Can Myxosporean parasites compromise fish and amphibian reproduction?

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1669, 2009, Pages 2861-2870

  Sitjà Bobadilla, Ariadna ^a  

^a CSIC Instituto de Acuicultura de Torre de la Sal IATS   (Spain)

Author keywords

Gonads; Immune response; Myxozoa; Pathology; Sex

Indexed keywords

AMPHIBIAN; AQUACULTURE; AQUATIC ENVIRONMENT; FISH; FRESHWATER ECOSYSTEM; HOST-PARASITE INTERACTION; IMMUNE RESPONSE; INFECTIOUS DISEASE; LIFE CYCLE; PARASITE; POPULATION DISTRIBUTION; REPRODUCTION; SEX REVERSAL; SPAWNING;

AMPHIBIA; AQUACULTURE; FISH; GONAD DYSFUNCTION; HUMAN; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; MYXOSPORE; PARASITOSIS; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SEX TRANSFORMATION;

AMPHIBIA; ANIMALIA; MYXOSPOREA; MYXOZOA;

EID: 68249104396     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.0368     Document Type: Review

References (74)

1. Abed, G. H. & Galal, A. A. 1993 The discovery of Myxobolus sp. in the testis of the Egyptian toad Bufo regularis, with detailed description of the cyst and spores. Assiut Vet. Med. J. 58, 115-122.
2. Afifi, S. H., Farid, R. N., Marwan, A. & Hassanein, A. M. 1999 Light and electronic microscopical observations on Myxosporidia in Nile catfish, Clarias lazera. Assiut Vet. Med. J. 41, 88-114.
3. Alderstein, S. A. & Dorn, M. W. 1998 The effect of Kudoa paniformis infection on the reproductive effort of female Pacific hake. Can. J. Zool. 76, 2285-2289.
4. Alvarez-Pellitero, P. & Sitjà-Bobadilla, A. 1993 Pathology of Myxosporea in marine fish culture. Dis. Aquat. Organ. 17, 229-238. (doi:10.3354/dao017229)
5. Aragão, M. 1919 Myxobolus lutzi n. sp. Rev. Soc. Bras. Ciéncias 3, 325.
6. Azevedo, C., Corral, L. & Matos, E. 1997 Light and ultrastructural data on Henneguya testicularis n. sp. (Myxozoa, Myxobolidae), a parasite from the testis of the Amazonian fish Moenkhausia oligolepis. Syst. Parasitol. 37, 111-114. (doi:10.1023/A:1005793930837)
7. Barber, I., Hoare, D. & Krause, J. 2000 Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev. Fish Biol. Fish. 10, 131-165. (doi:10.1023/ A:1016658224470)
8. Binuramesh, C., Prabakaran, M., Steinhagen, D. & Michael, R. D. 2006 Effect of sex ratio on the immune system of Oreochromis mossambicus (Peters). Brain Behav. Immun. 20, 300-308. (doi:10.1016/j.bbi. 2005.09.002)
9. Blazer, V. S. 2002 Histopathological assessment of gonadal tissue in wild fishes. Fish Physiol. Biochem. 26, 85-101. (doi:10.1023/A: 1023332216713)
10. Blázquez, M., Carrilo, M., Zanuy, S. & Piferrer, F. 1999 Sex ratios in offspring of sex-reversed sea bass and the relationship between growth and phenotypic sex differentiation. J. Fish Biol. 55, 916-930. (doi:10.1111/ j.1095-8649.1999.tb00730.x)
11. Bonetto, A. & Pignalberi, C. 1965 Myxobolus paranensis (Protozoa, Myxosporidea), una nueva especie parásita del 'Dorado' (Salminus maxillosus). Physis 25, 23-26.
12. Browne, R., Scheltinga, D., Pomering, M. & Mahony, M. 2002 Testicular myxosporidiasis in anurans, with a description of Myxobolus fallax n. sp. Syst. Parasitol. 52, 97-110. (doi:10.1023/A:1015609513809)
