Influence of the type of environment and of the hydrological level variation in endoparasitic infrapopulations of Pseudoplatystoma corruscans (Agassiz) and Schizodon borelli (Boulenger) (Osteichthyes) of the high Paraná River, Brazil

Machado, Marion H; Pavanelli, Gilberto C; Takemoto, Ricardo M

doi:10.1590/S0101-81751995000400023

Abstract

One hundred and ten specimens of Pseudoplatystoma corruscans (Agassiz, 1829) (Pimelodidae), "pintado", and 582 specimens of Schizodon borelli (Boulenger, 1900) (Anostomidae), "piava", collected in the floodplain of the high Paraná River were analyzed. P. corruscans presented 74.54% of parasitism while S. borelli presented 19.42%. Results of the present research show that in the case of P. corruscans, two species of proteocephalideans presented a significant relationship with the type of environment with regard to prevalence. Spasskyelina spinulifera (Woodland, 1935) was the only species that presented a relationship between the intensity of infection and the environment. In S. borelli only Cucullanus pinnai Travassos. Artigas & Pereira, 1928 presented a relationship with the environment. In this case the mean intensity was greater in lentic environments. The high values of the similarity index in the three environments studied indicate a considerable homogeneity of the endohelminths' species with regard to P. corruscans and S. borelli. This is probably due to what occurs with environments during the high water period when they are interlinked. The hydrological level was a less influential variable in endoparasitic infrapopulations of the hosts studied. In P. corruscans only three species, S. spinulifera, Nomimoscolex sudobim Woodland, 1934 and Megatnylacus travassosi Pavanelli & Rego, 1992 presented higher mean intensities in the high water period. This fact was also observed in the case of C. pinnai in S. borelli.

Ecology; endohelminths; freshwater fish; environment

Influence of the type of environment and of the hydrological level variation in endoparasitic infrapopulations of Pseudoplatystoma corruscans (Agassiz) and Schizodon borelli (Boulenger) (Osteichthyes) of the high Paraná River, Brazil

Marion H. Machado^I; Gilberto C. Pavanelli^II; Ricardo M. Takemoto^III

^IDepartamento de Biologia, NUPÉLIA, Universidade Estadual de Maringá. Av. Colombo 5790, 87020-900 Maringá, Paraná, Brasil

^IIPesquisador do CNPq

^IIIUniversidade Federal de São Carlos. Via Washington Luiz km 235, Caixa Postal 676, 13565-905 São Carlos, São Paulo, Brasil

ABSTRACT

One hundred and ten specimens of Pseudoplatystoma corruscans (Agassiz, 1829) (Pimelodidae), "pintado", and 582 specimens of Schizodon borelli (Boulenger, 1900) (Anostomidae), "piava", collected in the floodplain of the high Paraná River were analyzed. P. corruscans presented 74.54% of parasitism while S. borelli presented 19.42%. Results of the present research show that in the case of P. corruscans, two species of proteocephalideans presented a significant relationship with the type of environment with regard to prevalence. Spasskyelina spinulifera (Woodland, 1935) was the only species that presented a relationship between the intensity of infection and the environment. In S. borelli only Cucullanus pinnai Travassos. Artigas & Pereira, 1928 presented a relationship with the environment. In this case the mean intensity was greater in lentic environments. The high values of the similarity index in the three environments studied indicate a considerable homogeneity of the endohelminths' species with regard to P. corruscans and S. borelli. This is probably due to what occurs with environments during the high water period when they are interlinked. The hydrological level was a less influential variable in endoparasitic infrapopulations of the hosts studied. In P. corruscans only three species, S. spinulifera, Nomimoscolex sudobim Woodland, 1934 and Megatnylacus travassosi Pavanelli & Rego, 1992 presented higher mean intensities in the high water period. This fact was also observed in the case of C. pinnai in S. borelli.

Key words: Ecology, endohelminths, freshwater fish, environment

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ACKNOWLEDGMENTS. This paper is part of an interdisciplinary project, "Environmental studies of the Paraná River floodplain in the area comprehending the mouth of the River Paranapanema and the Itaipu Reservoir", undertaken with the help of PADCT/CIAMB, which we thank for the financial support. Acknowledgment is due to NUPELIA (Nucleus for the Research in Limnology. Ichthyology and Aquiculture) for the logistic support.

