Inflammatory response of "pintado" to the infection of Nomimoscolex pertierrae (Eucestoda: Proteocephalidea)
Keywords:
inflammation, Pseudoplatystoma corruscans, cestode, histology, intraspecific variationAbstract
An infectious process characterized by piercing lesion promoted by Nomimoscolex pertierrae on the intestine wall of Pseudoplatystoma corruscans (Spix & Agassiz, 1829) was analyzed by histopathology. This pathology was observed during the parasitic fauna study of P. corruscans collected on the high Paraná River floodplain. Samples of 2 cm2 size from the infected and uninfected fishes have been submitted to the usual histopathologic procedure, with the samples colored with hematoxylin-eosin and observed under a microscope. Nomimoscolex pertierrae fixes itself on the intestinal epithelium through perforations, resulting on damages to the host`s intestinal epithelium, hemorrhage, lymphocytary infiltration and, on the worst observed case, tissue necrosis. These damages were observed on 2.5% of the collected fishes, and did not present any correlation (p>0.05) between the lesions gravity and the parasite abundance, what may be correlated to an intraspecific variability, which promoted higher parasite virulence.
References
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BRITTON, J.R.; PEGG, J.; BAKER, D.; WILLIAMS,C.F. 2012 Do lower feeding rates result in reduced growth of a cyprinid fish infected with the Asian tapeworm? Ecology of Freshwater Fish,21: 172í 175.
BULLOCK, W.L. 1963 Intestinal histology of some salmonid fishes with particular reference to the histopathology of acanthocephalan infections. Journal of Morpholology, 112: 23í 44.
CAMPOS, C.M.; FONSECA, V.L.; TAKEMOTO, R.M.; MORAES, F.R. 2008 Fauna parasitária de cachara Pseudoplatystoma fasciatum (Siluriforme: Pimelodidae) do rio Aquidauana, Pantanal Sul Mato-grossense, Brasil. Acta Scientiarum Biological Sciences, 30: 91-96.
CHAICHARN, A. e BULLOCK, W.L. 1967 The histopathology of acanthocephalan infections in suckers with observations on the intestinal histology of two species of catostomid fishes.Acta Zoologica, 48: 19í 42.
CHAMBRIER, A.; TAKEMOTO, R.M.; PAVANELLI, G.C. 2006 Nomimoscolex pertierrae n. sp.(Eucestoda: Proteocephalidea), a parasite of Pseudoplatystoma corruscans (Siluriformes: Pimelodidae) in Brazil and redescription of N. sudobim Woodland, 1935, a parasite of P.fasciatum. Systematic Parasitology, 64: 191í 202.
CURY, M.X. 1992 Cultivo de pintado e cachara.Revista Panorama da Aqüicultura, 2: 8-9.
DEZFULI, B.S. 1991 Histopathology in Leuciscus cephalus (Pisces: Cyprinidae) resulting from infection with Pomphorhynchus laevis (Acanthocephala). Parassitologia, 33: 137í 145.
DEZFULI, B.S.; ARRIGHI, S.; DOMENEGHINI, C.;BOSI, G. 2000 Immunohistochemical detection of neuromodulators in the intestine of Salmo trutta L. naturally infected with Cyathocephalus truncates Pallas (Cestoda). Journal of Fish Diseases,23: 265í 273.
DEZFULI, B.S.; LUI, A.; GIOVINAZZO, G.;BOLDRINI, P.; GIARI, L. 2009 Intestinal inflammatory response of powan Coregonus lavaretus (Pisces) to the presence of
acanthocephalan infections. Parasitology, 136:929-937.
DEZFULI, B.S.; LUI, A.; GIARI, L.; PIRONI, F.; MANERA, M.; LORENZONI, M.; NOGA, E.J.
