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Current Knowledge of Small Flukes (Digenea: Heterophyidae) from South America

  • Santos, Claudia Portes (Laboratory of Evaluation and Promotion of Environmental Health, Oswaldo Cruz Institute) ;
  • Borges, Juliana Novo (Laboratory of Evaluation and Promotion of Environmental Health, Oswaldo Cruz Institute)
  • Received : 2020.03.31
  • Accepted : 2020.06.09
  • Published : 2020.08.31

Abstract

Fish-borne heterophyid trematodes are known to have a zoonotic potential, since at least 30 species are able to infect humans worldwide, with a global infection of around 7 million people. In this paper, a 'state-of-the-art' review of the South American heterophyid species is provided, including classical and molecular taxonomy, parasite ecology, host-parasite interaction studies and a list of species and their hosts. There is still a lack of information on human infections in South America with undetected or unreported infections probably due to the information shortage and little attention by physicians to these small intestinal flukes. Molecular tools for specific diagnoses of South American heterophyid species are still to be defined. Additional new sequences of Pygidiopsis macrostomum, Ascocotyle pindoramensis and Ascocotyle longa from Brazil are also provided.

Keywords

References

  1. Fried B, Graczyk TK, Tamang L. Food-borne intestinal trematodiases in humans. Parasitol Res 2004; 93: 159-170. https://doi.org/10.1007/s00436-004-1112-x
  2. Toledo R, Esteban JG, Fried B. Immunology and pathology of intestinal trematodes in their definitive hosts. Adv Parasitol 2006; 63: 285-365. https://doi.org/10.1016/S0065-308X(06)63004-2
  3. Simoes SBE, das Neves RFC, Santos CP. Life history of Acanthocollaritrema umbilicatum Travassos, Freitas and Buhrnheim, 1965 (Digenea: Cryptogonimidae). Parasitol Res 2008; 103: 523-528. https://doi.org/10.1007/s00436-008-1000-x
  4. Simoes SB, Barbosa HS, Santos CP. The life history of Pygidiopsis macrostomum Travassos, 1928 (Digenea: Heterophyidae). Mem Inst Oswaldo Cruz 2009; 104: 106-111. https://doi.org/10.1590/S0074-02762009000100016
  5. Ostrowski de Nunez M. Life history of Pygidiopsis crassus n. sp. (Trematoda, Digenea, Heterophyidae) in the Neotropical region. Mem Inst Oswaldo Cruz 1995; 90: 13-19. https://doi.org/10.1590/S0074-02761995000100005
  6. Ostrowski de Nunez, M. Life cycles of two new sibling species of Ascocotyle (Ascocotyle) (Digenea, Heterophyidae) in the Neotropical Region. Acta Parasitol 2001; 46: 119-129.
  7. Chai JY, Jung BK. Fishborne zoonotic heterophyid infections: an update. Food Waterborne Parasitol 2017; 8-9: 33-63. https://doi.org/10.1016/j.fawpar.2017.09.001
  8. Borges JN, Costa VS, Mantovani C, Barros E, Santos EGN, Mafra CL, Santos CP. Molecular characterization and confocal laser scanning microscopic study of Pygidiopsis macrostomum (Trematoda: Heterophyidae) parasites of guppies Poecilia vivipara. J Fish Dis 2017; 40: 191-203. https://doi.org/10.1111/jfd.12504
  9. Alda P, Bonel N, Panei CJ, Cazzaniga NJ, Martorelli SR. First molecular identification of Ascocotyle (Phagicola) longa in its first intermediate host the mud snail Heleobia australis. Acta Parasitol 2015; 60: 791-795.
  10. Thaekham U, Blair D, Nawa Y, Waikagul J. Families Opisthorchiidae and Heterophyidae: are they distinct? Parasitol Int 2012; 61: 90-93. https://doi.org/10.1016/j.parint.2011.06.004
  11. Skov J, Kania PW, Dalsgaard A, Jorgensen TR, Buchmann, K. Life cycle stages of heterophyid trematodes in Vietnamese freshwater fishes traced by molecular and morphometric methods. Vet Parasitol 2008; 160: 66-75. https://doi.org/10.1016/j.vetpar.2008.10.088
  12. Chai JY, Lee SH. Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int 2002; 51: 129-154. https://doi.org/10.1016/S1383-5769(02)00008-9
  13. Soganders-Bernal F, Lumsden RD. The generic status of the heterophyid trematodes of the Ascocotyle complex, including notes on the systematics and biology of Ascocotyle angrense Travassos, 1916. J Parasitol 1963; 49: 264-274. https://doi.org/10.2307/3275993
  14. Scholz T. Taxonomic study of Ascocotyle (Phagicola) longa Ransom, 1920 (Digenea: Heterophyidae) and related taxa. Syst Parasitol 1999; 43: 147-158. https://doi.org/10.1023/A:1006120500518
  15. Pearson J. Family Heterophyidae Leiper, 1909. In Bray RA, Gibson DI, Jones A eds, Keys to the Trematoda. Vol. 3. Wallingford, UK. CAB International. 2008, pp 113-141.
