vertebrates (reptiles and amphibians), which suggests a single evolutionary expansion from an aquatic Myxidium-clade ancestor to semi-aquatic and terrestrial hosts and environments. Given the diversity of potential mammalian and avian hosts, we expect additional myxosporean parasites to be discovered with further scrutiny of these homeotherms, especially in sparsely surveyed regions including Africa and South America.

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

  • Bartholomew JL, Atkinson SD, Hallett SL, Lowenstine LJ, Garner MM, Gardiner CH, Rideout BA, Keel MK, Brown JD (2008) Myxozoan parasitism in waterfowl. Int J Parasitol 38:1199–1207

    PubMed  Google Scholar 

  • Boreham RE, Hendrick S, O’Donoghue PJ, Stenzel DJ (1998) Incidental finding of Myxobolus spores (Protozoa: Myxozoa) in stool samples from patients with gastrointestinal symptoms. J Clin Microbiol 36:3728–3730

    PubMed Central  CAS  PubMed  Google Scholar 

  • Butterfield J, Coulson JC, Wanless S (1981) Studies on the distribution, food, breeding biology and relative abundance of the pygmy and common shrews (Sorex minutus and S. araneus) in upland areas of northern England. J Zool Lond 195:169–180

    Google Scholar 

  • Churchfield S, Rychlik L, Taylor JRE (2012) Food resources and foraging habits of the common shrew, Sorex araneus: does winter food shortage explain Dehnel’s phenomenon? Oikos 121:1593–1602. doi:10.1111/j.1600-0706.2011.20462.x

    Article  Google Scholar 

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

    Google Scholar 

  • Dyková I, Tyml T, Fiala I, Lom J (2007) New data on Soricimyxum fegati (Myxozoa) including analysis of its phylogenetic position inferred from the SSU rRNA gene sequence. Folia Parasitol 54:272–276

    PubMed  Google Scholar 

  • Dyková I, Tyml T, Kostka M (2011) Xenoma-like formations induced by Soricimyxum fegati (Myxosporea) in three species of shrews (Soricomorpha: Soricidae), including records of new hosts. Folia Parasitol 58:249–256

    PubMed  Google Scholar 

  • Eiras JC (2005) An overview on the myxosporean parasites in amphibians and reptiles. Acta Parasitol 50:267–275

    Google Scholar 

  • El-Matbouli M, Hoffmann RW (1991) Effects of freezing, aging, and passage through the alimentary canal of predatory animals on the viability of Myxobolus cerebralis spores. J Aquat Anim Health 4:44–47

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • El-Matbouli M, Sobottka I, Schumacher U, Schottelius J (2005) Effect of passage through the gastrointestinal tract of mice on the viability of Myxobolus cerebralis (Myxozoa) spores. Bull Eur Assoc Fish Pathol 25:276–279

    Google Scholar 

  • Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534

    CAS  PubMed  Google Scholar 

  • Ficke AD, Myrick CA, Hansen LJ (2007) Potential impacts of global climate change on freshwater fisheries. Rev Fish Biol Fisher 17:581–613

    Google Scholar 

  • Friedrich C, Ingolic E, Freitag B, Kastberger G, Hohmann V, Skofitsch G, Neumeister U, Kepka O (2000) A myxozoan-like parasite causing xenomas in the brain of the mole, Talpa europaea L., 1758 (Vertebrata, Mammalia). Parasitol 121:483–492

    Google Scholar 

  • Garner MM, Bartholomew JL, Whipps CM, Nordhausen RW, Raiti P (2005) Renal myxozoanosis in crowned river turtles Hardella thurjii: description of the putative agent Myxidium hardella n. sp. by histopathology, electron microscopy, and DNA sequencing. Vet Pathol 42:589–595

    CAS  PubMed  Google Scholar 

  • Grabner DS, Yokoyama H, Shirakashi S, Kinami R (2012) Diagnostic PCR assays to detect and differentiate Kudoa septempunctata, K. thyrsites and K. lateolabracis (Myxozoa, Multivalvulida) in muscle tissue of olive flounder (Paralichthys olivaceus). Aquaculture 338–341:36–40