2013 Piscidins in the intestine of European perch, Perca fluviatilis, naturally infected with an enteric worm. Fish and Shellfish Immunology, 35(5): 1539í 1546
EIRAS, J.C.; REGO, A.A.; PAVANELLI, G.C. 1986 Histopathology in Paulicea luetkeni (Pisces -Pimelodidae) resulting from infections with Megathylacus brooksi and Jauella glandicephalus (Cestoda - Proteocephalidae). Journal of Fish Biology, 28: 359-365.
EIRAS, J.C.; TAKEMOTO, R.M.; PAVANELLI, G.C. (ed.) 2006 Métodos de Estudo e Técnicas Laboratoriais em Parasitologia de Peixes. Maringá:EDUEM, 2ªed. 199p.
ESCH, G.W. e HUFFINES, W.J. 1973 Histopathology associated with endoparasitic helminths in bass.Journal of Parasitology, 59: 306-313.
GOMES, L.H.; AGUIAR, D.V.C.; HIPOLITO, M.;MARTINS, A.M.C.R.P.F.; CHAVES, A.C.P. 2008 Avaliação histológica do intestino médio, do fígado e do pí¢ncreas de girinos de rã-touro alimentados com rações comerciais formuladas com três níveis de proteína bruta. Brazilian Journal of Animal Sciences, 37: 2090-2096.
HAMERS, R.L.; STURENBERG, F.J.;TARASCHEWSKI, H. 1992 In vitro study of migratory and adherent responses of fish leucocytes to the eel pathogenic acanthocephalan Paratenuisentis ambiguus (Van Cleave, 1921) Bullock et Sammuel, 1975 (Eoacanthocephala: Tenuisentidae). Fish Shellfish Immunology, 2: 43í 51.
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IRSHADULLAH, M. e MUSTAFA, Y. 2012 Pathology induced by Pomporhynchus kashmiriensis (Acanthocephala) in the alimentary canal of naturally infected Chirruh snow trout, Schizothorax esocinus (Heckel). Helminthology, 49:11-15.
KHALIL, L.F.; JONES, A.; BRAY, R.A. 1994 Keys to the cestode parasites of vertebrates. Wallingford, Oxon, CAB International. 768p.
KUSMA, C.M. e FERREIRA, F.W. 2010 Mechanism of fish's transposition from a small hydroelectric system. Ciência Rural, 40: 89-94.
LACERDA, A.C.F.; TAKEMOTO, R.M.; TAVARESDIAS, M.; POULIN, R.; PAVANELLI, G.C. 2012 Comparative parasitism of the fish Plagioscion squamosissimus in native and invaded river basins. Journal of Parasitology, 98: 713í 717.
LE-CREN, E.D. 1951 The length-weight relationship and seasonal cycle in gonad weight and conditions in the perch Perca fluviatilis. Journal of Animal Ecology, 20: 201-211.
LIZAMA, M.A.P.; TAKEMOTO, R.M.; TAVARES, M.J. 2007 Relação parasito-hospedeiro em peixes de pisciculturas da região de Assis, Estado de São Paulo, Brasil. Acta Scientiarum. Biological Sciences, 29: 437-445.
MACHADO, M.H.; PAVANELLI, G.C.;TAKEMOTO, R.M. 1994 Influence of host’s sex
and size on endoparasitic infrapopulations of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the high Paraná river, Brazil. Revista Brasileira de Parasitologia Veterinária, 3:143-148.
MACHADO, M.H.; PAVANELLI, G.C.;TAKEMOTO, R.M. 1995 Influence of the type of
environment and the hydrological level variation in endoparasitic infrapopulations of
Pseudoplatystoma corruscans (Agassiz) and Schizodon borelli (Boulenger)(Osteichthyes) of the high Paraná River, Brazil. Revista Brasileira de Zoologia, 12: 961-976.
MACHADO, M.H.; PAVANELLI, G.C.;TAKEMOTO, R.M. 1996 Structure and diversity
of endoparasitic infracommunities and the trophic level of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the high Paraná River. Memórias do Instituto Oswaldo Cruz,91: 441-448.