  16. Hernandez-Orts JS, Georgieva S, Landete DN, Scholz T. Heterophyid trematodes (Digenea) from penguins: a new species of Ascocotyle Looss, 1899, first description of metacercaria of Ascocotyle (A.) patagoniensis Hernandez-Orts, Montero, Crespo, Garcia, Raga and Aznar, 2012, and first molecular data. Int J Parasitol Parasites Wildl 2019; 8: 94-105. https://doi.org/10.1016/j.ijppaw.2018.12.008
  17. Martorelli SR, Lino A, Marcotegui P, Montes MM, Alda P, Panei CJ. Morphological and molecular identification of the fish-borne metacercaria of Ascocotyle (Phagicola) longa Ransom, 1920 in Mugil liza from Argentina. Vet Par 2012; 190: 599-603. https://doi.org/10.1016/j.vetpar.2012.07.002
  18. Galvan-Borja D, Olivero-Verbel J, Barrios-Garcia L. Occurrence of Ascocotyle (Phagicola) longa Ransom, 1920 (Digenea: Heterophyidae) in Mugil incilis from Cartagena Bay, Colombia. Vet Parasitol 2010; 168: 31-35. https://doi.org/10.1016/j.vetpar.2009.10.011
  19. WoRMS Editorial Board. World Register of Marine Species [Internet]; [cited 2020 May 21]. Available from: http://www.marinespecies.org at VLIZ. 2020.
  20. Integrated Taxonomic Information System (ITIS). On-line database [Internet]. Available from: https://www.itis.gov/.
  21. Muller R, Wakelin D. Worms and Human Diseases. 2nd ed. Wallingford, UK. CAB International. 2002, pp 300.
  22. Chai JY. Human Intestinal Flukes: from Discovery to Treatment and Control. Dordebrecht, The Netherlands. Springer. 2019, pp 1-167.
  23. Scholz T, Aguirre-Macedo ML, Salgado-Maldonado G. Trematodes of the family Heterophyidae (Digenea) in Mexico a review of species and new host and geographical records. J Nat Hist 2001; 35: 1733-1772. https://doi.org/10.1080/00222930152667087
  24. Simoes SB, Barbosa H, Santos, CP. The life cycle of Ascocotyle (Phagicola) longa (Digenea: Heterophyidae), a causative agent of fish-borne trematodosis. Acta Trop 2010; 113: 226-233. https://doi.org/10.1016/j.actatropica.2009.10.020
  25. Hung NM, Madsen H, Fried B. Global status of fish-borne zoonotic trematodiasis in humans. Acta Parasitol 2013; 58: 231-258.
  26. Santos CP, Lopes KC, Costa VS, Santos EGN. Fish-borne trematodosis: potential risk of infection by Ascocotyle (Phagicola) longa (Heterophyidae). Vet Parasitol 2013; 193: 302-306. https://doi.org/10.1016/j.vetpar.2012.12.011
  27. Montes MM, Marcotegui PS, Martorelli SR. Digeneos parasitos de juveniles de Mugil liza (Pisces: Mugilidae) en la Bahia de Samborombon, Argentina, con el reporte de metacercarias zoonoticas de Ascocotyle (Phagicola) longa. Rev Arg Parasitol 2013; 1: 97-124 (in Spanish).
  28. Montes MM, Martorelli SR. An ecological and comparative analysis of parasites in juvenile Mugil liza (Pisces, Mugilidae) from two sites in Samborombon bay, Argentina. Iheringia Ser Zool 2015; 105: 403-410 (in Spanish). https://doi.org/10.1590/1678-476620151054403410
  29. Carnevia D, Speranza G. Seasonal variations in parasites found in mullet (Mugil platanus Gunther, 1880) juveniles captured on the Uruguayan coast of the River Plate. Bull Eur Ass Fish Pathol 2003; 23: 245-249.
  30. Fernandez JB. Los parasitos de la lisa Mugil cephalus L., en Chile: sistematica y aspectos poblacionales (Perciformes: Mugilidae). Gayana Zool 1987; 51: 3-58.
  31. Carnevia D, Perretta A, Venzal JM, Castro O. Heleobia australis (Mollusca, Hydrobiidae) y Mugil platanus (Pisces, Mugilidae), primer y segundo hospedador intermediario de Ascocotyle (Phagicola) longa (Digenea, Heterophyidae) en Uruguay. Rev Bras Parasit Vet 2004; 13: 283 (in Spanish).
  32. Jara CA, Escalante H. Phagicola arnaldoi: identificacion de sus metacercarias obtenidas de Mugil cephalus. Hidrobios 1982; 6: 37-43.
  33. Ostrowski de Nunez M. Life-history studies of heterophyid trematodes in the Neotropical Region: Ascocotyle (Phagicola) diminuta (Stunkard & Haviland, 1924) and A. (P.) angrense Travassos, 1916. Syst Parasitol 1993; 24: 191-199. https://doi.org/10.1007/BF00010532
  34. Ostrowski de Nunez M. Life cycle of Ascocotyle (Phagicola) angeloi (Digenea: Heterophyidae) in the Neotropical Region. Folia Parasitol 1998; 45: 199-204.
