Morphological and molecular characterisation of Gyrodactylus salmonis (Platyhelminthes, Monogenea) isolates collected in Mexico from rainbow trout (Oncorhynchus mykiss Walbaum)

Veterinary Parasitology

Volumn 186, Issue 3-4, 2012, Pages 289-300

  Rubio Godoy, Miguel ^a   Paladini, Giuseppe ^b   Freeman, Mark A ^c   García Vásquez, Adriana ^d   Shinn, Andrew P ^b  

^a INSTITUTO DE ECOLOGÍA   (Mexico)

^b UNIVERSITY OF STIRLING   (United Kingdom)

^c UNIVERSITY OF MALAYA   (Malaysia)

^d UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Gyrodactylidae; Monogenean; North america; Parasite; Salmonidae

Indexed keywords

INTERNAL TRANSCRIBED SPACER; RIBOSOME DNA;

ARTICLE; CONTROLLED STUDY; DNA SEQUENCE; GENE; GENE IDENTIFICATION; GENETIC ANALYSIS; GEOGRAPHIC DISTRIBUTION; GYRODACTYLUS GOBIENSIS; GYRODACTYLUS RUTILENSIS; GYRODACTYLUS SALARIS; GYRODACTYLUS SALMONIS; HELMINTH; HOST PARASITE INTERACTION; MEXICO; MITOCHONDRIAL COX1 GENE; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE EXAMINATION; PARASITE IDENTIFICATION; PARASITE ISOLATION; PLATYHELMINTH; PROMOTER REGION; PROTOZOAL GENETICS; RAINBOW TROUT; SEQUENCE ANALYSIS; SPECIES DIFFERENTIATION; TAXONOMIC RANK;

ANIMALS; FISH DISEASES; MEXICO; ONCORHYNCHUS MYKISS; PHYLOGENY; PLATYHELMINTHS; TREMATODE INFECTIONS;

GYRODACTYLIDAE; GYRODACTYLUS; GYRODACTYLUS GOBIENSIS; GYRODACTYLUS RUTILENSIS; GYRODACTYLUS SALARIS; MONOGENEA; ONCORHYNCHUS; ONCORHYNCHUS MYKISS; PLATYHELMINTHES; SALMONIDAE;

EID: 84860227411     PISSN: 03044017     EISSN: 18732550     Source Type: Journal    
DOI: 10.1016/j.vetpar.2011.11.005     Document Type: Article

References (68)