13. Browne, R. K., Li, R. & Vaughan, M. 2006 Sexually mediated shedding of Myxobolus fallax spores during spermiation of Litoria fallax (Anura). Dis. Aquat. Organ. 72, 71-75. (doi:10.3354/dao072071)
14. Canning, E. U. & Okamura, B. 2004 Biodiversity and evolution of the Myxozoa. Adv. Parasitol. 56, 43-131. (doi:10.1016/S0065-308X(03) 56002-X)
15. Chen, C. L. & Hsieh, S. R. 1984 A genus and two new species of family Myxobolidae from freshwater fishes of China (Myxosporidia: Myxobolidae). Acta Zootaxon. Sin. 9, 113-117.
16. Cohn, L. 1895 Ueber die Myxosporidien von Esox lucius und Perca fluviatilis. Inaugural diss, Albertus Univ Königsber, pp. 1-14.
17. Cone, D. K. & Easy, R. H. 2005 Supplemental diagnosis and molecular taxonomy of Myxobolus diaphanous (Fantham, Porter and Richardson, 1940) (Myxozoa) parasitizing Fundulus diaphanous (Cyprinodontifornes) in Nova Scotia, Canada. Folia Parasitol. 52, 217-222.
18. Diamant, A. 1997 Fish-to-fish transmission of a marine myxosporean. Dis. Aquat. Organ. 30, 99-105. (doi:10.3354/ dao030099)
19. Diamant, A., Ucko, M., 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. (doi:10.1645/ GE-491R.1)
20. Dunkerly, J. S. 1915 Agarella gracilis, a new genus and species of myxosporidian parasitic in Lepidosiren paradoxa. Proc. R. Phys. Soc. Edinb. 19, 213-219.
21. Eiras, J. C., Molnár, K. & Lu, Y. S. 2005 Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Syst. Parasitol. 61, 1-46. (doi:10.1007/s11230-004- 6343-9)
22. El Garhy, M. F. 2003 A survey of the parasites of some freshwater fishes from the River Nile. J. Egypt. Ger. Soc. Zool. 40, 115-137.
23. Elkamel, A. A. & Tantawy, A. 2005 Myxobolus infestation in ovaries of sharptooth catfish, Clarias gariepinus. Assiut Vet. Med. J. 51, 54-66.
24. Ewers, W. H. 1973 Myxobolus chimbuensis sp. n. (family Myxobolidae: Cnidsoporidia; Protozoa) from the testes of the hylid frog Litoria darlingtoni from New Guinea. Sci. N. G. 1, 16-20.
25. Fijak, M. & Meinhardt, A. 2006 The testis in immune privilege. Immunol. Rev. 13, 66-81.
26. Fomena, A. & Bouix, G. 1997 Myxosporea (Protozoa: Myxozoa) of freshwater fishes in Africa: keys to genera and species. Syst. Parasitol. 37, 161-178. (doi:10.1023/ A:1005839220014)
27. Gbankoto, A., Pampoulie, C., Marques, A. & Sakiti, G. N. 2001 Myxobolus dahomeyensis infection in ovaries of Tilapia species from Benin (West Africa). J. Fish Biol. 58, 883-886. (doi:10.1111/j.1095- 8649.2001.tb00539.x)
28. Jiménez-Guri, E., Philippe, H., Okamura, B. & Holland, P. W. H. 2007 Buddenbrockia is a Cnidarian worm. Science 317, 116-118. (doi:10.1126/science.1142024)
29. Jobling, S., Nolan, M., Tyler, C. B., Brighty, G. & Sumpter, J. P. 1998 Widespread sexual disruption in wild fish. Environ. Sci. Technol. 32, 2498-2506. (doi:10.1021/ es9710870)
30. Johnson, P. T. J., Sutherland, D. R., Kinsella, J. M. & Lunde, K. B. 2004 Review of the trematode genus Ribeiroia (Psilostomidae): ecology, life history and pathogenesis with special emphasis on the amphibian malformation problem. Adv. Parasitol. 57, 191-253. (doi:10.1016/ S0065-308X(04)57003-3)