  35. Ostrowski de Nunez M. Life history studies of heterophyid trematodes in the Neotropical region: Ascocotyle (Leighia) hadra sp.n. Mem Inst Oswaldo Cruz 1992; 87: 539-543. https://doi.org/10.1590/S0074-02761992000400012
  36. Ostrowski de Nunez M. Fauna de agua dulce en la Republica Argentina. IV. Las cercarias de Ascocotyle (A.) tenuicolis Price 1935 y de Pygidiopsis pindoramensis Travassos 1929 (Trematoda, Heterophyidae). Physis Sec B 1976; 35: 51-57.
  37. Travassos L. Deux nouvelles especes du genre Ascocotyle Looss, 1899. Comptes Rendues 1928; 100: 939-940.
  38. Odening K 1969. Exkretionssystem und systematische Stellung kubanischer Fledermaustrematoden. Bijdr Dierk 39: 45-62. https://doi.org/10.1163/26660644-03901004
  39. Zdzitowiecki K, Rutkowska MA. The helminthofauna of bats (Chiroptera) from Cuba. III. A review of trematodes. Acta Parasitol Polonica 1980; 26: 201-214.
  40. Simoes SBE, Barbosa HS, Santos CP. Redescription and surface ultrastructure of Pygidiopsis macrostomum (Digenea: Heterophyidae). J Parasitol 2005; 91: 931-936. https://doi.org/10.1645/GE-417R.1
  41. Ostrowski de Nunez M. Life history studies of heterophyid trematodes in the Neotropical Region: Pygidiopsis australis sp. n., a sibling species of P. pindoramensis Travassos, 1929. Acta Parasitol 1996; 41: 13-19.
  42. Alda P, Martorelli SR, Sarria R. Digenean parasites in the white-backed stilt Himantopus melanurus vieillot, 1817 (Recurvirostridae) from the Argentine Coast. Comp Parasitol 2011; 78: 217-219. https://doi.org/10.1654/4479.1
  43. Pinto HA, de Melo AL. Melanoides tuberculata (Mollusca: Thiaridae) as an intermediate host of Centrocestus formosanus (Trematoda: Heterophyidae) in Brazil. Rev Inst Med Trop Sao Paulo 2010; 52: 207-210. https://doi.org/10.1590/S0036-46652010000400008
  44. Pinto HA, Melo AL. Metacercariae of Centrocestus formosanus (Trematoda: Heterophyidae) in Australoheros facetus (Pisces: Cichlidae) in Brazil. Rev Bras Parasitol Vet 2012; 21: 334-337. https://doi.org/10.1590/S1984-29612012000300032
  45. Pinto HA, Goncalves NQ, Lopez-Hernandez D, Pulido-Murillo EA, Melo AL. The life cycle of a zoonotic parasite reassessed: Experimental infection of Melanoides tuberculata (Mollusca: Thiaridae) with Centrocestus formosanus (Trematoda: Heterophyidae). PLoS ONE 2018; 13: e0194161. https://doi.org/10.1371/journal.pone.0194161
  46. Bogea, T, Cordeiro FM, Gouveia JS. Melanoides tuberculatus (Gastropoda: Thiaridae) as intermediate host of Heterophyidae (Trematoda: Digenea) in Rio de Janeiro metropolitan area, Brazil. Rev Inst Med Trop Sao Paulo 2005; 47: 87-90. https://doi.org/10.1590/S0036-46652005000200005
  47. Santos EGN, Costa VS, Santos CP. Does the trematode Centrocestus formosanus affect the locomotory activity of the mollusc Melanoides tuberculatus? Parasit Vectors 2013; 6: 92-96. https://doi.org/10.1186/1756-3305-6-92
  48. Casalins LM, Arbetman MP, Viozzi GP, Flores VR. A new species of Cryptocotyle (Digenea: Heterophyidae) infecting kelp gull and a galaxiid fish in Patagonian freshwater environments: morphological and molecular analyses. J Parasitol 2020; 106: 203-210. https://doi.org/10.1645/18-44
  49. Velasquez LE, Bedoya JC, Areiza A, Velez I. First record of Centrocestus formosanus (Digenea: Heterophyidae) in Colombia. Rev Mex Biodivers 2006; 77: 119-121.
  50. Pullido-Murillo EA, Furtado LFV, Melo AL, Rabelo EML, Pinto HA. Fishborne zoonotic trematodes transmitted by Melanoides tuberculata snails, Peru. Emerg Infec Dis 2018; 24: 606-608. https://doi.org/10.3201/eid2403.172056
  51. Diaz MT, Hernandez LE, Gonzalez G. Studies on the life history of Centrocestus formosanus Nishigori, 1924 (Trematoda: Heterophyidae) in Venezuela. Parasitol Int 1998; 47: 300.
  52. McIntosh A. 1953. A new heterophyid trematode from a Brazilian otter. Thapar Commemoration Volume. University of Lucknow, Lucknow, India. 209-210.
  53. Gardner SL, Thew PT. Redescription of Cryptocotyle thapari McIntosh, 1953 (Trematoda: Heterophyidae), in the river otter Lutra longicaudis from Bolivia. Comp Parasitol 2006; 73: 20-23. https://doi.org/10.1654/0001.1
  54. Ostrowski de Nunez, M. Fishes as definitive or intermediate hosts of Opisthorchioid trematodes in South America. Wiad Parazytol 1999; 45: 329-336.