REFERENCES

Agostinho, A.A. & M. Zalewski. (in press). The dependence of fish community structure and dynamics on floodplain and riparian ecotone zone in Paraná river, Brazil. Hydrobiologia.

Amato, J.F.R.; W.A. Boeger & S.B. Amato. 1991. Protocolos para laboratório - coleta e processamento de parasites do pescado. Universidade Federal Rural do Rio de Janeiro, Imprensa Universitária, 81p.

Andrian, I.F.; G. Torrente & C.M.L. Ferreti. 1994. Atividade alimentar das piavas Schizodon borelli Boulenger, 1900 e Schizodon altoparanae Garavello e Britski, 1990 (Characiformes, Anostomidae), na planície de inundação do alto rio Paraná (22º40' - 22º50' S / 53º15' - 53º40' W), Brasil. Rev. UNIMAR. 16 (supl. 3):107-116.

Bell, G. & A. Burt. 1991. The comparative biology of parasite species diversity: internal helminths of freshwater fish. J. Animal Ecol. 60:1047-1063.

Fowler, H.W. 1951. Os peixes de água doce do Brasil. Arq. Zool. São Paulo 6:405-625.

Fuem/Nupelia. 1993. Estudos ambientais da planície de inundação do rio Paraná, no trecho compreendido entre a foz do rio Paranapanema e o reservatório de Itaipu. Maringá, 3 v. Relatório anual - Apoio PADCT/CIAMB.

______. 1994. Estudos ambientais da planície de inundação do rio Paraná, no trecho compreendido entre a foz do rio Paranapanema e o reservatório de Itaipu. Maringá, 3 vol. Relatório anual - Apoio PADCT/CIAMB.

Goulding, M.; M.L. Carvalho & E.J.G. Ferreira. 1988. Rio Negro: rich life in poor water - Amazonian diversity and floodchain ecology as seen through fish communities. The Hague, SPB Academic Publishing, 200p.

Holmes, J.C. & P.W. Price. 1986. Communities of parasites, p. 187-213. In: Kikkawa, J. & D.I. Anderson (Eds). Community Ecology: Pattern and Process. Oxford, Blackwell Scientific Publications, 432p.

Lowe-McConnel, R.H. 1975. Fish Communities in Tropical Freshwaters: their distribution, ecology and evolution. London, Longman, 337p.

______. 1987. Ecological studies in tropical fish communities. Cambridge, Cambridge University Press, 382p.

Ludwig, J.A. & J.F. Reynolds. 1988. Statistical Ecology: A Primer on Methods and Computing. New York, Wiley-Interscience Publication, 337p.

Machado, M.H.; G.C. Pavanelli & R.M. Takemoto. (1994). Influence of host's sex and size on endoparasitic infrapopulation of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the high Paraná River. Rev. Bras. Parasitol. Vet. 3 (2):143-148.

______. (in press). Structure and diversity of endoparasitic infracommunities and the trophic level of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the High Paraná River. Mem. Inst. Oswaldo Cruz 91.

Magalhães, A.C. 1931. Sorubim pintado, pintado - Pseudoplatystoma corruscans, Agassiz, p. 157-158. In: Monografia Brasileira de Peixes Fluviais. São Paulo, Graphicar.

Margolis, L.; G.W. Esch; J.C. Holmes; A.M. Kuris & G.A. Schad. 1982. The use of ecological terms in parasitology (report of an Ad hoc Committee of the American society of Parasitologists). J. Parasitol. 68:131-133.

Marques, E.E. 1993. Biologia reprodutiva, alimentação natural e dinâmica da nutrição de pintado, Pseudoplatystoma corruscans (Agassiz, 1829) (Osteichthyes, Pimelodidae) no alto rio Paraná. Dissertação de Mestrado, Departamento de Zoologia, Universidade Federal do Paraná, 104p.

Nikolsky, G.V. 1963. The Ecology of Fishes. London, Academic Press, 352p.

Ringuelet, R.A.; R.A. Aramburu & A.A. Aramburu. 1967. Los Peces Argentinos de Agua Dulce. La Plata, Comissión de Investigación Científica, 602p.

Schmidt, G.D. & L.S. Roberts. 1989. Foundations of Parasitology. 4. ed. St. Louis: Times Mirror/Mosby College Publishing. p. 331-334.