1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
2. Armijo O.A. Algunas enfermedades que se presentan en los centros acuícolas de México. II Simposio Latinoamericano de Acuicultura 1980, 1607-1618.
3. Bakke T.A., Cable J., Harris P.D. The biology of gyrodactylid monogeneans: the " Russian-doll killers. Adv. Parasitol. 2007, 64:161-376.
4. Buchmann K., Bresciani J. Parasitic infections in pond-reared rainbow trout Oncorhynchus mykiss in Denmark. Dis. Aquat. Org. 1997, 28:125-138.
5. Buchmann K., Uldal A., Lyholt H. A checklist of metazoan parasites from rainbow trout (Oncorhynchus mykiss). Acta Vet. Scand. 1995, 36:299-318.
6. Camarena-Rosales F., Ruiz-Campos G., De La Rosa-Velez J., Mayden R.L., Hendrickson D.A., Varela-Romero A., García de León F.J. Mitochondrial haplotype variation in wild trout populations (Teleostei: Salmonidae) from northwestern Mexico. Rev. Fish Biol. Fish 2008, 18:33-45.
7. Cavender T.M., Miller R.R. Salmo australis, a new species of fossil salmonid from southwestern Mexico. Contrib. Mus. Paleontol. Univ. Mich. 1982, 26:1-17.
8. Cone D.K., Beverley-Burton M., Wiles M., MacDonald T.E. The taxonomy of Gyrodactylus (Monogenea) parasitizing certain salmonid fishes of North America, with a description of Gyrodactylus nerkae n. sp. Can. J. Zool. 1983, 61:2587-2597.
9. Cone D.K., Cusack R. A study of Gyrodactylus colemanensis Mizelle and Kritsky, 1967 and Gyrodactylus salmonis (Yin and Sproston, 1948) parasitizing captive salmonids in Nova Scotia. Can. J. Zool. 1988, 66:409-415.
10. Cone D.K., Wiles M. Ultrastructural study of attachment of Gyrodactylus colemanensis (Monogenea) to fins of fry of Salmo gairdneri. Proc. Helminth. Soc. Wash. 1989, 56:29-32.
11. Crane J.W., Mizelle J.D. Studies on monogenetic trematodes XXXI Five new species of Gyrodactylus from California fishes. J. Parasitol. 1967, 53:270-273.
12. Ergens R. Gyrodactylus from Eurasian freshwater Salmonidae and Thymallidae. Folia Parasitol. 1983, 30:15-26.
13. Ergens R. Gyrodactylus bohemicus sp. n. (Monogenea: Gyrodactylidae) from Oncorhynchus mykiss (Walbaum) and Salvelinus fontinalis (Mitchill) (Clupeiformes: Salmonidae) in Czechoslovakia. Folia Parasitol. 1992, 39:391-394.
14. Ergens R., Yukhimenko S.S. Gyrodactylus somnaensis sp. n. (Monogenea: Gyrodactylidae), a new fish parasite from the basin of the River Amur. Folia Parasitol. 1990, 37:313-314.
15. FAO Cultured Aquatic Species Information Programme 2005, FAO Fisheries and Aquaculture Department, Rome.
16. Flores-Crespo J., Flores C.R. Principales tremátodos y céstodos de importancia económica en acuicultura. Tópicos de parasitología animal; céstodos y tremátodos. Universidad Autónoma del Estado de Morelos 1993, 13-36.
17. Freeman M.A., Ogawa K. Variation in the small subunit ribosomal DNA confirms that Udonella (Monogenea: Udonellidae) is a species-rich group. Int. J. Parasitol. 2010, 40:255-264.
18. Froese, R., Pauly, D., 2010. FishBase, Froese, R., Pauly, D. (Eds.) (), World Wide Web electronic publication. http://www.fishbase.org/.
19. García-Vásquez A., Hansen H., Christison K.W., Bron J.E., Shinn A.P. Description of three new species of Gyrodactylus Nordmann 1832 (Monogenea) from oreochromids (Oreochromis, Cichlidae). Acta Parasitol. 2011, 56:20-33.
20. García-Vásquez A., Hansen H., Christison K.W., Rubio-Godoy M., Bron J.E., Shinn A.P. Gyrodactylids (Gyrodactylidae Monogenea) infecting Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) (Cichlidae): a pan-global survey. Acta Parasitol. 2010, 55:215-229.
21. Gilmore S.R., Abbott C.L., Cone D.K. The placement of Gyrodactylus salmonis (Yin & Sproston) in the molecular phylogeny of studied members of the Gyrodactylus wageneri-group parasitizing salmonids. J. Fish Dis. 2010, 33:461-467.
22. Gläser H.J. Sechs neue Arten der Gyrodactylus-wageneri Gruppe (Monogenea, Gyrodactylidae) nebst Bemerkungen zur Präparation, Determination, Terminologie und Wirtsspezifität. Zool. Anz. 1974, 192:56-76.
23. Granath W.O., Gilbert M.A., Wyatt-Pescador E.J., Vincent E.R. Epizootiology of Myxobolus cerebralis, the causative agent of salmonid whirling disease in the Rock Creek drainage of West-Central Montana. J. Parasitol. 2007, 91:104-119.
24. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. 1999, 41:95-98.