  55. Kreiter A, Semenas L. Helmintos parasitos de Larus dominicanus en la Patagonia Argentina. Bol Chil Parasitol 1997; 52: 39-42 (in Spanish).
  56. Tantalean M, Sarmiento L, Huiza A. Digeneos (Trematoda) del Peru. Bol Lima 1992; 80: 47-84.
  57. Travassos L. Contribuicao ao conhecimento dos Heterophyidae observados no Brasil. These Vet 1929; 1-31.
  58. Travassos L, Freitas JFT, Kohn A. Trematodeos do Brasil. Mem Inst Oswaldo Cruz 1969; 67: 1-886.
  59. Thatcher VE. Trematodeos Neotropicais. Manaus, Brazil. Instituto Nacional de Pesquisas da Amazonia. 1993, pp 1-553.
  60. Velez I. Some digested trematodes of Sula dactylatra (birds) in northern Colombia. Actual Biol 1980; 9: 3-11.
  61. Fischtal JH, Nasir P. Some digenetic trematodes from freshwater and marine fishes of Venezuela. Norweg J Zool 1974; 22: 71-80.
  62. Lutz A. Estudios sobre trematodes observados en Venezuela. Estudios de Zoologia y Parasitologia Venezoelanas 1928; 101-125.
  63. Diaz MT, Hernandez LE, Bashirullah AT. Studies on the life cycle of Haplorchis pumilio (Looss, 1896) (Trematoda: Heterophyidae) in Venezuela. Rev Cient 2008; 18: 35-42.
  64. Dzikowski R, Levy MG, Poore MF, Flowers JR, Paperna I. Use of rDNA polymorphism for identification of Heterophyidae infecting freshwater fishes. Dis Aquat Org 2004; 59: 35-41. https://doi.org/10.3354/dao059035
  65. Miller TL, Cribb TH. Two new cryptogonimid genera Beluesca n. gen. and Chelediadema n. gen. (Digenea: Cryptogonimidae) from tropical Indo-West Pacific Haemulidae (Perciformes). Zootaxa 2007; 1543: 45-60. https://doi.org/10.11646/zootaxa.1543.1.2
  66. Thaenkham U, Dekumyoy P, Komalamisra C, Sato M, Dung DT, Waikagul J. Systematics of the subfamily Haplorchiinae (Trematoda: Heterphyidae), based on nuclear ribosomal DNA genes and ITS2 region. Parasitol Int 2010; 59: 460-465. https://doi.org/10.1016/j.parint.2010.06.009
  67. Brusentsov II, Katokhin AV, Brusentsova IV, Shekhovtsov SV, Borovikov SN, Goncharenko GG, Lider LA, Romashov BV, Rusinek OT, Shibitov SK, Suleymanov MM, Yevtushenko AV, Mordvinov VA. Low genetic diversity in wide-spread Eurasian liver fluke Opisthorchis felineus suggests special demographic history of this trematode species. PLoS One 2013; 8: e62453. https://doi.org/10.1371/journal.pone.0062453
  68. Vanhove MP, Tessens B, Schoelinck C, Jondelius U, Littlewood DT, Artois T, Huyse T. Problematic barcoding in flatworms: a case-study on monogeneans and rhabdocoels (Platyhelminthes). ZooKeys 2013; 365: 355-379. https://doi.org/10.3897/zookeys.365.5776
  69. Besansky NJ, Severson DW, Ferding MT. DNA barcoding of parasites and invertebrate disease vectors: what you don't know can hurt you. Trends Parasitol 2003; 19: 545-546. https://doi.org/10.1016/j.pt.2003.09.015
  70. Santos EGN, Santos CP. Parasite-induced and parasite development-dependent alteration of the swimming behavior of fish hosts. Acta Trop 2013; 127: 56-62. https://doi.org/10.1016/j.actatropica.2013.03.008
  71. Lopes KC, Ferrao Filho AS, Santos EGN, Cunha RA, Santos CP. Effects of crude extracts of a saxitoxin-producer strain of the cyanobacterium Cylindrospermopsis raciborskii on the swimming behavior of wild and laboratory reared guppy Poecilia vivipara. Toxicon 2017; 129: 44-51. https://doi.org/10.1016/j.toxicon.2017.02.002
  72. Lopes KC, Ferrao-Filho AS, Santos EGN, Santos CP. First report of neurotoxic effect of the cyanobacterium Cylindrospermopsis raciborskii on the motility of trematode metacercariae. J Helminthol 2018; 92: 244-249. https://doi.org/10.1017/S0022149X17000281
  73. Carnevia D, Castro O, Perretta A, Venzal JM. Identificacion en Uruguay de metacercarias de Ascocotyle (Phagicola) longa Digenea: Heterophyidae parasitando lisas, Mugil platanus Pisces: Mugilidae y evaluacion del riesgo de zoonosis y afecciones en mascotas. Veterinaria (Montevideo) 2005; 40: 19-23.
  74. Armas de Conroy G. Investigaciones sobre la fagicolosis en lisas (Mugilidae) de aguas americanas. I. Estudios taxonomicos de Phagicola sp. (Trematoda: Heterophyidae) en mugilidos sudamericanos. Rev Iber Parasitol 1986; 46: 39-46.