MARTIN, L.B.; HAWLEY, D.M.; ARDIA, D.R. 2011 An introduction to ecological immunology.Functional Ecology, 25: 1-4.
MAYNARD-SMITH, J. 1972 On Evolution. Edinburgh University Press, Edinburgh, UK. 358p.
MCDONOUGH, J.M. e GLEASON, L.N. 1981 Histopathology in the rainbow darter,
Etheostoma caeruleum, resulting from infection with the acanthocephalans, Pomporhynchus bulbocolli and Acanthocephalus dirus. Journal of Parasitology, 67: 403-409.
MIRANDA, M.O.T. e RIBEIRO, L.P. 1997 Características zootécnicas do surubim
Pseudoplatystoma corruscans. In: MIRANDA,M.O.T. (ed.) Surubim. Belo Horizonte: IBAMA.p.43-56.
PAVANELLI, G.C. e REGO, A.A. 1992 Megathylacus travassoi sp. and Nomimoscolex sudobim Woodland, 1935 (Cestoda í Proteocephalidea) parasites of Pseudoplatystoma corruscans (Agassiz, 1829) (Siluriformes - Pimelodidae) from the
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RIBEIRO, L.P. e MIRANDA, M.O.T. 1997 Rendimentos de processamento do surubim
Pseudoplatystoma corruscans. In: MIRANDA,M.O.T. (Ed.). Surubim. Belo Horizonte: IBAMA.p.101-111.
ROBERTS, L.S.; JANOVY-JR, J.; SCHMIDT, P. 2004 Foundations of Parasitology. 7ª ed. McGraw-Hill Science/Engineering/Math, USA. 728p.
SATO, Y. e GODINHO, H.P. 2003 Migratory Fishes of the São Francisco River. In: CAROLSFELD, J.;HARVEY, B.; ROSS, C.; BAER, A. Migratory Fishes of South America. Biology, Fisheries and Conservation Status. IDRC/World Bank, Victoria.p.195-232.
SATO, Y.; CARDOSO, E.L.; SALLUM, W.B.; GODINHO, H.P. 1997 Indução experimental da desova do Surubim Pseudoplatystoma corruscans.In: MIRANDA, M.O.T. (ed.). Surubim. Belo Horizonte: IBAMA. p.69-79.
SCOTT, A.L. e GRIZZLE, J.M. 1979 Pathology of cyprinid fishes caused by Bothriocephalus gowkongensis Yea, 1955 (Cestoda: Pseudophyllidea). Journal of Fish Diseases, 2: 69í 73.
SEIXAS-FILHO, J.T.; HIPOLITO, M.; CARVALHO, V.F.; MARTINS, A.M.C.R.P.F.; SILVA, L.N.; CASTAGNA, A.A. 2008 Alterações histopatológicas em girinos de rã-touro
alimentados com rações comerciais de diferentes níveis protéicos. Brazilian Journal of Animal Sciences, 37: 2085-2089.
SHARKEY, K.A. 1992 Substance P and calcitonin gene-related peptide (CGRP) in gastrointestinal inflammation. Annals of New York Academy Sciences, 664: 425í 442.
SATO, Y. e GODINHO, H.P. 2003 Migratory Fishes of the São Francisco River. In: CAROLSFELD, J.; HARVEY, B.; ROSS, C.; BAER, A. Migratory Fishes of South America. Biology, Fisheries and Conservation Status. IDRC/World Bank, Victoria.p.195-232.
SATO, Y.; CARDOSO, E.L.; SALLUM, W.B.; GODINHO, H.P. 1997 Indução experimental da desova do Surubim Pseudoplatystoma corruscans. In: MIRANDA, M.O.T. (ed.). Surubim. Belo Horizonte: IBAMA. p.69-79.