Silgel, S. 1975. Estatística Não Paramétrica (Para Ciências do Comportamento). São Paulo, McGraw-Hill do Brasil, 350p.

Stone, J.E. & D.B. Pence. 1978. Ecology of helminth parasitism in the bobcat from West Texas. J. Parasitol. 64:295-302.

Stromberg, P.C. & J.L Crites. 1974. The life cycle and development of Camallanus oxycephalus Ward and Magath 1916 (Nematoda: Camallanidae). J. Parasitol. 60 (1):117-124.

Thomaz, S.M., M.C. Roberto; F.A. Lansac Tôha; F.A. Esteves & A.F. Lima. 1991. Dinâmica temporal dos principais fatores limnológicos do rio Baía - planície de inundação do alto rio Paraná - MS, Brasil. Rev. UNIMAR 13 (2):299-312.

Thomaz, S.M.; F.A. Lansac Tôha; M.C. Roberto; F.A. Esteves & A.F. Lima. 1992a. Seasonal variation of some hidrological factors of lagoa do Guaraná, a várzea lake of the high Rio Paraná, State of Mato Grosso do Sul, Brazil. Rev. Hydrobiol. trop. 25 (4):269-276.

Thomaz, S.M.; M.C. Roberto; F.A. Lansac Tôha; A.F. Lima & F.A. Esteves. 1992b. Características limnológicas de uma estação de amostragem alto rio Paraná e outro do baixo rio Ivinheima - (PR, MS - Brasil). Acta Lininol. Brasil. 4:32-51.

Thul, J.E.; D.J. Forrester & C.L. Abercrombie. 1985. Ecology of parasitic helminths of wood ducks Aix sponsa, in the Atlantic Flyway. Proc. Helminthol. Soc. Wash. 52:297-310.

Torrente, G. 1994. Dieta alimentar e suas relações com aspectos morfológicos do trato digestivo de Schizodon borelli Boulenger, 1900 (Characiformes, Anostomidae), da planície de inundação do alto rio Paraná (22º40'-22º50' S, 53º15'-53º40' W), Brasil. Monografia de Bacharelado, Departamento de Biologia Universidade Estadual de Maringá, 22p.

Welcomme, R.L. 1985. River Fisheries. Roma, Food and Agriculture Organization of the United Nations, 330p. (FAO Fisheries Technical Papers, 262).

Williams, H. & A. Jones. 1994. Parasitic Worms of Fish. London; Bristol, Taylor & Francis, p. 85-88.

Yanez, D.M. & A.G. Canaris. 1988. Metazoan parasite community composition and structure of migrating Wilson's phalarope, Steganopus tricolor Viellot, 1819 (Aves), from El Paso county, Texas. J. Parasitol. 74:754-762.

Recebido em 25.VIII.1995; aceito em 19.IV.1996.