  75. Almeida-Dias ER, Woiciechovski, E. Ocorrencia da Phagicola longa (Trematoda: Heterophyidae) em mugilideos e no homem. Registro e Cananeia, SP. Hig Alim 1994; 8: 43-46.
  76. Citti AL, Ribeiro NAS, Telles EO, Balian SC. Ascocotyle (Phagicola) longa parasitando tainhas (Mugil liza, Valenciennes, 1836) em Sao Paulo: ocorrencia, importancia na saude publica e estrategias de controle. Rev Ed Cont Med Vet Zoot CRMV-SP 2014; 12: 36-43.
  77. Barros LA, Arruda VS, Gomes DC, Magalhaes R. First natural infection by Ascocotyle (Phagicola) longa Ransom (Digenea, Heterophyidae) in an avian host, Ardea cocoa L. (Aves, Ciconiformes, Ardeidae) in Brazil. Rev Bras Zool 2002; 19: 151-155. https://doi.org/10.1590/S0101-81752002000600014
  78. Brandao M, Luque JL, Scholz T, Kostadinova A. New records and descriptions of digeneans from the Magellanic penguin Spheniscus magellanicus (Forster) (Aves: Sphenisciformes) on the coast of Brazil. Syst Parasitol 2013, 85: 79-98. https://doi.org/10.1007/s11230-013-9410-2
  79. Jordan HE, Maples WP. Third record of Phagicola longa (Ransom, 1920) (Trematoda: Heterophyidae) in dogs from the United States. J Parasitol 1966; 52: 362-363. https://doi.org/10.2307/3276500
  80. Mello EBF, Carvalho Mauge G, Campos MS, Rocha UF, Dell'Porto A. Distribuicao de helmintos do genero Ascocotyle Looss, 1899 (Trematoda Fascioloidea Heterophyidae - Ascocotylinae) no tubo gastrointestinal de cao. Rev Fac Med Vet Univ Sao Paulo 1977; 14: 239-242. https://doi.org/10.11606/issn.2318-3659.v14i2p239-242
  81. Manfredi MT, Oneto M. Phagicola longa (Heterophyidae) in dogs in Chile: morfological findings and taxonomical problems. Parasitologia 1997; 39: 9-11.
  82. Costa HMA, Lima WS, Costa JO. Phagicola arnaldoi (Travassos, 1928) Travassos, 1929 (Trematoda, Heterophyidae) em Canis familiaris. Arq Bras Med Vet Zootec 1988; 36: 591-595.
  83. Costa JO, Guimaraes MP, Lima WS, Lima EA. Frequencia de endo e ectoparasitos de caes capturados nas ruas de Vitoria, ES, Brasil. Arq Bras Med Vet Zootec 1990; 42: 451-452.
  84. Freitas JT, Ibanez N, Cordova E. Ocurrencia de Phagicola arnaldoi en perros de Arequipa, Peru. Rev Per Med Trop 1972; 1: 55-57.
  85. Chieffi PP, Leite OH, Dias RM, Torres DM, Mangini AC. Human parasitism by Phagicola sp. (Trematoda-Heterophyidae) in Cananeia, Sao Paulo State, Brazil. Rev Inst Med Trop Sao Paulo 1990; 32: 285-288. https://doi.org/10.1590/S0036-46651990000400008
  86. Chieffi PP, Gorla MC, Torres DM, Dias RM, Mangini AC, Monteiro AV, Woiciechovski E. Human infection by Phagicola sp. (Trematoda, Heterophyidae) in the municipality of Registro, Sao Paulo State, Brazil. J Trop Med Hyg 1992; 95: 346-348.
  87. Antunes SA, Almeida-Dias ER. Phagicola longa (Trematoda: Heterophyidae) em mugili'deos estocados resfriados e seu consumo cru em Sao Paulo, SP. Hig Alim 1994; 8: 41-42.
  88. Knoff M, Luque JL, Amato JF. Community ecology of the metazoan parasites of grey mullets, Mugil platanus (Osteichthyes: Mugilidae) from the Littoral of the State of Rio de Janeiro, Brazil. Rev Bras Biol 1997; 57: 441-454.
  89. Conceicao JCS, Sao Clemente SC, Matos E. Ocorrencia de Phagicola longus (Ransom, 1920) Price, 1932 em tainhas (Mugil sp.) comercializadas em Belem, Estado do Para. Rev Bras Cienc Agr 2000; 33: 97-101.
  90. Oliveira SA, Blazquez FJH, Antunes SA, Maia AAM. Metacercarias de Ascocotyle (Phagicola) longa Ransom, 1920 (Digenea: Heterophyidae), em Mugil platanus, no estuario de Cananeia, SP, Brasil. Cienc Rural 2007; 37: 1056-1059. https://doi.org/10.1590/S0103-84782007000400022
  91. Gueretz JS, Moura AB, Martins ML, Souza AP. Estudo da prevalencia de Ascocotyle (Phagicola) longa em mugilideos capturados na Baia da Babitonga, Santa Catarina, Brasil. Arch Vet Sci 2019; 24: 79-87.
  92. Brasil Ministerio da Saude (2010) Classificacao de risco dos agentes biologicos. 2. ed. Serie A. Normas e Manuais Tecnicos [Internet]; [cited 2019 Oct 9]. Available from: http://bvsms.saude.gov.br/bvs/publicacoes/classificacao_risco_agentes_biologicos_2ed.pdf.