SCOTT, A.L. e GRIZZLE, J.M. 1979 Pathology of cyprinid fishes caused by Bothriocephalus gowkongensis Yea, 1955 (Cestoda: Pseudophyllidea). Journal of Fish Diseases, 2: 69í 73.
SEIXAS-FILHO, J.T.; HIPOLITO, M.; CARVALHO,V.F.; MARTINS, A.M.C.R.P.F.; SILVA, L.N.;
CASTAGNA, A.A. 2008 Alterações histopatológicas em girinos de rã-touro alimentados com rações comerciais de diferentes níveis protéicos. Brazilian Journal of Animal Sciences, 37: 2085-2089.
SHARKEY, K.A. 1992 Substance P and calcitonin gene-related peptide (CGRP) in gastrointestinal inflammation. Annals of New York Academy Sciences, 664: 425í 442.
TARASCHEWSKI, H. 1989 Acanthocephalus anguillae in intra and extraintestinal positions in experimentally infected juveniles of gold fish and carp and in sticklebacks. Journal of Parasitology, 75: 108í 118.
TAVARES, M.P.O. 1997 O Surubim. In: MIRANDA,M.O.T. (ed.). Surubim. Belo Horizonte: IBAMA. p.9-25.
THOMPSON, J.N. 1989 Concepts of coevolution.Trends in Ecology and Evolution, 4: 179-183.
TOFT, C.A. e KARTER, A.J. 1990 Parasite-host coevolution. Trends in Ecology and Evolution, 5:326-329.
WANSTALL, S.T.; ROBOTHAM, P.W.J.; THOMAS, J.S. 1986 Pathological changes induced by Pomphorhynchus laevis Müller (Acanthocephala) in the gut of rainbow trout, Salmo gairdneri Richardson. Zeitschrift fur Parasitenkunde, 72:105í 114.
WANSTALL S.T.; THOMAS J.S.; ROBOTHAM R.W.J. 1988 The pathology caused by
Pomphorhynchus laevis Muller in the alimentary tract of the stone loach Noemacheilus barbatulus (L.). Journal of Fish Diseases, 11: 511- 523.
BRASIL-SATO, M.C. 2003 Parasitos de peixes da bacia do São Francisco. In:GODINHO, H.P. e GODINHO, A.L. Águas, peixes e pescadores do São Francisco das Minas Gerais (org.). PUC Minas, Belo Horizonte. p.149-165.
BRITSKI, H.A.; SATO, Y.; ROSA, A.B.S. 1984 Manual de identificação de peixes da região de Três Marias (com chave de identificação para peixes da bacia do rio São Francisco). CODEVASF, Brasília. 143p.
BRITTON, J.R.; PEGG, J.; BAKER, D.; WILLIAMS,C.F. 2012 Do lower feeding rates result in reduced growth of a cyprinid fish infected with the Asian tapeworm? Ecology of Freshwater Fish,21: 172í 175.
BULLOCK, W.L. 1963 Intestinal histology of some salmonid fishes with particular reference to the histopathology of acanthocephalan infections. Journal of Morpholology, 112: 23í 44.
CAMPOS, C.M.; FONSECA, V.L.; TAKEMOTO, R.M.; MORAES, F.R. 2008 Fauna parasitária de cachara Pseudoplatystoma fasciatum (Siluriforme: Pimelodidae) do rio Aquidauana, Pantanal Sul Mato-grossense, Brasil. Acta Scientiarum Biological Sciences, 30: 91-96.
CHAICHARN, A. e BULLOCK, W.L. 1967 The histopathology of acanthocephalan infections in suckers with observations on the intestinal histology of two species of catostomid fishes.Acta Zoologica, 48: 19í 42.
CHAMBRIER, A.; TAKEMOTO, R.M.; PAVANELLI, G.C. 2006 Nomimoscolex pertierrae n. sp.(Eucestoda: Proteocephalidea), a parasite of Pseudoplatystoma corruscans (Siluriformes: Pimelodidae) in Brazil and redescription of N. sudobim Woodland, 1935, a parasite of P.fasciatum. Systematic Parasitology, 64: 191í 202.
