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Parasitism by Monogenoidea in Piaractus mesopotamicus (Characiformes, Characidae) cultivated in Paraná River (Brazil)

Parasitismo por Monogenoidea em Piaractus mesopotamicus (Characiformes, Characidae) cultivados no rio Paraná (Brasil)

Abstract

This study investigated the occurrence, prevalence, mean abundance and mean intensity of monogenoidean parasites in Piaractus mesopotamicus farmed in cages in the reservoir of the Itaipu Hydroelectric Power Station, Paraná River, Brazil. The parasite distribution pattern and the correlation of prevalence and abundance with the total length of hosts were also investigated. Four monogenoidean species were collected: Anacanthorus penilabiatus, A. toledoensis, Mymarothecium ianwhitingtoni and M. viatorum. All the parasites collected in P. mesopotamicus showed the typical aggregated distribution pattern, and the abundance and the prevalence did not shown any correlation with the total length of hosts.

Keywords:
Monogenoidea; Piaractus mesopotamicus; Paraná River; Anacanthorus; Mymarothecium

Resumo

Neste estudo foi investigada a ocorrência, prevalência, abundância média e intensidade média de Monogenoidea parasitos de Piaractus mesopotamicus, cultivados em tanques-rede no reservatório da Usina Hidrelétrica de Itaipu, rio Paraná, Brasil. Foram investigados ainda o padrão de distribuição parasitária e a correlação entre a prevalência e abundância com o comprimento total dos hospedeiros. Quatro espécies de Monogenoidea foram coletadas: Anacanthorus penilabiatus, A. toledoensis, Mymarothecium ianwhitingtoni e M. viatorum. Todos os parasitos coletados em P. mesopotamicus apresentaram típico padrão de distribuição agregada e não foi observada correlação entre a abundância e a prevalência e o comprimento total dos hospedeiros.

Palavras-chave:
Monogenoidea; Piaractus mesopotamicus; rio Paraná; Anacanthorus; Mymarothecium