  93. Coelho MRT, Sao Clemente SC, Gottshalk S. Acao de diferentes metodos de conservacao na sobrevivencia de metacercarias de Phagicola longus (Ranson, 1920) Price, 1932, parasito de mugilideos capturados no litoral do Estado do Rio de Janeiro. Hig Alim 1997; 11: 39-42.
  94. Rodrigues MV, Perez ACA, Machado TM, Orisaka FM, Kurissio JK, Lafisca A. Research of Ascocotyle (Phagicola) longa in heat treated fillets of mullets (Mugil platanus). Fish Aquac J 2015; 6: 115.
  95. Borges JN, Lopes KC, Santos CP. Viability of Ascocotyle (Phagicola) longa (Trematoda: Heterophyidae) metacercariae from mullets (Mugil liza) from Rio de Janeiro, Brazil after exposure to freezing and heating in the temperature range from $-35^{\circ}C$ to $180^{\circ}C$. Food Control 2018; 89: 117-122. https://doi.org/10.1016/j.foodcont.2017.11.037
  96. Ostrowski de Nunez M. Estudio sobre estadios larvales de trematodes Digeneos de peces Cyprinodontiformes. Physis 1974; 33: 45-61.
  97. Drago FB, Lunaschi LI. Update of checklist of digenean parasites of wild birds from Argentina, with comments about the extent of their inventory. Neotrop Helminthol 2015; 9: 325-350.
  98. Boero JJ, Led JE, Brandetti E. Algunos parasitos de la avifauna Argentina. Analecta Vet 1972; 4:17-34.
  99. Alda P, Martorelli SR. Trematodes infecting the South-American intertidal mud snail Heleobia australis (Rissooidea: Cochliopidae). Acta Parasitol 2014; 59: 50-67.
  100. Lunaschi LI, Cremonte F, Drago FB. Checklist of digenean parasites of birds from Argentina. Zootaxa 2007; 1403: 1-36. https://doi.org/10.11646/zootaxa.1403.1.1
  101. Arruda VS, Muniz-Pereira LC, Pinto RM. Ascocotyle (Phagicola) rara sp. n. (Digenea, Heterophyidae) from Ixobrychus exilis (Aves, Ardeidae) in Brazil. Rev Bras Zool 2002; 19: 145-149. https://doi.org/10.1590/S0101-81752002000100012
  102. Arruda VS, Pinto RM, Muniz-Pereira LC. New host and geographical records for helminths parasites of Ardeidae (Aves, Ciconiiformes) in Brazil. Rev Brasil Zool 2001: 18: 225-232.
  103. McNeil R, Diaz MT, Casanova B, Villeneuve A, Thibault M. Trematode infestation as a factor in shorebird oversummering: a case study of the greater yellowlegs (Tringa melanoleuca). Bull Scand Soc Parasitol 1996; 6: 114-117.
  104. Mcneil R, Diaz MT, Casanova B, Villeneuve A. Trematode parasitism as a possible factor in over-summering of greater yellowlegs (Tringa melanoleuca). Ornitol Neotrop 1995; 6: 57-65.
  105. Digiani MC. Digeneans and cestodes parasitic in the white-faced ibis Plegadis chihi (Aves: Threskiornithidae) from Argentina. Folia Parasitol 2000; 47: 195-204. https://doi.org/10.14411/fp.2000.037
  106. Perez ACA, Machado TM, Lopes RG, Okumura MPM, Rodrigues MV, Correa AM, Montano AP, Sao Clemente SC Aspectos parasitologicos do pescado comercializado na costa da mata atlantica. Hig Alimentar 2012; 26: 120-124.
  107. Carrera-Jativa PD, Rodriguez-Hidalgo R, Sevilla C, Jimenez-Uzcategui G, Boero JJ, Led JE, Brandetti E. Gastrointestinal parasites in the Galapagos penguin Spheniscus mendiculus and the flightless cormorant Phalacrocorax harrisi in the Galapagos Islands. Mar Ornithol 2014; 42: 77-80.
  108. Pinto HA, Mati VLT, Melo AL. Metacercarial infection of wild Nile tilapia (Oreochromis niloticus) from Brazil. Sci World J 2014; 2014: 80749.
  109. Lizama MAP, Takemoto RM, Pavanelli GC. Ecological aspects of metazoan parasites of Astyanax altiparanae Garutti e Britski, 2000 (Characidae) of the upper Parana River floodplain, Brazil. Bol Insti Pesca 2008; 34: 527-533.
  110. Torres P, Hott A, Boehmwald H. Protozoa, helminths and arthropods in cats of Valdivia City and their importance to man. Arch Med Vet 1972; 4: 20-29.
  111. Pinto HA, Mati VLT, Melo AL. New records and a checklist of trematodes from Butorides striata (Aves: Ardeidae). Rev Mex Biodivers 2013; 84: 1100-1110. https://doi.org/10.7550/rmb.34431
  112. Gonzalez-Acuna D, Lohse E. Parasites of the American Kestrel (Falco sparverius) in South-central Chile. J Raptor Res 2011; 45: 188-193. https://doi.org/10.3356/JRR-10-68.1
  113. Moreno L, Gonzalez-Acuna D. Los parasitos de las aves rapaces de Chile: una revision. Bol Chil Ornitol 2015; 2: 93-102.