31. Johnston, T. H. & Bancroft, M. J. 1918 A parasite Myxobolus hylae n. sp. of the reproductive organs of the golden swamp frog, Hyla aurea. J. R. Soc. NSW 43, 171-175.
32. Kabata, Z. 1962 Five new species of Myxosporidia from marine fishes. Parasitology 52, 177-186.
33. Kent, M. L. et al. 2001 Recent advances in our knowledge of the Myxozoa. J. Eukaryot. Microbiol. 48, 395-413. (doi:10.1111/j.1550- 7408.2001.tb00173.x)
34. Lom, J. & Dyková, I. 2006 Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol. 53, 1-36.
35. Longshaw, M., Katsiadaki, I., Assuncao, M., Small, H. & Feist, S. W. 2007 Redescription of a long lost Myxobilatus sp. (Myxozoa) from the ovaries of the three-spined stickleback (Gasterosteus aculeatus). ISFP VII Abstracts. Parassitologia 49, 158.
36. Mandour, A. M., Galal, A. A. & Abed, G. H. 1993 Myxobolus clarii n. sp. in the testis of fish Clarias lazera from the river Nile of Assiut. Assiut Vet. Med. J. 58, 108-114.
37. Mills, L. J. & Chichester, C. 2005 Review of evidence: are endocrine-disrupting chemicals in the aquatic environment impacting fish populations? Sci. Total Environ. 343, 1-34.
38. Mochida, K. & Takahashi, H. 1993 Sperm fertility caused by experimental testicular autoimmunity in the Nile tilapia. Nippon Suisan Gakk. 59, 253-261.
39. Moran, J. D. W., Whitaker, D. J. & Kent, M. L. 1999 A review of the myxosporean genus Kudoa Meglitsch, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172, 163-195. (doi:10.1016/S0044-8486(98)00437-2)
40. Moshu, A. Y. 1992 Description of Sphaerospora lucioperca sp. nov. (Protista: Myxosporea): parasite of Stizostedion lucioperca. Bul. Akad. Stiinte Republicci Moldova. Stinnte Biologice si Chimice 2, 54-56.
41. Mubarak, M. & Abed, G. H. 2001 Morphopathological changes of the testicular tissue of Egyptian toad, Bufo regularis (Amphibia, Bufonidae) infected with Myxobolus sp. (Myxozoa, Myxobolidae). Acta Parasitol. 46, 113-118.
42. Nóbrega, R. H., Batlouni, S. R. & França, L. R. 2009 An overview of functional and stereological evaluation of spermatogenesis and germ cell transplantation in fish. Fish Physiol. Biochem. 35, 197-206. (doi:10.1007/ s10695-008-9252-z)
43. Obiekezie, A. I. & Okaeme, N. 1990 Myxosporea (Protozoa) infections of cultured tilapias in Nigeria. J. Afr. Zool. 104, 77-91.
44. Ottová, E., Simková, A., Jurajda, P., Dá vidová, M., Ondrackova ́, M., Pecínkova, M. & Gelnar, M. 2005 Sexual ornamentation and parasite infection in males of common bream (Abramis brama): a reflection of immunocompetence status or simple cost of reproduction? Evol. Ecol. Res. 7, 581-593.
45. Palenzuela, O. 2006 Myxozoan infections in Mediterranean mariculture. Parassitologia 48, 27-29.
46. Paperna, I. 1973 Occurrence of Cnidospora infections in freshwater fishes in Africa. Bull. Inst. Fr. Afr. Noire 35, 509-521.
47. Pasmans, F., Mutschmann, F., Halliday, T. & Zwart, P. 2006 Amphibian decline: the urgent need for amphibian research in Europe. Vet. J. 171, 18-19. (doi:10.1016/j. tvjl.2004.12.006)