1 Introduction

Piaractus mesopotamicus (Holmberg, 1887) is a characiform fish commonly known as “pacu” in Brazil. This fish reaches maturity at a length of 40.5 cm and is one of the most commonly farmed species in Brazil, because of its importance for the food diet, ecology and sport fishery (Jégu, 2003JÉGU, M., 2003. Serrasalminae (Pacus and piranhas). In: R.E. REIS, SOK and C.J. FERRARIS JUNIOR, eds. Checklist of the freshwater fishes of South and Central America. Porto Alegre: EDIPUCRS, pp. 182-196.). The significant increment in aquaculture around the world has increased the importance of studies of parasites and other pathogens of aquatic organisms, especially in those hosts that have the potential for production and sale (Luque, 2004LUQUE, J.L., 2004. Parasitologia de peixes marinhos na América do Sul: estado atual e perspectivas. In: M.J.T. RANZANI-PAIVA, R.M. TAKEMOTO and M.A.P. LIZAMA. Sanidade de organismos aquáticos. São Paulo: Varela, pp. 199-215.). The monitoring of parasites and other fish pathogens is an important part of prophylactic management both for production (Pavanelli et al., 2008PAVANELLI, G.C., EIRAS, J.C. and TAKEMOTO, R.M., 2008. Doenças de peixes: profilaxia, diagnóstico e tratamento. Maringá: EDUEM.). Parasitic infections are more relevant in the Neotropical region because of the climatic characteristics of this region, which facilitate the rapid and continuous spread of these pathogens (Thatcher and Brites-Neto, 1994THATCHER, V.E. and BRITES-NETO, J., 1994. Diagnóstico, prevenção e tratamento das enfermidades de peixes neotropicais de água doce. Revista Brasileira de Medicina Veterinária, vol. 16, pp. 111-128.). The Monogenoidea are one of the largest groups of parasitic flatworms, comprising about 60 families and more than 3000 described species. Some species have detrimental effects on both wild and farmed fish populations, causing important economic damage (Fannes et al. 2015FANNES, W., MAARTEN, P.M., VANHOVE, M.P.M., HUYSE, T. and PALADINI, G., 2015. A scanning electron microscope technique for studying the sclerites of Cichlidogyrus.Parasitology Research, vol. 114, no. 5, pp. 2031-2034. PMid:25828814. http://dx.doi.org/10.1007/s00436-015-4446-7.
http://dx.doi.org/10.1007/s00436-015-444...
). Several authors have studied monogenoideans in P. mesopotamicus: to date, parasitological (Alexandrino et al., 1995ALEXANDRINO, A.C., RANZANI-PAIVA, M.J.T., ESHIKAWA, C.M., ARANA, S., MANDELLI JÚNIOR, J. and EIRAS, A.C., 1995. Infestação aguda por sp. (Protozoa, Myxosporea) e Dactylogyridae (Platyhelminthes, Monogenea), em Pacu, . HenneguyaPiaractus mesopotamicus (Holmberg, 1887) (Osteichthyes, Characidae)Boletim do Instituto de Pesca, vol. 22, pp. 115-119.; Eiras et al., 1995EIRAS, J.C., RANZANI-PAIVA, M.J.T., ISHIKAWA, C.M. and ALEXANDRINO, A.C., 1995. Ectoparasites of semi-intensively farmed tropical freshwater fish . Piaractus mesopotamicus, Prochilodus lineatus and Colossoma macropomum in BrazilBulletin of the European Association of Fish Pathologists, vol. 15, pp. 148-151.; Kohn and Cohen, 1998KOHN, A. and COHEN, S.C., 1998. South American Monogenea: list of species, hosts and geographical distribution. International Journal for Parasitology, vol. 28, no. 10, pp. 1517-1554. PMid:9801914. http://dx.doi.org/10.1016/S0020-7519(98)00083-6.