  114. Gonzalez-Acuna D, Cerda F, Lopez J, Ortega R, Mathieu C, Kinsella M. Checklist of the helminths of the kelp gull, Larus dominicanus (Aves: Laridae), with new records from Chile. Zootaxa 2009; 2297: 27-43. https://doi.org/10.11646/zootaxa.2297.1.3
  115. Brandao ML, Moreira J, Luque JL. Checklist of Platyhelminthes, Acanthocephala, Nematoda and Arthropoda parasitizing penguins of the world. Check List 2014; 10: 562-573. https://doi.org/10.15560/10.3.562
  116. Drago FB. Community structure of metazoan parasites of silverside, Odontesthes bonariensis (Pisces, Atherinopsidae) from Argentina. Iheringia Ser Zool 2012; 102: 26-32. https://doi.org/10.1590/S0073-47212012000100004
  117. Santos CP, Simoes SBE, Barbosa HS, Scholz T. Redescription of Ascocotyle (Ascocotyle) felippei Travassos, 1928 (Digenea: Heterophiydae) with new synonymies. J Parasitol 2007; 93: 1468-1475. https://doi.org/10.1645/GE-1212.1
  118. Zdzitowiecki K, Niewiadomska K, Drozdz J. Trematodes of birds and mammals in the environs of H. Arctowski Station (South Shetlands, Antarctic). Acta Parasitol 1989; 34: 247-257.
  119. Lunaschi LI, Cremonte F, Drago F. Checklist of digenean parasites of birds from Argentina. Zootaxa 2007; 1403: 1-36. https://doi.org/10.11646/zootaxa.1403.1.1
  120. Diaz MT, Gomez E, Bashiryllah AK, Guilarte DV. Ascocotyle nana Ransom, 1920 (Trematoda: Heterophyidae) from Venezuela and notes on its life cycle. Saber 2017; 29: 788-793.
  121. Boero JJ, Led JE. El parasitismo de la fauna autoctona. III. Los parasitos de las aves argentinas. Rev Fac C Vet, La Plata 1968; 10: 97-129.
  122. Boero JJ, Led JE, Brandetti E. El parasitismo de la fauna autoctona. Rev Fac Agro Vet, Buenos Aires 1972; 1: 17-29.
  123. Drago FB, Lunaschi LI. Digenean parasites of ciconiiform birds from Argentina. Rev Mex Biodivers 2011; 82: 77-83.
  124. Torres P, Schlatter R, Montefusco A, Gesche W, Ruiz E, Contreras A. Helminth parasites of piscivorous birds from lakes in the south of Chile. Mem Inst Oswaldo Cruz 1993; 88: 341-343. https://doi.org/10.1590/S0074-02761993000200028
  125. Travassos L. Sur une nouvelle espece du genre Pygidiopsis, Pygidiopsis pindoramensis n. sp. (Trematoda). Compt Rend Soc Bresil Biol (Paris)1928; 100: 956-957.
  126. Travassos, L. Revisao do genero Ascocotyle Looss, 1899. Mem Inst Oswaldo Cruz 1930; 23: 61-97. https://doi.org/10.1590/S0074-02761930000200001
  127. Rietschl G, Werding B. Trematodes of birds from northern Columbia. Z Parasitenkd 1978; 57: 57-82. https://doi.org/10.1007/BF00927629
  128. Ortubay SG, Semenas LG, Ubeda CA, Quaggiotto AE, Viozzi GP. Catalogo de peces dulceacuicolas de la Patagonia Argentina y sus parasitos metazoos. Rio Negro, Argentina. Direccion de Pesca. 1994, pp 1-110 (in Spanish).
  129. Coelho MRT, Sao Clemente SC, Gottshalk S. Acao de diferentes metodos de conservacao na sobrevivencia de metacercarias de Phagicola longus (Ransom, 1920) Price, 1932, a parasite of mullet caught on the coast of the state of Rio de Janeiro. Revista Higiene Alimentar 1997; 11: 39-42.
  130. Torres P, Hott A, Boehmwald H. Protozoos, helmintos y artropodos en gatos de la ciudad de Valdivia y su importancia para el hombre. Arch Med Vet 1972; 4: 20-29.
  131. Torres P, Ramos M, Carrasco L, Neuman M, Franjola R, Navarrete N, Figueroa L. Protozoos helmintos y artropodos parasitos del perro domestico en la ciudad de Valdivia, Chile. Bol Chil Parasitol 1974; 29: 18-23 (in Spanish).
  132. Oberg C, Franjola R, Leyan V. 1979. Helmintos del perro domestico Canis familiaris en la ciudad de Valdivia, Chile. Bol Chil Parasitol 1979; 34: 21-26 (in Spanish).
  133. Bargiela JF. Los parasitos de la lisa Mugil cephalus L., en Chile: sistematica y aspectos poblacionales (Perciformes: Mugilidae). Gayaiia Zool 1987; 51: 3-58.
  134. Nasir P, Lemus de Guevara D, Diaz MT. Estudio sobre larvas de trematodos de agua dulce. XXIV. Ciclo vital parcial de Ascocotyle paratenuicollis sp. n. (Trematoda: Digenea). Acta Biol Venez 1970; 7: 1-4.