25. Hanek G., Threlfall W. Monogenetic trematodes from Newfoundland Canada. 1. New species of the genus Gyrodactylus Nordmann, 1832. Can. J. Zool. 1969, 47:951-955.
26. Hathaway R.P., Herlevich J.C. Gyrodactylus stableri sp. n., with new host and locality records for species of Gyrodactylus. J. Parasitol. 1973, 59:801-802.
27. Hendrickson D.A., Espinoza Pérez H., Findley L.T., Forbes W., Tomelleri J.R., Mayden R.L., Nielsen J.L., Jensen B., Ruiz Campos G., Varela Romero A., van der Heiden A., Camarena F., García de León F.J. Mexican native trouts: a review of their history and current systematic and conservation status. Rev. Fish Biol. Fish. 2002, 12:273-316.
28. ISSG, 2010. Global Invasive Species Database (Invasive Species Specialist Group, ),World Wide Web electronic publication. http://www.issg.org/.
29. Johnsen B.O., Jensen A.J. The Gyrodactylus story in Norway. Aquaculture 1991, 98:289-302.
30. Karasev A.B., Mitenev V.K., Kalinina N.R. Parasite fauna of cage-reared rainbow trout Oncorhynchus mykiss (Walbaum): research in freshwater farms (Kola Peninsula Russia). Bull. Eur. Assoc. Fish Pathol. 1997, 17:177-179.
31. Koski P., Malmberg G. Occurrence of Gyrodactylus (Monogenea) on salmon and rainbow trout in fish farms in Northern Finland. Bull. Scan. Soc. Parasitol. 1995, 5:76-88.
32. Kuusela J., Zietara M.S., Lumme J. Description of three new European cryptic species of Gyrodactylus Nordmann, 1832 supported by nuclear and mitochondrial phylogenetic characterization. Acta Parasitol. 2008, 53:120-126.
33. Lautraite A., Blanc G., Thiery R., Daniel P., Vigneulle M. Gyrodactylids parasitizing salmonids in Brittany and Western Pyrenees water basins: Epidemiological features of infection and species composition. Bull. Fr. Pêche Piscic. 1999, 355:305-325.
34. López-Jiménez S. Estudio parasitológico de los peces de aguas dulces del estado de Tabasco. Gaceta Sigolfo Sistema de Investigación del Golfo de México 2001, 8-10.
35. Lux E. Gyrodactylus salaris-Parasitierung von Salmoniden, ein diagnostisch-taxonomisches Problem. Tagung der Fachgruppe " Fischkrankheiten" in Verbindung mit der EAFP/-deutsche Sektion European Association of Fish Pathologists. 1990, 87-98. Deutsche Veterinärmedizinische Gesellschaft e. V, Giessen. E.-M. Bernoth, R. Hoffmann (Eds.).
36. Malmberg G. Om förekomsten av Gyrodactylus på svenska fiskar. Särtryck ur Skrifter Utgivna av Södra Sveriges Fiskeriförening årsskrift 1957, 1956:19-76.
37. Malmberg G. The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda Monogenea). Ark. Zool. 1970, 23:1-235.
38. Malmberg G. Gyrodactylidae and Gyrodactylosis of Salmonidae. Bull. Fr. Pêche Piscic. 1993, 328:5-46.
39. Malmberg G., Collins C.M., Cunningham C.O., Jalali B.J. Gyrodactylus derjavinoides sp. nov. (Monogenea, Platyhelminthes) on Salmo trutta trutta L. and G. derjavini Mikailov, 1975 on S. t. caspius Kessler, two different species of Gyrodactylus - combined morphological and molecular investigations. Acta Parasitol. 2007, 52:89-103.
40. Mendoza-Franco E.F., Scholz T., Vivas-Rodríguez C., Vargas-Vázquez J. Monogeneans of freshwater fishes from cenotes (sinkholes) of the Yucatan Peninsula. Mexico. Folia Parastol. 1999, 46:267-273.
41. Mendoza-Palmero C.A., Sereno-Uribe A.L., Salgado-Maldonado G. Two new species of Gyrodactylus von Nordmann, 1832 (Monogenea: Gyrodactylidae) parasitizing Girardinichthys multiradiatus (Cyprinodontiformes: Goodeidae), an endemic freshwater fish from central Mexico. J. Parasitol. 2009, 95:315-318.
42. Mizelle J.D., Kritsky D.C. Studies on monogenetic trematodes XXXIII New species of Gyrodactylus and a key to the North American species. Trans. Am. Microscop. Soc. 1967, 86:390-401.
43. Morris D.J., Freeman M.A. Hyperparasitism has wide-ranging implications for studies on the invertebrate phase of myxosporean (Myxozoa) life cycles. Int. J. Parasitol. 2010, 40:357-359.
44. Ogawa K. A monogenean parasite Gyrodactylus masu sp. n. (Monogenea: Gyrodactylidae) of salmonid fish in Japan. Bull. Jap. Soc. Sci. Fish. 1986, 52:947-950.
45. Ogawa K. Monogenean parasites of freshwater fishes of Hokkaido. Sci. Rep. Hokk. Fish Hatch. 1994, 48:59-67.
46. Paladini G., Gustinelli A., Fioravanti M.L., Hansen H., Shinn A.P. The first report of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes, Monogenea) on Italian cultured stocks of rainbow trout (Oncorhynchus mykiss Walbaum). Vet. Parasitol. 2009, 165:290-297.