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; Martins et al., 2002aMARTINS, M.L., ONAKA, E.M., MORAES, F.R., BOZZO, F.R., PAIVA, A.M.F.C. and GONÇALVES, A., 2002a. Recent studies on parasitic infections of freshwater cultivated fish in the state of São Paulo, Brazil. Acta Scientiarum, vol. 24, pp. 981-985.; Pamplona-Basilio et al., 2001PAMPLONA-BASILIO, M.C., KOHN, A. and FEITOSA, V.A., 2001. New host records and description of the egg of (Monogenea, Dactylogyridae). Anacanthorus penilabiatusMemorias do Instituto Oswaldo Cruz, vol. 96, no. 5, pp. 667-668. PMid:11500767. http://dx.doi.org/10.1590/S0074-02762001000500014.
http://dx.doi.org/10.1590/S0074-02762001...
; Schalch et al., 2006SCHALCH, S.H.C., MORAES, J.R.E. and MORAES, F.R., 2006. Fauna parasitária de peixes oriundos de “pesque-pague” do município de Guariba, São Paulo, Brazil. Acta Scientiarum Biological Sciences, vol. 28, pp. 291-297.; Lizama et al., 2007LIZAMA, M.A.P., TAKEMOTO, R.M., RANZANI-PAIVA, M.J.T., AYROSA, L.M.S. and PAVANELLI, G.C., 2007. Relação parasito-hospedeiro em peixes de piscicultura da região de Assis, estado de São Paulo, Brasil. 2. Piaractus mesopotamicus (Holmberg, 1887). Acta Scientiarum Biological Sciences, vol. 29, pp. 437-445. http://dx.doi.org/10.4025/actascibiolsci.v29i2.594.
http://dx.doi.org/10.4025/actascibiolsci...
; Cohen and Kohn, 2005COHEN, S.C. and KOHN, A., 2005. A new species of and new hosts and geographical records for M. viatorum (Monogenea: Dactylogyridae) parasites of freshwater fishes in Brazil. MymarotheciumFolia Parasitologica, vol. 52, no. 4, pp. 307-310. PMid:16405294. http://dx.doi.org/10.14411/fp.2005.042.
http://dx.doi.org/10.14411/fp.2005.042...
, 2009COHEN, S.C. and KOHN, A., 2009. On Dactylogyridae (Monogenea) of four species of characid fishes from Brazil. Check List, vol. 5, no. 2, pp. 351-356. http://dx.doi.org/10.15560/5.2.351.
http://dx.doi.org/10.15560/5.2.351...
; Franceschini et al., 2013FRANCESCHINI, L., ZAGO, A.C., SCHALCH, S.H.C., GARCIA, F., ROMERA, D.M. and SILVA, R., 2013. Parasitic infections of . Piaractus mesopotamicus and hybrid (P. mesopotamicus x Piaractus brachypomus) cultured in BrazilRevista Brasileira de Parasitologia Veterinária, vol. 22, no. 3, pp. 407-414. PMid:24142174. http://dx.doi.org/10.1590/S1984-29612013000300015.
http://dx.doi.org/10.1590/S1984-29612013...
), histopathological (Martins and Romero, 1996MARTINS, M.L. and ROMERO, N.G., 1996. Efectos del parasitismo sobre el tejido branquial em peces cultivados: Estudio parasitologico e histopatologico. Revista Brasileira de Zoologia, vol. 13, no. 2, pp. 489-500. http://dx.doi.org/10.1590/S0101-81751996000200017.
http://dx.doi.org/10.1590/S0101-81751996...
; Campos et al., 2011CAMPOS, C.M., MORAES, J.R.E. and MORAES, F.R., 2011. Histopathology of gills of (Holmberg, 1887) and . Piaractus mesopotamicusProchilodus lineatus (Valenciennes, 1836) infested by monogenean and myxosporea, caugth in Aquidauana River, State of Mato Grosso do Sul, BrazilRevista Brasileira de Parasitologia Veterinária, vol. 20, no. 1, pp. 67-70. PMid:21439236. http://dx.doi.org/10.1590/S1984-29612011000100014.
http://dx.doi.org/10.1590/S1984-29612011...