Agostinho, A.A. & M. Zalewski. (in press). The dependence of fish community structure and dynamics on floodplain and riparian ecotone zone in Paraná river, Brazil. Hydrobiologia.
Amato, J.F.R.; W.A. Boeger & S.B. Amato. 1991. Protocolos para laboratório - coleta e processamento de parasites do pescado. Universidade Federal Rural do Rio de Janeiro, Imprensa Universitária, 81p.
Andrian, I.F.; G. Torrente & C.M.L. Ferreti. 1994. Atividade alimentar das piavas Schizodon borelli Boulenger, 1900 e Schizodon altoparanae Garavello e Britski, 1990 (Characiformes, Anostomidae), na planície de inundação do alto rio Paraná (22º40' - 22º50' S / 53º15' - 53º40' W), Brasil. Rev. UNIMAR. 16 (supl. 3):107-116.
Bell, G. & A. Burt. 1991. The comparative biology of parasite species diversity: internal helminths of freshwater fish. J. Animal Ecol. 60:1047-1063.
Fowler, H.W. 1951. Os peixes de água doce do Brasil. Arq. Zool. São Paulo 6:405-625.
Fuem/Nupelia. 1993. Estudos ambientais da planície de inundação do rio Paraná, no trecho compreendido entre a foz do rio Paranapanema e o reservatório de Itaipu. Maringá, 3 v. Relatório anual - Apoio PADCT/CIAMB.
______. 1994. Estudos ambientais da planície de inundação do rio Paraná, no trecho compreendido entre a foz do rio Paranapanema e o reservatório de Itaipu. Maringá, 3 vol. Relatório anual - Apoio PADCT/CIAMB.
Goulding, M.; M.L. Carvalho & E.J.G. Ferreira. 1988. Rio Negro: rich life in poor water - Amazonian diversity and floodchain ecology as seen through fish communities. The Hague, SPB Academic Publishing, 200p.
Holmes, J.C. & P.W. Price. 1986. Communities of parasites, p. 187-213. In: Kikkawa, J. & D.I. Anderson (Eds). Community Ecology: Pattern and Process. Oxford, Blackwell Scientific Publications, 432p.
Lowe-McConnel, R.H. 1975. Fish Communities in Tropical Freshwaters: their distribution, ecology and evolution. London, Longman, 337p.
______. 1987. Ecological studies in tropical fish communities. Cambridge, Cambridge University Press, 382p.
Ludwig, J.A. & J.F. Reynolds. 1988. Statistical Ecology: A Primer on Methods and Computing. New York, Wiley-Interscience Publication, 337p.
Machado, M.H.; G.C. Pavanelli & R.M. Takemoto. (1994). Influence of host's sex and size on endoparasitic infrapopulation of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the high Paraná River. Rev. Bras. Parasitol. Vet. 3 (2):143-148.
______. (in press). Structure and diversity of endoparasitic infracommunities and the trophic level of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the High Paraná River. Mem. Inst. Oswaldo Cruz 91.
Magalhães, A.C. 1931. Sorubim pintado, pintado - Pseudoplatystoma corruscans, Agassiz, p. 157-158. In: Monografia Brasileira de Peixes Fluviais. São Paulo, Graphicar.
Margolis, L.; G.W. Esch; J.C. Holmes; A.M. Kuris & G.A. Schad. 1982. The use of ecological terms in parasitology (report of an Ad hoc Committee of the American society of Parasitologists). J. Parasitol. 68:131-133.
Marques, E.E. 1993. Biologia reprodutiva, alimentação natural e dinâmica da nutrição de pintado, Pseudoplatystoma corruscans (Agassiz, 1829) (Osteichthyes, Pimelodidae) no alto rio Paraná. Dissertação de Mestrado, Departamento de Zoologia, Universidade Federal do Paraná, 104p.
Nikolsky, G.V. 1963. The Ecology of Fishes. London, Academic Press, 352p.
Ringuelet, R.A.; R.A. Aramburu & A.A. Aramburu. 1967. Los Peces Argentinos de Agua Dulce. La Plata, Comissión de Investigación Científica, 602p.
Schmidt, G.D. & L.S. Roberts. 1989. Foundations of Parasitology. 4. ed. St. Louis: Times Mirror/Mosby College Publishing. p. 331-334.
Silgel, S. 1975. Estatística Não Paramétrica (Para Ciências do Comportamento). São Paulo, McGraw-Hill do Brasil, 350p.
Stone, J.E. & D.B. Pence. 1978. Ecology of helminth parasitism in the bobcat from West Texas. J. Parasitol. 64:295-302.
Stromberg, P.C. & J.L Crites. 1974. The life cycle and development of Camallanus oxycephalus Ward and Magath 1916 (Nematoda: Camallanidae). J. Parasitol. 60 (1):117-124.
Thomaz, S.M., M.C. Roberto; F.A. Lansac Tôha; F.A. Esteves & A.F. Lima. 1991. Dinâmica temporal dos principais fatores limnológicos do rio Baía - planície de inundação do alto rio Paraná - MS, Brasil. Rev. UNIMAR 13 (2):299-312.
Thomaz, S.M.; F.A. Lansac Tôha; M.C. Roberto; F.A. Esteves & A.F. Lima. 1992a. Seasonal variation of some hidrological factors of lagoa do Guaraná, a várzea lake of the high Rio Paraná, State of Mato Grosso do Sul, Brazil. Rev. Hydrobiol. trop. 25 (4):269-276.
Thomaz, S.M.; M.C. Roberto; F.A. Lansac Tôha; A.F. Lima & F.A. Esteves. 1992b. Características limnológicas de uma estação de amostragem alto rio Paraná e outro do baixo rio Ivinheima - (PR, MS - Brasil). Acta Lininol. Brasil. 4:32-51.
Thul, J.E.; D.J. Forrester & C.L. Abercrombie. 1985. Ecology of parasitic helminths of wood ducks Aix sponsa, in the Atlantic Flyway. Proc. Helminthol. Soc. Wash. 52:297-310.
Torrente, G. 1994. Dieta alimentar e suas relações com aspectos morfológicos do trato digestivo de Schizodon borelli Boulenger, 1900 (Characiformes, Anostomidae), da planície de inundação do alto rio Paraná (22º40'-22º50' S, 53º15'-53º40' W), Brasil. Monografia de Bacharelado, Departamento de Biologia Universidade Estadual de Maringá, 22p.
Welcomme, R.L. 1985. River Fisheries. Roma, Food and Agriculture Organization of the United Nations, 330p. (FAO Fisheries Technical Papers, 262).
Williams, H. & A. Jones. 1994. Parasitic Worms of Fish. London; Bristol, Taylor & Francis, p. 85-88.
Yanez, D.M. & A.G. Canaris. 1988. Metazoan parasite community composition and structure of migrating Wilson's phalarope, Steganopus tricolor Viellot, 1819 (Aves), from El Paso county, Texas. J. Parasitol. 74:754-762.