47. Pérez-Ponce de León G., Rosas-Valdez R., Aguilar-Aguilar R., Mendoza-Garfias B., Mendoza-Palmero C., García-Prieto L., Rojas-Sánchez A., Briosio-Aguilar R., Pérez-Rodríguez R., Domínguez-Domínguez O. Helminth parasites of freshwater fishes Nazas River basin, northern Mexico. Check List 2010, 6:26-35.
48. Pugachev O.N., Gerasev P.I., Gusev A.V., Ergens R., Khotenowsky I. Guide to Monogenoidea of freshwater fish of Palaeartic and Amur regions 2009, Ledizioni, p. 564.
49. Rokicka M., Lumme J., Zietara M.S. Identification of Gyrodactylus ectoparasites in Polish salmonid farms by PCR-RFLP of the nuclear ITS segment of ribosomal DNA (Monogenea Gyrodactylidae). Acta Parasitol. 2007, 52:185-195.
50. Rosas M.M. Peces dulce-acuícolas que se explotan comercialmente en México y datos sobre su cultivo 1976, Instituto Nacional de Pesca, México, D.F, 135 p.
51. Rubio-Godoy M., Paladini G., García-Vásquez A., Shinn A.P. Gyrodactylus jarocho sp. nov. and Gyrodactylus xalapensis sp. nov. (Platyhelminthes: Monogenea) from Mexican poeciliids (Teleostei: Cyprinodontiformes), with comments on the known gyrodactylid fauna infecting poeciliid fish. Zootaxa 2010, 2509:1-29.
52. Saitou N., Nei M. The Neighbour-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4:406-425.
53. Salgado-Maldonado G. Checklist of helminth parasites of freshwater fishes from Mexico. Zootaxa 2006, 1324:1-357.
54. Salgado-Maldonado G., Aguilar-Aguilar R., Cabañas-Carranza G., Soto-Galera E., Mendoza-Palmero C. Helminth parasites in freshwater fish from the Papaloapan river basin Mexico. Parasitol. Res. 2005, 96:69-89.
55. Salgado-Maldonado G., Cabañas-Carranza G., Soto-Galera E., Caspeta-Mandujano J.M., Moreno-Navarrete R.G., Sánchez-Nava P., Aguilar-Aguilar R. A checklist of helminth parasites of freshwater fishes from the Lerma-Santiago river basin Mexico. Comp. Parasitol. 2001, 68:204-218.
56. Sánchez-Nava P., Salgado-Maldonado G., Soto-Galera E., Cruz B.J. Helminth parasites of Girardinichthys multiradiatus (Pisces: Goodeidae) in the upper Lerma River sub-basin. Mexico. Parasitol. Res. 2004, 93:396-402.
57. Schulman S.S. New species of monogenetic trematodes on cyprinids (In Russian). Akad. Nauk SSSR. Rab. Gelmint. 1953, 75:778-780.
58. Shinn A.P., Hansen H., Olstad K., Bachmann L., Bakke T.A. The use of morphometric characters to discriminate specimens of laboratory-reared and wild populations of Gyrodactylus salaris and G. thymalli (Monogenea). Folia Parasitol. 2004, 51:239-252.
59. Shinn, A.P., Harris, P.D., Cable, J., Bakke, T.A., Paladini, G., Bron, J.E., 2011. GyroDb. (), World Wide Web electronic publication. http://www.gyrodb.net/.
60. Shinn A.P., Sommerville C., Gibson D.I. Distribution and characterization of species of Gyrodactylus Nordmann, 1832 (Monogenea) parasitizing salmonids in the UK, and their discrimination from G. salaris Malmberg, 1957. J. Nat. Hist. 1995, 29:1383-1402.
61. Swofford D.L. PAUP*Phylogenetic analysis using parsimony (*and other methods), v 4. 0 beta10 2002, Sinauer Associates, Sunderland, MA, USA.
62. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nuc. Acids Res. 1997, 24:4876-4882.
63. Wang Z.M., Wang B.Q., Li J.X., Wang X.J., Liu G., Wang X.J., Zhao E.Y. The experiment on the prevention and cure of the salmonid gyrodactylosis (Gyrodactylus lenoki). Chin. J. Fish. 1997, 10:28-37.
64. Wells P.R., Cone D.K. Experimental studies on the effect of Gyrodactylus colemanensis and G. salmonis (Monogenea) on the density of mucous cells in the epidermis of fry of Oncorhynchus mykiss. J. Fish Biol. 1990, 37:599-603.
65. Yin W.Y., Sproston N.G. Studies on the monogenetic trematodes of China. Sinensia 1948, 19:57-85.
66. You P., Yuan B., Yang J., Easy R., Dong Z., Cone D. Pathogenic infections of Gyrodactylus brachymystacis (Monogenea) on Oncorhynchus mykiss (Walbaum) at a fish farm in the Qinling Mountain region of China. J. Fish Dis. 2006, 29:313-316.
67. You P., MacMillan J., Cone D. Local patchiness of Gyrodactylus colemanensis and G. salmonis parasitizing salmonids in the South River watershed, Nova Scotia, Canada. Dis. Aquat. Org. 2011, 96:137-143.
68. Zietara M.S., Huyse T., Lumme J., Volckaert F.A. Deep divergence among subgenera of Gyrodactylus inferred from rDNA ITS region. Parasitology 2002, 124:39-52.