CURY, M.X. 1992 Cultivo de pintado e cachara.Revista Panorama da Aqüicultura, 2: 8-9.
DEZFULI, B.S. 1991 Histopathology in Leuciscus cephalus (Pisces: Cyprinidae) resulting from infection with Pomphorhynchus laevis (Acanthocephala). Parassitologia, 33: 137í 145.
DEZFULI, B.S.; ARRIGHI, S.; DOMENEGHINI, C.;BOSI, G. 2000 Immunohistochemical detection of neuromodulators in the intestine of Salmo trutta L. naturally infected with Cyathocephalus truncates Pallas (Cestoda). Journal of Fish Diseases,23: 265í 273.
DEZFULI, B.S.; LUI, A.; GIOVINAZZO, G.;BOLDRINI, P.; GIARI, L. 2009 Intestinal inflammatory response of powan Coregonus lavaretus (Pisces) to the presence of
acanthocephalan infections. Parasitology, 136:929-937.
DEZFULI, B.S.; LUI, A.; GIARI, L.; PIRONI, F.; MANERA, M.; LORENZONI, M.; NOGA, E.J.
2013 Piscidins in the intestine of European perch, Perca fluviatilis, naturally infected with an enteric worm. Fish and Shellfish Immunology, 35(5): 1539í 1546
EIRAS, J.C.; REGO, A.A.; PAVANELLI, G.C. 1986 Histopathology in Paulicea luetkeni (Pisces -Pimelodidae) resulting from infections with Megathylacus brooksi and Jauella glandicephalus (Cestoda - Proteocephalidae). Journal of Fish Biology, 28: 359-365.
EIRAS, J.C.; TAKEMOTO, R.M.; PAVANELLI, G.C. (ed.) 2006 Métodos de Estudo e Técnicas Laboratoriais em Parasitologia de Peixes. Maringá:EDUEM, 2ªed. 199p.
ESCH, G.W. e HUFFINES, W.J. 1973 Histopathology associated with endoparasitic helminths in bass.Journal of Parasitology, 59: 306-313.
GOMES, L.H.; AGUIAR, D.V.C.; HIPOLITO, M.;MARTINS, A.M.C.R.P.F.; CHAVES, A.C.P. 2008 Avaliação histológica do intestino médio, do fígado e do pí¢ncreas de girinos de rã-touro alimentados com rações comerciais formuladas com três níveis de proteína bruta. Brazilian Journal of Animal Sciences, 37: 2090-2096.
HAMERS, R.L.; STURENBERG, F.J.;TARASCHEWSKI, H. 1992 In vitro study of migratory and adherent responses of fish leucocytes to the eel pathogenic acanthocephalan Paratenuisentis ambiguus (Van Cleave, 1921) Bullock et Sammuel, 1975 (Eoacanthocephala: Tenuisentidae). Fish Shellfish Immunology, 2: 43í 51.
INOUE, L.; CECCARELLI, P.S.; SENHORINI, J.A. 2003 A larvicultura e a alevinagem do Pintado e do Cachara. Revista Panorama da Aquicultura, 74:13-21.
IRSHADULLAH, M. e MUSTAFA, Y. 2012 Pathology induced by Pomporhynchus kashmiriensis (Acanthocephala) in the alimentary canal of naturally infected Chirruh snow trout, Schizothorax esocinus (Heckel). Helminthology, 49:11-15.
KHALIL, L.F.; JONES, A.; BRAY, R.A. 1994 Keys to the cestode parasites of vertebrates. Wallingford, Oxon, CAB International. 768p.
KUSMA, C.M. e FERREIRA, F.W. 2010 Mechanism of fish's transposition from a small hydroelectric system. Ciência Rural, 40: 89-94.