Publication Dates

Publication in this collection
22 July 2009
Date of issue
1995

History

Accepted
19 Apr 1996
Received
25 Aug 1995

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] Agostinho, A.A. & M. Zalewski. (in press). The dependence of fish community structure and dynamics on floodplain and riparian ecotone zone in Paraná river, Brazil. Hydrobiologia.

[2] Amato, J.F.R.; W.A. Boeger & S.B. Amato. 1991. Protocolos para laboratório - coleta e processamento de parasites do pescado. Universidade Federal Rural do Rio de Janeiro, Imprensa Universitária, 81p.

[3] Andrian, I.F.; G. Torrente & C.M.L. Ferreti. 1994. Atividade alimentar das piavas Schizodon borelli Boulenger, 1900 e Schizodon altoparanae Garavello e Britski, 1990 (Characiformes, Anostomidae), na planície de inundação do alto rio Paraná (22º40' - 22º50' S / 53º15' - 53º40' W), Brasil. Rev. UNIMAR. 16 (supl. 3):107-116.

[4] Bell, G. & A. Burt. 1991. The comparative biology of parasite species diversity: internal helminths of freshwater fish. J. Animal Ecol. 60:1047-1063.

[5] Fowler, H.W. 1951. Os peixes de água doce do Brasil. Arq. Zool. São Paulo 6:405-625.

[6] Fuem/Nupelia. 1993. Estudos ambientais da planície de inundação do rio Paraná, no trecho compreendido entre a foz do rio Paranapanema e o reservatório de Itaipu. Maringá, 3 v. Relatório anual - Apoio PADCT/CIAMB.

[7] ______. 1994. Estudos ambientais da planície de inundação do rio Paraná, no trecho compreendido entre a foz do rio Paranapanema e o reservatório de Itaipu. Maringá, 3 vol. Relatório anual - Apoio PADCT/CIAMB.

[8] Goulding, M.; M.L. Carvalho & E.J.G. Ferreira. 1988. Rio Negro: rich life in poor water - Amazonian diversity and floodchain ecology as seen through fish communities. The Hague, SPB Academic Publishing, 200p.

[9] Holmes, J.C. & P.W. Price. 1986. Communities of parasites, p. 187-213. In: Kikkawa, J. & D.I. Anderson (Eds). Community Ecology: Pattern and Process. Oxford, Blackwell Scientific Publications, 432p.

[10] Lowe-McConnel, R.H. 1975. Fish Communities in Tropical Freshwaters: their distribution, ecology and evolution. London, Longman, 337p.

[11] ______. 1987. Ecological studies in tropical fish communities. Cambridge, Cambridge University Press, 382p.

[12] Ludwig, J.A. & J.F. Reynolds. 1988. Statistical Ecology: A Primer on Methods and Computing. New York, Wiley-Interscience Publication, 337p.

[13] Machado, M.H.; G.C. Pavanelli & R.M. Takemoto. (1994). Influence of host's sex and size on endoparasitic infrapopulation of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the high Paraná River. Rev. Bras. Parasitol. Vet. 3 (2):143-148.