; Tavares-Dias et al., 2002TAVARES-DIAS, M., MARTINS, M.L., SCHALCH, S.H.C., ONAKA, E.D., QUINTANA, C.I.F., MORAES, J.R.E. and MORAES, F.R., 2002. Alterações hematológicas e histopatológicas em pacu, Holmberg, 1887 (Osteichthyes, Characidae), tratado com sulfato de cobre (CuSO4). Piaractus mesopotamicusActa Scientiarum, vol. 24, pp. 547-554.; Jerônimo et al., 2014JERÔNIMO, G.T., PÁDUA, S.B., BAMPI, D., GONÇALVES, E.L.T., GARCIA, P., ISHIKAWA, M.M. and MARTINS, M.L., 2014. Haematological and histhological analysis in South American fish Piaractus mesopotamicus parasitized by monogenean (Dactylogyridae). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 74, no. 4, pp. 1000-1006. PMid:25627614. http://dx.doi.org/10.1590/1519-6984.09513.
http://dx.doi.org/10.1590/1519-6984.0951...
), morphological (Boeger et al., 1995BOEGER, W.A., HUSAK, W.S. and MARTINS, M.L., 1995. Neotropical Monogenoidea. 25. Anacanthorus penilabiatus n.sp. (Dactylogyridae: Ancyrocephalinae) from Piaractus mesopotamicus (Osteichthyes: Serrasalmidae), cultivated in the State of São Paulo, Brazil. Memorias do Instituto Oswaldo Cruz, vol. 90, no. 6, pp. 699-701. http://dx.doi.org/10.1590/S0074-02761995000600008.
http://dx.doi.org/10.1590/S0074-02761995...
; Souza et al., 2000SOUZA, M.L.R., MARTINS, L.M. and SANTOS, J.M., 2000. Microscopia eletrônica de varredura de parasitos branquiais de Holmberg, 1887 cultivados no Estado de São Paulo, Brasil. Piaractus mesopotamicusActa Scientiarum Biological Sciences, vol. 22, pp. 527-531.; Cohen and Kohn, 2008COHEN, S.C. and KOHN, A., 2008. South American Monogenea: list of species, hosts and geographical distribution from 1997 to 2008. Zootaxa, vol. 1924, pp. 1-42.; Leão et al., 2015LEÃO, M.S.L., SÃO CLEMENTE, S.C. and COHEN, S.C., 2015. Anacanthorus toledoensis n. sp. and Mymarothecium ianwhittingtoni n. sp. (Dactylogyridae: Monogenoidea) parasitizing cage-reared (Characiformes, Characidae) in the State of Paraná, Brazil. Piaractus mesopotamicusComparative Parasitology, vol. 82, no. 2, pp. 268-273. http://dx.doi.org/10.1654/4759.1.
http://dx.doi.org/10.1654/4759.1...
), pathological (Tavares‐Dias et al., 2000TAVARES‐DIAS, M., MARTINS, M.L., MORAES, F.R. and KRONKA, S.N., 2000. Fator de condição e relação esplenossomática em teleósteos de água doce naturalmente parasitados. Acta Scientiarum, vol. 22, pp. 533-537.), hemathological (Martins et al., 1995MARTINS, M.L., CASTAGNDLI, N., ZUIM, S.M.F. and URBINATI, E.C., 1995. Influência de diferentes níveis de vitamina C na ração sobre parâmetros hematológicos de alevinos de . Piaractus mesopotamicus Hoemberg (Osteichthyes, Characidae)Revista Brasileira de Zoologia, vol. 12, no. 3, pp. 609-618. http://dx.doi.org/10.1590/S0101-81751995000300016.
http://dx.doi.org/10.1590/S0101-81751995...
; Tavares-Dias et al., 2002TAVARES-DIAS, M., MARTINS, M.L., SCHALCH, S.H.C., ONAKA, E.D., QUINTANA, C.I.F., MORAES, J.R.E. and MORAES, F.R., 2002. Alterações hematológicas e histopatológicas em pacu, Holmberg, 1887 (Osteichthyes, Characidae), tratado com sulfato de cobre (CuSO4). Piaractus mesopotamicusActa Scientiarum, vol. 24, pp. 547-554., 2008TAVARES‐DIAS, M., MORAES, F.R. and MARTINS, M.L., 2008. Hematological assessment in four Brazilian teleost fish with parasitic infections collected in feefishing from Franca, São Paulo, Brazil. Boletim do Instituto de Pesca, vol. 34, pp. 189-196.) and terapeutic (Martins, 1998MARTINS, M.L., 1998. Evaluation of the addition of ascorbic acid to the ration of cultivade (Characidae) on the infrapopulation of (Monogenea). Piaractus mesopotamicusAnacanthorus penilabiatusBrazilian Journal of Medical and Biological Research, vol. 31, no. 5, pp. 655-658. PMid:9698770. http://dx.doi.org/10.1590/S0100-879X1998000500008.