48. Pinto, C. 1928 Myxosporideos e outros protozoarios intestinaes de pixes observados na America do Sul. Inst. Biol., S. Paulo 1, 101-136.
49. Pough, F. H. 2007 Amphibian biology and husbandry. ILAR J. 48, 203-213.
50. Powell, M. L., Kavanaugh, S. I. & Sower, S. A. 2005 Current knowledge of hagfish reproduction: implications for fisheries management. Integr. Comp. Biol. 45, 158-165. (doi:10.1093/icb/45.1.158)
51. Redondo, M. J., Palenzuela, O. & Alvarez-Pellitero, P. 2005 Studies on transmission and life cycle of Enteromyxum scophthalmi (Myxozoa), an enteric parasite of turbot Scophthalmus maximus. Folia Parasitol. 51, 188-198.
52. Reed, C. C., Basson, L. & Van As, L. L. 2003 Myxozoans infecting the sharptooth catfish, Clarias gariepinus in the Okavango River and Delta, Botswana, including descriptions of two new species, Henneguya samochimensis sp. n. and Myxobolus gariepinus sp. n. Folia Parasitol. 50, 183-189.
53. Rigos, G., Christophilogiannis, P., Yiagnisi, M., Andriopoulou, A., Koutsodimou, M., Nengas, I. & Alexis, M. 1999 Myxosporean infection in Greek mariculture. Aquacult. Int. 7, 361-364. (doi:10.1023/A: 1009200732200)
54. Sakiti, G. N., Blanc, E., Marques, A. & Bouix, G. 1991 Myxosporidies (Myxozoa, Myxosporea) du genre Myxobolus Bütschli, 1882 parasites de poissons Cichlidae du lac Nokoué au Bénin (Afrique de l'Ouest). J. Afr. Zool. 105, 173-186.
55. Schärer, L. & Vizoso, D. B. 2003 Earlier sex change in infected individuals of the protogynous reef fish Thalassoma bifasciatum. Behav. Ecol. Sociobiol. 55, 137-143. (doi:10.1007/s00265-003-0694-0)
56. Shulman, S. S. 1966 Myxosporidia of the USSR. Nauka Publ., Moscow-Leningrad. English translation for US Department of Interior and National Science Foundation, Washington DC by Amerind Publication Company Pvt. Ltd, New Delhi, 1988.
57. Siau, Y. 1971 Myxosporidies de Synodontis ansorgii Bouleng. Ann. Et N.H. 1911 et de Eleotris (Kribia) kribensis Boulenger 1964, poisons des eaux saumâtres de la lagune de PortoNovo (Dahomey). Bull. Soc. Zool. Fr. 96, 563-570.
58. Sitjà-Bobadilla, A. & Alvarez-Pellitero, P. 1990 Sphaerospora testicularis sp. nov. (Myxosporea: Sphaerosporidae) in wild and cultured sea bass (Dicentrarchus labrax) from the Spanish Mediterranean area. J. Fish Dis. 13, 193-203. (doi:10.1111/j.1365- 2761.1990.tb00774.x)
59. Sitjà-Bobadilla, A. & Alvarez-Pellitero, P. 1992a Light and electron microscopic description of Sphaerospora dicentrarchi n. sp. (Myxosporea: Sphaerosporidae) from wild and cultured sea bass, Dicentrarchus labrax L. J. Protozool. 39, 273-281.
60. Sitjà-Bobadilla, A. & Alvarez-Pellitero, P. 1992b Effect of Fumagillin treatment on sea bass Dicentrarchus labrax parasitized by Sphaerospora testicularis (Myxosporea: Bivalvulida). Dis. Aquat. Organ. 14, 171-178. (doi:10.3354/dao014171)
61. Sitjà-Bobadilla, A. & Alvarez-Pellitero, P. 1993a Ultrastructural and cytochemical observations on the sporogenesis of Sphaerospora testicularis (Protozoa: Myxosporea) from Mediterranean sea bass, Dicentrarchus labrax (L.). Eur. J. Protistol. 29, 219-229.