    Article  Google Scholar 

  • Guo QX, Gu ZM, Jia L, Qing JH, Li H (2014) Pathogenicity studies of Myxobolus honghuensis (Myxosporea: Bivalvulida) using suckling mice model. Paper presented at the 7th international symposium on aquatic animal health, Portland Oregon, USA, 31 Aug—4 Sept 2014

    Google Scholar 

  • Harada T, Kawai T, Sato H, Yokoyama H, Kumeda Y (2012a) Development of a quantitative polymerase chain reaction assay for detection of Kudoa septempunctata in olive flounder (Paralichthys olivaceus). Int J Food Microbiol 156:161–167

    CAS  PubMed  Google Scholar 

  • Harada T, Kawai T, Jinnai M, Ohnishi T, Sugita-Konishi Y, Kumeda Y (2012b) Detection of Kudoa septempunctata 18S Ribosomal DNA in patient fecal samples from novel food-borne outbreaks caused by consumption of raw olive flounder (Paralichthys olivaceus). J Clin Microbiol 50:2964–2968

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hartigan A, Fiala I, Dyková I, Rose K, Phalen DN, Šlapeta J (2012) New species of Myxosporea from frogs and resurrection of the genus Cystodiscus Lutz, 1889 for species with myxospores in gallbladders of amphibians. Parasitology 139:478–496

    Article  PubMed  Google Scholar 

  • Iijima Y, Nakanishi N, Furusawa H, Ohnishi T, Sugita-Konishi Y (2012) Inter-laboratory validation and applications of quantitative real-time PCR for the detection of Kudoa septempunctata in olive flounder (Paralichthys olivaceus). Jpn J Infect Dis 65:436–438

    CAS  PubMed  Google Scholar 

  • Iwashita Y, Kamijo Y, Nakahashi S, Shindo A, Yokoyama K, Yamamoto A, Omori Y, Ishikura K, Fujioka M, Hatada T, Takeda T, Maruyama K, Imai H (2013) Food poisoning associated with Kudoa septempunctata. J Emerg Med 44:943–945. doi:10.1016/j.jemermed.2012.11.026

    PubMed  Google Scholar 

  • Jirkù M, Bolek MG, Whipps CM, Janovy J Jr, Kent ML, Modrÿ D (2006) A new species of Myxidium (Myxosporea: Myxidiidae), from the western chorus frog, Pseudacris triseriata triseriata, and Blanchard’s cricket frog, Acris crepitans blanchardi (Hylidae), from eastern Nebraska: morphology, phylogeny, and critical comment. J Parasitol 92:611–619

    PubMed  Google Scholar 

  • 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  Google Scholar 

  • Lebbad M, Willcox M (1998) Spores of Henneguya salminicola in human stool specimens. J Clin Microbiol 36:182

    Google Scholar 

  • Lom J, Dyková I (2005) Microsporidian xenomas in fish seen in wider perspective. Folia Parasitol 52:69–81

    PubMed  Google Scholar 

  • Lom J, Dyková I, Feist S (1989) Myxosporea-induced xenoma formation in pike, Esox lucius L., renal corpuscles associated with Myxidium lieberkuehni infection. Eur J Protistol 24:271–280

    CAS  PubMed  Google Scholar 

  • Martínez de Velasco G, Cuéllar C (2003) Humoral immune responses induced by Kudoa sp. (Myxosporea: Multivalvulida) in BALB/c mice: oral administration, immunization and cross-reactions with Myxobolus aeglefini (Myxosporea: Bivalvulida). Parasite Immunol 25:449–456

    PubMed  Google Scholar 

  • Martínez de Velasco G, Rodero M, Zapatero L, Cuéllar C (2002) Humoral immune responses induced by Kudoa sp. (Myxosporea: Multivalvulida) antigens in BALB/c mice. Memórias do Instituto Oswaldo Cruz 97:1091–1095