LACERDA, A.C.F.; TAKEMOTO, R.M.; TAVARESDIAS, M.; POULIN, R.; PAVANELLI, G.C. 2012 Comparative parasitism of the fish Plagioscion squamosissimus in native and invaded river basins. Journal of Parasitology, 98: 713í 717.
LE-CREN, E.D. 1951 The length-weight relationship and seasonal cycle in gonad weight and conditions in the perch Perca fluviatilis. Journal of Animal Ecology, 20: 201-211.
LIZAMA, M.A.P.; TAKEMOTO, R.M.; TAVARES, M.J. 2007 Relação parasito-hospedeiro em peixes de pisciculturas da região de Assis, Estado de São Paulo, Brasil. Acta Scientiarum. Biological Sciences, 29: 437-445.
MACHADO, M.H.; PAVANELLI, G.C.;TAKEMOTO, R.M. 1994 Influence of host’s sex
and size on endoparasitic infrapopulations of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the high Paraná river, Brazil. Revista Brasileira de Parasitologia Veterinária, 3:143-148.
MACHADO, M.H.; PAVANELLI, G.C.;TAKEMOTO, R.M. 1995 Influence of the type of
environment and the hydrological level variation in endoparasitic infrapopulations of
Pseudoplatystoma corruscans (Agassiz) and Schizodon borelli (Boulenger)(Osteichthyes) of the high Paraná River, Brazil. Revista Brasileira de Zoologia, 12: 961-976.
MACHADO, M.H.; PAVANELLI, G.C.;TAKEMOTO, R.M. 1996 Structure and diversity
of endoparasitic infracommunities and the trophic level of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the high Paraná River. Memórias do Instituto Oswaldo Cruz,91: 441-448.
MARTIN, L.B.; HAWLEY, D.M.; ARDIA, D.R. 2011 An introduction to ecological immunology.Functional Ecology, 25: 1-4.
MAYNARD-SMITH, J. 1972 On Evolution. Edinburgh University Press, Edinburgh, UK. 358p.
MCDONOUGH, J.M. e GLEASON, L.N. 1981 Histopathology in the rainbow darter,
Etheostoma caeruleum, resulting from infection with the acanthocephalans, Pomporhynchus bulbocolli and Acanthocephalus dirus. Journal of Parasitology, 67: 403-409.
MIRANDA, M.O.T. e RIBEIRO, L.P. 1997 Características zootécnicas do surubim
Pseudoplatystoma corruscans. In: MIRANDA,M.O.T. (ed.) Surubim. Belo Horizonte: IBAMA.p.43-56.
PAVANELLI, G.C. e REGO, A.A. 1992 Megathylacus travassoi sp. and Nomimoscolex sudobim Woodland, 1935 (Cestoda í Proteocephalidea) parasites of Pseudoplatystoma corruscans (Agassiz, 1829) (Siluriformes - Pimelodidae) from the
Itaipu reservoir and Paraná river, Paraná state, Brazil. Memórias do Instituto Oswaldo Cruz, 87:191-195.
RIBEIRO, L.P. e MIRANDA, M.O.T. 1997 Rendimentos de processamento do surubim
Pseudoplatystoma corruscans. In: MIRANDA,M.O.T. (Ed.). Surubim. Belo Horizonte: IBAMA.p.101-111.
ROBERTS, L.S.; JANOVY-JR, J.; SCHMIDT, P. 2004 Foundations of Parasitology. 7ª ed. McGraw-Hill Science/Engineering/Math, USA. 728p.
SATO, Y. e GODINHO, H.P. 2003 Migratory Fishes of the São Francisco River. In: CAROLSFELD, J.;HARVEY, B.; ROSS, C.; BAER, A. Migratory Fishes of South America. Biology, Fisheries and Conservation Status. IDRC/World Bank, Victoria.p.195-232.