  135. Nasir P, Diaz MT. Studies on freshwater larval trematodes. XXVII. Partial life cycle of Caiguiria anterouteria gen. n., sp. n. (Trematoda: Digenea). Proc Helm Soc Wash 1971; 38: 21-23.
  136. Carnevia D, Mazzoni RA A preliminary note on the parasitofauna of the lebranche mullet (Mugil liza, Val 1836) in Uruguay. Riv Ital Piscic Ittiop 1986; 21: 109-111.
  137. Morgades D, Katz H, Castro O, Capellino D, Casas L, Benitez G, Venzal J, Morana A. Fauna Parasitaria del Lobo Fino (Arctocephalus australis) y del Leon Marino (Otaria flavescens) (Mammalia, Otariidae) en la costa de Uruguay. In Menafra R, Rodriguez-Gallego L, Scarabino F, Conde D eds, Bases para la conservacion y el manejo de la Costa Uruguaya. Montevideo, Uruguay. Vida Silvestre Uruguay. 2006, pp 89-96.
  138. Pereira EM, Muller G, Secchi E, Pereira Jr J, Valente ALS. Digenetic trematodes in South American sea lions from southern Brazilian waters. J Parasitol 2013; 99: 910-913. https://doi.org/10.1645/GE-3216.1
  139. Conroy D, Cecarelli P, Almeida ER. Diseases and parasites detected in grey mullet (Mugiliidae) from coastal waters of Sao Paulo State, Brazil. 3 Juvenile silver mullet (Mugil curema Val., 1836) and lebranche mullet (Mugil liza Val., 1836). Riv Ital Piscic Ittiop 1986; 21: 153-156.
  140. Antunes SA, Almeida Dias ER. Phagicola longa (Trematoda: Heterophyidae) em mugilideos estocados resfriados e seu consumo cru em Sao Paulo, SP. Hig Alimentar 1994; 8: 41.
  141. Barros L, Amato S. Experimental infection of dogs with metacercariae of Phagicola longa (Ransom, 1920) Price, 1932. Rev Bras Paras Vet 1996; 5: 61-64.
  142. Conroy D, Perez K. A report on the experimental infection of a smooth-headed capuchin monkey (Cebus apella) with metacercariae of Phagicola longa obtained from silver mullet (Mugil curema) viscera. Riv Ital Piscic Ittiop 1985; 20: 154-155.
  143. Pozza A, Lima F, Haas ML, Lehmann Albornoz PC. Clinostomum sp. (Digenea: Clinostomidae) and Ascocotyle sp. (Digenea: Heterophyidae): metacercariae with zoonotic potential in fishes from Tramandai River basin, southern Brazil. Bol Inst Pesca 2018, 44: 105-109. https://doi.org/10.20950/1678-2305.2018.303
  144. Yamada FH, Takemoto R, Pavanelli GC. Ecological aspects of ectoparasites from the gills of Satanoperca pappaterra (Heckel, 1840) (Cichlidae) from the upper Parana River floodplain, Brazil. Acta Sci Biol Sci 2007; 29: 331-336.
  145. Camargo AA, Pedro NHO, Pelegrini LS, Azevedo RK, Silva RJ, Abdallah VD. Parasites of Acestrorhynchus lacustris (Lutken, 1875) (Characiformes: Acestrorhynchidae) collected from the Peixe River, southeast Brazil. Acta Sci Biol Sci 2015; 37: 231-237. https://doi.org/10.4025/actascibiolsci.v37i2.24303
  146. Yamada FH, Santos LN, Takemoto RM. Gill ectoparasite assemblages of two non-native Cichla populations (Perciformes, Cichlidae) in Brazilian reservoirs. J Helminthol 2011; 85: 185-191. https://doi.org/10.1017/S0022149X10000441
  147. Hernandez-Orts, JS, Montero FE, Juan-Garcia A, Garcia NA, Crespo EA, Raga JA, Aznar FJ. Intestinal helminth fauna of the South American sea lion Otaria flavescens and fur seal Arctocephalus australis from northern Patagonia, Argentina. J Helminthol 2013; 87: 336-347. https://doi.org/10.1017/S0022149X12000454
  148. Hernandez-Orts JS, Montero FE, Crespo EA, Garcia NA, Raga JA, Aznar FJ. A new species of Ascocotyle (Trematoda: Heterophyidae) from the South American sea lion, Otaria flavescens, off Patagonia, Argentina. J Parasitol 2012; 98: 810-816. https://doi.org/10.1645/GE-2959.1
  149. Simoes SBE, Scholz T, Barbosa HS, Santos CP. Taxonomic status, redescription, and surface ultrastructure of Ascocotyle (Phagicola) pindoramensis n. comb. (Digenea: Heterophyidae). J Parasitol 2006; 92: 501-508. https://doi.org/10.1645/GE-757R.1
  150. Scholz T, Muniz-Pereira LC, Santos CP. Taxonomic status of Ascocotyle (Phagicola) rara Arruda, Muniz-Pereira et Pinto, 2002 (Digenea: Heterophyidae). Folia Parasitol 2006; 53: 297-301. https://doi.org/10.14411/fp.2006.036

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