    Article  PubMed  Google Scholar 

  • Martínez de Velasco G, Rodero M, Chivato C, Cuéllar C (2007) Seroprevalence of anti-Kudoa sp. (Myxosporea: Multivalvulida) antibodies in a Spanish population. Parasitol Res 100:1205–1211

    PubMed  Google Scholar 

  • Martínez de Velasco G, Rodero M, Cuéllar C, Chivato T, Mateos JM, Laguna R (2008) Skin prick test of Kudoa sp. antigens in patients with gastrointestinal and/or allergic symptoms related to fish ingestion. Parasitol Res 103:713–715

    PubMed  Google Scholar 

  • 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  Google Scholar 

  • McClelland RS, Murphy DM, Cone DK (1997) Report of spores of Henneguya salminicola (Myxozoa) in human stool specimens: possible source of confusion with human spermatozoa. J Clin Microbiol 35:2815–2818

    PubMed Central  CAS  PubMed  Google Scholar 

  • Moncada LI, Lo´pez MC, Murcia MI, Nicholls S, León F, Guío OL, Corredor A (2001) Myxobolus sp., another opportunistic parasite in immunosuppressed patients. J Clin Microbiol 39:1938–1940

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ohnishi T, Kikuchi Y, Furusawa H, Kamata Y, Sugita-Konishi Y (2013a) Kudoa septempunctata invasion increases the permeability of human intestinal epithelial monolayer. Foodborne Pathog Dis 10:137–142. doi:10.1089/fpd.2012.1294

    PubMed  Google Scholar 

  • Ohnishi T, Furusawa H, Yoshinari T, Yamazaki A, Horikawa K, Kamata Y, Sugita-Konishi Y (2013b) Electron microscopic study of Kudoa septempunctata infecting Paralichthys olivaceus (olive flounder). Jpn J Infect Dis 66:348–350

    PubMed  Google Scholar 

  • Prunescu C-C, Prunescu P, Pucek Z, Lom J (2007) The first finding of myxosporean development from plasmodia to spores in terrestrial mammals: Soricimyxum fegati gen. et sp. n. (Myxozoa) from Sorex araneus (Soricomorpha). Folia Parasitol 54:159–164

    PubMed  Google Scholar 

  • Redondo MJ, Palenzuela O, Riaza A, Macías Á, Álvarez-Pellitero P (2002) Experimental transmission of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. J Parasitol 88:482–488

    PubMed  Google Scholar 

  • Székely C, Cech G, Ostoros G, Gubányi A (2011) First occurrence of myxozoan parasites in small mammals (Sorex araneus and Sorex minutus) in Hungary. In: Abstract book of the 15th international conference on diseases of fish and shellfish, Split, Croatia, p 436, 12–16 Sept

    Google Scholar 

  • Whipps CM (2013) Myxozoa: the spore-forming cnidarians. In: Goater TM, Goater CP, Esch GW (eds) Parasitism: the diversity and ecology of animal parasites, 2nd edn. Cambridge University Press, New York, p 109

    Google Scholar 

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

    Google Scholar 

Download references

Acknowledgments

We are grateful to Dr Richard Ostfeld for providing the North American East coast shrews, Sorex sp. CsS received support from the Hungarian Scientific Research Fund (OTKA) grant K 100132 and KTIA-AIK-12-1-2013-0017 for the shrew research. SLH and JLB received support from the Oregon State University General Research Fund for the duck myxozoan DNA analyses.

Author information

Authors and Affiliations

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

    Sascha L. Hallett, Stephen D. Atkinson & Jerri L. Bartholomew

  2. Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungarian Academy of Sciences, Budapest, Hungary

    Csaba Székely

Authors
  1. Sascha L. Hallett
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen D. Atkinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jerri L. Bartholomew
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Csaba Székely
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sascha L. Hallett .

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

Hallett, S.L., Atkinson, S.D., Bartholomew, J.L., Székely, C. (2015). Myxozoans Exploiting Homeotherms. 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_7

Download citation

Publish with us

Policies and ethics

Search

Navigation