http://dx.doi.org/10.1590/S0100-879X1998...
; Martins et al., 2000MARTINS, M.L., MORAES, F.R., FUJIMOTO, R.Y., ONAKA, E.M., NOMURA, D.T., SILVA, C.A.H. and SCHALCH, S.H.C., 2000. Parasitic infections in cultivated freshwater fishes a survey of diagnosticated cases from 1993 to 1998. Revista Brasileira de Parasitologia Veterinária, vol. 9, pp. 23-28., 2002bMARTINS, M.L., MORAES, F.R., MIYAZAKI, D.M.Y., BRUM, C.D., ONAKA, E.M., FENERICK JUNIOR, J. and BOZZO, F.R., 2002b. Alternative treatment for (Monogenea: Dactylogyridae) infection in cultivated pacu, . Anacanthorus penilabiatusPiaractus mesopotamicus (Osteichthyes: Characidae) in Brazil and its haematological effectsParasite (Paris, France), vol. 9, no. 2, pp. 175-180. PMid:12116864. http://dx.doi.org/10.1051/parasite/2002092175.
http://dx.doi.org/10.1051/parasite/20020...
; Tavares-Dias et al., 2002TAVARES-DIAS, M., MARTINS, M.L., SCHALCH, S.H.C., ONAKA, E.D., QUINTANA, C.I.F., MORAES, J.R.E. and MORAES, F.R., 2002. Alterações hematológicas e histopatológicas em pacu, Holmberg, 1887 (Osteichthyes, Characidae), tratado com sulfato de cobre (CuSO4). Piaractus mesopotamicusActa Scientiarum, vol. 24, pp. 547-554.; Onaka et al., 2003ONAKA, E.M., MARTINS, M.L. and MORAES, F.R., 2003. Eficácia do albendazol e praziquantel no controle de Anacanthorus penilabiatus (monogenea: dactylogyridae), parasito de pacu (osteichthyes: characidae). I. Banhos terapêuticos. Piaractus mesopotamicusBoletim do Instituto de Pesca, vol. 29, pp. 101-107.; Belo et al., 2005BELO, M.A., FENERICK JUNIOR, J., SOARES, V.E. and MORAES, F.R., 2005. Suplementação com DL-ɑ acetato de tocoferila e parasitismo por (Monogenea: Dactylogyridae) em . Anacanthorus penilabiatusPiaractus mesopotamicus (Osteichthyes: Characidae)Acta Scientiarum, vol. 27, pp. 73-79.; Schalch et al., 2006SCHALCH, S.H.C., MORAES, J.R.E. and MORAES, F.R., 2006. Fauna parasitária de peixes oriundos de “pesque-pague” do município de Guariba, São Paulo, Brazil. Acta Scientiarum Biological Sciences, vol. 28, pp. 291-297.; Cruz et al., 2008CRUZ, C., MACHADO NETO, J.G., FUJIMOTO, R.Y., HENARES, M.N.P. and DUÓ, D.A., 2008. Eficácia do paration metílico e do extrato aquoso de folhas secas de nim no controle de (Monogenoidea) em pacu (. Anacanthorus penilabiatusPiaractus mesopotamicus)Boletim do Instituto de Pesca, vol. 34, pp. 61-69.; Fujimoto et al., 2010FUJIMOTO, R.Y., CASTRO, M.P., MARTINS, M.L., MORAES, F.R., VARELLA, J.E.A. and DINIZ, D.G., 2010. Effects of Chromium Supplementation on the infrapopulations of Anacanthorus penilabiatus (Monogenoidea) and Piscinoodinium pillulare (Dinoflagellida) parasites of (Characidae). Piaractus mesopotamicusBrazilian Archives of Biology and Technology, vol. 53, no. 4, pp. 827-833. http://dx.doi.org/10.1590/S1516-89132010000400011.
http://dx.doi.org/10.1590/S1516-89132010...
; Figueiredo et al., 2011FIGUEIREDO, A.B., 2011. Influência de banho de imersão com babosa, Aloe barbadensis (Miller, 1768) sobre os parâmetros hematológicos e Monogenoidea parasites de pacu, Piaractus mesopotamicus (Holmberg,1887). Florianópolis: Universidade Federal de Santa Catarina, 22 p. Trabalho de Conclusão de Curso de Engenharia de Aquicultura.; Carraschi et al., 2014CARRASCHI, S.P., BARBUIO, R., IKEFUTI, C.V., FLORÊNCIO, T., CRUZ, C. and RANZANI-PAIVA, M.J.T., 2014. Effectiveness of therapeutic agents in disease treatment in Piaractus mesopotamicus.Aquaculture (Amsterdam, Netherlands), vol. 431, pp. 124-128. http://dx.doi.org/10.1016/j.aquaculture.2013.12.026.