62. Sitjà-Bobadilla, A. & Alvarez-Pellitero, P. 1993b Pathological effects of Sphaerospora dicentrarchi Sitjà-Bobadilla et Alvarez-Pellitero (1992) and S. testicularis Sitjà-Bobadilla-Alvarez-Pellitero, (1990) parasitic of sea bass (Dicentrarchus labrax L.) (Teleostei: Serranidae), and cell mediated immune reaction: light and electron microscopic study. Parasitol. Res. 79, 119-129. (doi:10.1007/ BF00932257)
63. Sitjà-Bobadilla, A. & Alvarez-Pellitero, P. 1993c Population dynamics of Sphaerospora dicentrarchi Sitjà-Bobadilla et Alvarez-Pellitero, 1992 and S. testicularis Sitjà-Bobadilla et al. varez-Pellitero, 1990 (Myxosporea: Bivalvulida) infections in wild and cultured sea bass (Dicentrarchus labrax L.). Parasitology 106, 39-45.
64. Skarstein, F., Folstad, I. & Liljedal, S. 2001 Whether to reproduce or not: immune suppression and costs of parasites during reproduction in the Arctic charr. Can. J. Zool. 79, 271-278. (doi:10.1139/cjz-79-2- 271)
65. Souder, W. 2000 A plague of frogs. New York, NY: Hyperion Press.
66. Summerfelt, R. C. & Warner, M. 1970 Incidence and intensity of infection of Pleistophora ovariae, a microsporidian parasite of the golden shiner, Notemigonus crysoleucas. In Symp. on Diseases of Fishes and Shellfishes Special Publ. no. 5. (ed. S. F. Sniezsko), pp. 142-160. Washington, DC: American Fish Society.
67. Swearer, S. E. & Robertson, D. R. 1999 Life history, pathology, and description of Kudoa ovivora n. sp. (Myxozoa, Myxosporea): an ovarian parasite of Caribbean labroid fishes. J. Parasitol. 85, 337-353. (doi:10.2307/3285645)
68. Tajdari, J., Matos, E., Mendonta, I. & Azevedo, C. 2005 Ultrastructural morphology of Myxobolus testicularis sp. n., parasite of the testis of Hemiodopsis microlepis (Teleostei: Hemiodontidae) from the NE of Brazil. Acta Protozool. 44, 377-384.
69. Théodoridès, J., Pujol, P., Neyrand-de-Leffemebr, F. & Delso, M. 1981 New cases of testicular parasitism of amphibians by myxosporideans of the genus Myxobolus. Bull. Soc. Zool. Fr. 106, 386.
70. Torres, A., Matos, E. & Azevedo, C. 1994 Fine structure of Henneguya amazonica (Myxozoa) in ovarian follicles of Hoplosternum littorale (Teleostei) from the Amazon River. Dis. Aquat. Organ. 19, 168-172.
71. Upton, S. J., Freed, P. S., Freed, D. A., McAllister, C. T. & Goldberg, S. R. 1992 Testicular myxosporidiasis in the flatbacked toad, Bufo maculatus (Amphibia: Bufonidae), from Cameroon, Africa. J. Wildl. Dis. 28, 326-329.
72. Walliker, D. 1969 Myxosporidia of Brazilian freshwater fishes. J. Parasitol. 55, 942-948. (doi:10.2307/3277155)
73. Xiao, C. & Desser, S. S. 1997 Sphaerospora ovophila n. sp. and Myxobolus algonquinensis n. sp. (Myxozoa, Myxosporea) ovarian parasites of fish from Algonquin Park, Ontario, Canada. J. Eukaryot. Microbiol. 44, 157-161. (doi:10.1111/j.1550-7408.1997.tb05953.x)
74. Zuk, M. 1996 Disease, endocrine-immune interactions, and sexual selection. Ecology 77, 1037-1042. (doi:10.2307/ 2265574)