SATO, Y.; CARDOSO, E.L.; SALLUM, W.B.; GODINHO, H.P. 1997 Indução experimental da desova do Surubim Pseudoplatystoma corruscans.In: MIRANDA, M.O.T. (ed.). Surubim. Belo Horizonte: IBAMA. p.69-79.
SCOTT, A.L. e GRIZZLE, J.M. 1979 Pathology of cyprinid fishes caused by Bothriocephalus gowkongensis Yea, 1955 (Cestoda: Pseudophyllidea). Journal of Fish Diseases, 2: 69í 73.
SEIXAS-FILHO, J.T.; HIPOLITO, M.; CARVALHO, V.F.; MARTINS, A.M.C.R.P.F.; SILVA, L.N.; CASTAGNA, A.A. 2008 Alterações histopatológicas em girinos de rã-touro
alimentados com rações comerciais de diferentes níveis protéicos. Brazilian Journal of Animal Sciences, 37: 2085-2089.
SHARKEY, K.A. 1992 Substance P and calcitonin gene-related peptide (CGRP) in gastrointestinal inflammation. Annals of New York Academy Sciences, 664: 425í 442.
SATO, Y. e GODINHO, H.P. 2003 Migratory Fishes of the São Francisco River. In: CAROLSFELD, J.; HARVEY, B.; ROSS, C.; BAER, A. Migratory Fishes of South America. Biology, Fisheries and Conservation Status. IDRC/World Bank, Victoria.p.195-232.
SATO, Y.; CARDOSO, E.L.; SALLUM, W.B.; GODINHO, H.P. 1997 Indução experimental da desova do Surubim Pseudoplatystoma corruscans. In: MIRANDA, M.O.T. (ed.). Surubim. Belo Horizonte: IBAMA. p.69-79.
SCOTT, A.L. e GRIZZLE, J.M. 1979 Pathology of cyprinid fishes caused by Bothriocephalus gowkongensis Yea, 1955 (Cestoda: Pseudophyllidea). Journal of Fish Diseases, 2: 69í 73.
SEIXAS-FILHO, J.T.; HIPOLITO, M.; CARVALHO,V.F.; MARTINS, A.M.C.R.P.F.; SILVA, L.N.;
CASTAGNA, A.A. 2008 Alterações histopatológicas em girinos de rã-touro alimentados com rações comerciais de diferentes níveis protéicos. Brazilian Journal of Animal Sciences, 37: 2085-2089.
SHARKEY, K.A. 1992 Substance P and calcitonin gene-related peptide (CGRP) in gastrointestinal inflammation. Annals of New York Academy Sciences, 664: 425í 442.
TARASCHEWSKI, H. 1989 Acanthocephalus anguillae in intra and extraintestinal positions in experimentally infected juveniles of gold fish and carp and in sticklebacks. Journal of Parasitology, 75: 108í 118.
TAVARES, M.P.O. 1997 O Surubim. In: MIRANDA,M.O.T. (ed.). Surubim. Belo Horizonte: IBAMA. p.9-25.
THOMPSON, J.N. 1989 Concepts of coevolution.Trends in Ecology and Evolution, 4: 179-183.
TOFT, C.A. e KARTER, A.J. 1990 Parasite-host coevolution. Trends in Ecology and Evolution, 5:326-329.
WANSTALL, S.T.; ROBOTHAM, P.W.J.; THOMAS, J.S. 1986 Pathological changes induced by Pomphorhynchus laevis Müller (Acanthocephala) in the gut of rainbow trout, Salmo gairdneri Richardson. Zeitschrift fur Parasitenkunde, 72:105í 114.
WANSTALL S.T.; THOMAS J.S.; ROBOTHAM R.W.J. 1988 The pathology caused by
Pomphorhynchus laevis Muller in the alimentary tract of the stone loach Noemacheilus barbatulus (L.). Journal of Fish Diseases, 11: 511- 523.
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