http://dx.doi.org/10.1016/j.aquaculture....
) studies were conducted. The first monogenoidean found in “pacus” was Anacanthorus penilabiatus Boeger, Husack and Martins, 1995, described in the state of São Paulo and posteriorly reported by Martins et al. (2000)MARTINS, M.L., MORAES, F.R., FUJIMOTO, R.Y., ONAKA, E.M., NOMURA, D.T., SILVA, C.A.H. and SCHALCH, S.H.C., 2000. Parasitic infections in cultivated freshwater fishes a survey of diagnosticated cases from 1993 to 1998. Revista Brasileira de Parasitologia Veterinária, vol. 9, pp. 23-28. in the same region. One year later, Pamplona-Basilio et al. (2001)PAMPLONA-BASILIO, M.C., KOHN, A. and FEITOSA, V.A., 2001. New host records and description of the egg of (Monogenea, Dactylogyridae). Anacanthorus penilabiatusMemorias do Instituto Oswaldo Cruz, vol. 96, no. 5, pp. 667-668. PMid:11500767. http://dx.doi.org/10.1590/S0074-02762001000500014.
http://dx.doi.org/10.1590/S0074-02762001...
presented the descriptions of the egg and reported this species in another host, Colossoma macropomum (Cuvier, 1818). Mymarothecium viatorum Boeger, Piasecki and Sobecka, 2002 was originally described from Piaractus brachypomus (Cuvier, 1818) in Poland and later, it was reported by Cohen and Kohn (2005)COHEN, S.C. and KOHN, A., 2005. A new species of and new hosts and geographical records for M. viatorum (Monogenea: Dactylogyridae) parasites of freshwater fishes in Brazil. MymarotheciumFolia Parasitologica, vol. 52, no. 4, pp. 307-310. PMid:16405294. http://dx.doi.org/10.14411/fp.2005.042.
http://dx.doi.org/10.14411/fp.2005.042...
parasitizing P. mesopotamicus in the state of Ceará, Brazil. Franceschini et al. (2013)FRANCESCHINI, L., ZAGO, A.C., SCHALCH, S.H.C., GARCIA, F., ROMERA, D.M. and SILVA, R., 2013. Parasitic infections of . Piaractus mesopotamicus and hybrid (P. mesopotamicus x Piaractus brachypomus) cultured in BrazilRevista Brasileira de Parasitologia Veterinária, vol. 22, no. 3, pp. 407-414. PMid:24142174. http://dx.doi.org/10.1590/S1984-29612013000300015.
http://dx.doi.org/10.1590/S1984-29612013...
reported findings of A. penilabiatus and M. viatorum in the same host. In 2007, Lizama et al. recorded A. penilabiatus, Anacanthorus spatulathus and Mymarothecium sp. from the same host. Recently, Leão et al. (2015)LEÃO, M.S.L., SÃO CLEMENTE, S.C. and COHEN, S.C., 2015. Anacanthorus toledoensis n. sp. and Mymarothecium ianwhittingtoni n. sp. (Dactylogyridae: Monogenoidea) parasitizing cage-reared (Characiformes, Characidae) in the State of Paraná, Brazil. Piaractus mesopotamicusComparative Parasitology, vol. 82, no. 2, pp. 268-273. http://dx.doi.org/10.1654/4759.1.
http://dx.doi.org/10.1654/4759.1...
described two new species, Anacanthorus toledoensis and Mymarothecium ianwhitingtoni, increasing the diversity of known species of Monogenoidea in P. mesopotamicus. The aim of the present study was to investigate prevalence, mean abundance, mean intensity, parasite distribution pattern and the correlation of prevalence and abundance with the total length of hosts of monogenoidean parasites in P. mesopotamicus farmed in cages in the reservoir of the Itaipu Hydroelectric Power Station, Paraná, Brazil.