[14] ______. (in press). Structure and diversity of endoparasitic infracommunities and the trophic level of Pseudoplatystoma corruscans and Schizodon borelli (Osteichthyes) of the High Paraná River. Mem. Inst. Oswaldo Cruz 91.

[15] Magalhães, A.C. 1931. Sorubim pintado, pintado - Pseudoplatystoma corruscans, Agassiz, p. 157-158. In: Monografia Brasileira de Peixes Fluviais. São Paulo, Graphicar.

[16] Margolis, L.; G.W. Esch; J.C. Holmes; A.M. Kuris & G.A. Schad. 1982. The use of ecological terms in parasitology (report of an Ad hoc Committee of the American society of Parasitologists). J. Parasitol. 68:131-133.

[17] Marques, E.E. 1993. Biologia reprodutiva, alimentação natural e dinâmica da nutrição de pintado, Pseudoplatystoma corruscans (Agassiz, 1829) (Osteichthyes, Pimelodidae) no alto rio Paraná. Dissertação de Mestrado, Departamento de Zoologia, Universidade Federal do Paraná, 104p.

[18] Nikolsky, G.V. 1963. The Ecology of Fishes. London, Academic Press, 352p.

[19] Ringuelet, R.A.; R.A. Aramburu & A.A. Aramburu. 1967. Los Peces Argentinos de Agua Dulce. La Plata, Comissión de Investigación Científica, 602p.

[20] Schmidt, G.D. & L.S. Roberts. 1989. Foundations of Parasitology. 4. ed. St. Louis: Times Mirror/Mosby College Publishing. p. 331-334.

[21] Silgel, S. 1975. Estatística Não Paramétrica (Para Ciências do Comportamento). São Paulo, McGraw-Hill do Brasil, 350p.

[22] Stone, J.E. & D.B. Pence. 1978. Ecology of helminth parasitism in the bobcat from West Texas. J. Parasitol. 64:295-302.

[23] Stromberg, P.C. & J.L Crites. 1974. The life cycle and development of Camallanus oxycephalus Ward and Magath 1916 (Nematoda: Camallanidae). J. Parasitol. 60 (1):117-124.

[24] Thomaz, S.M., M.C. Roberto; F.A. Lansac Tôha; F.A. Esteves & A.F. Lima. 1991. Dinâmica temporal dos principais fatores limnológicos do rio Baía - planície de inundação do alto rio Paraná - MS, Brasil. Rev. UNIMAR 13 (2):299-312.

[25] Thomaz, S.M.; F.A. Lansac Tôha; M.C. Roberto; F.A. Esteves & A.F. Lima. 1992a. Seasonal variation of some hidrological factors of lagoa do Guaraná, a várzea lake of the high Rio Paraná, State of Mato Grosso do Sul, Brazil. Rev. Hydrobiol. trop. 25 (4):269-276.

[26] Thomaz, S.M.; M.C. Roberto; F.A. Lansac Tôha; A.F. Lima & F.A. Esteves. 1992b. Características limnológicas de uma estação de amostragem alto rio Paraná e outro do baixo rio Ivinheima - (PR, MS - Brasil). Acta Lininol. Brasil. 4:32-51.

[27] Thul, J.E.; D.J. Forrester & C.L. Abercrombie. 1985. Ecology of parasitic helminths of wood ducks Aix sponsa, in the Atlantic Flyway. Proc. Helminthol. Soc. Wash. 52:297-310.

[28] Torrente, G. 1994. Dieta alimentar e suas relações com aspectos morfológicos do trato digestivo de Schizodon borelli Boulenger, 1900 (Characiformes, Anostomidae), da planície de inundação do alto rio Paraná (22º40'-22º50' S, 53º15'-53º40' W), Brasil. Monografia de Bacharelado, Departamento de Biologia Universidade Estadual de Maringá, 22p.

[29] Welcomme, R.L. 1985. River Fisheries. Roma, Food and Agriculture Organization of the United Nations, 330p. (FAO Fisheries Technical Papers, 262).

[30] Williams, H. & A. Jones. 1994. Parasitic Worms of Fish. London; Bristol, Taylor & Francis, p. 85-88.

[31] Yanez, D.M. & A.G. Canaris. 1988. Metazoan parasite community composition and structure of migrating Wilson's phalarope, Steganopus tricolor Viellot, 1819 (Aves), from El Paso county, Texas. J. Parasitol. 74:754-762.