2 Material and Methods

In january 2011 (summer season), samples of gills were taken from forty-one P. mesopotamicus that were kept in cages upstream and downstream of the reservoir of the Itaipu Hydroelectric Power Station, Paraná River, state of Paraná, Brazil (24°44’29.0” S; 53°44’51.2” W). During all the cultive period water physical and chemical parameters were measured with portable devices. Dissolved oxygen (Hanna Instruments, model HI9146) and pH (Hanna Instruments, model HI8314) were weekly monitored as the water temperature was monitored daily (mornings and evenings) with a mercury bulb thermometer. The fish were anesthetized with benzocaine at a concentration of 74mg/L and euthanized with benzocaine at a concentration of 250mg/L according to the recommendations of Gomes et al. (2001)GOMES, L.C., CHIPPARI-GOMES, A.R., LOPES, N.P., ROUBACH, R. and ARAUJO-LIMA, C., 2001. Efficacy of benzocaine as an anesthetic in juvenile tambaqui Colossoma macropomum.Journal of the World Aquaculture Society, vol. 32, no. 4, pp. 426-431. http://dx.doi.org/10.1111/j.1749-7345.2001.tb00470.x.
http://dx.doi.org/10.1111/j.1749-7345.20...
,weighed (g), measured (cm) and transported to the laboratory. The gills were removed and placed in vials containing 1:4000 formalin solution and shaken vigorously and the formalin solution of each vial was increased to about 5%. In the laboratory, parasites were collected with the aid of a stereoscopic microscope and were stored in the same fixative. Some specimens were mounted unstained in Hoyer’s mounting medium (Humason, 1979HUMASON, G.L., 1979. Animal tissue techniques. San Francisco: W.H. Freeman and Company.) in order to study the sclerotized parts and the remaining were stained with Gomori’s trichrome, cleared in beechwood creosote and mounted on slides in Canada balsam (Kritsky et al., 1978KRITSKY, D.C., LEIBY, P.D. and KAYTON, R.J., 1978. A rapid stain technique for haptoral bars of species (Monogenea). GyrodactylusThe Journal of Parasitology, vol. 69, no. 1, pp. 862-865. PMid:76672.).

The prevalence (P), mean abundance (MA) and mean intensity (MI) of the parasites were calculated as described by Bush et al. (1997)BUSH, A.O., LAFFERTY, K.D., LOTZ, J.M. and SHOSTAK, A.W., 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology, vol. 83, no. 4, pp. 575-583. PMid:9267395. http://dx.doi.org/10.2307/3284227.
http://dx.doi.org/10.2307/3284227...
.

The index of dispersion (quotient between variance and mean of parasite abundance) and d test were used to determine distribution patterns (Ludwing and Reynolds, 1988LUDWING, J.A. and REYNOLDS, J.F., 1988. Statistical Ecology: a primer methods and Computing. Wiley-Interscience Publications.). Spearman’s rank correlation coefficient (rs) was used to determine possible correlations between host’stotal length and parasite abundance. Pearson’s correlation coefficient (r) was used to determine possible correlations between the host’s total length and the prevalence of parasites, with angular transformation of prevalence values (Zar, 1996ZAR, J.H., 1996. Biostatistical analysis. 3rd ed. Upper Saddle River: Prentice-Hall.). The statistical significance level of p ≤ 0.05 was used.

3 Results and Discussion

The average values for the physical and chemical water parameters measured during the experimental period were 30.4 ± 0.7 °C for temperature; 6.40 ± 0.3 mg/L for dissolved oxygen; 7.1 ± 0.3 for pH; and 0.06 ± 0.03 mg/L for ammonia content (as shown in Table 1). These values are within the recommended range when rearing tropical species (Ostrensky and Boeger, 1998OSTRENSKY, A. and BOEGER, W., 1998. Piscicultura: fundamentos e técnicas de manejo. Guaíba: Agropecuária Ltda.; Urbinati et al., 2010URBINATI, E.C., GONÇALVES, F.D. and TAKAHASHI, L.S., 2010. Pacu (Piaractus mesopotamicus). In: B. BALDISSEROTTO and L.C. GOMES. Espécies nativas para piscicultura no Brasil. Santa Maria: UFSM, pp. 205-244.). Features of the habitat (local abiotic factors such as water temperature, pH and lakesize) and certain traits of the host population like size, could facilitate the transmission and establishment of fish parasites (Bagge et al., 2004BAGGE, A.M., POULIN, R. and VALTONEN, E.T., 2004. Fish population size, and not density, as the determining factor of parasite infection: a case study. Parasitology, vol. 128, no. pt 3, pp. 305-313. PMid:15074879. http://dx.doi.org/10.1017/S0031182003004566.
http://dx.doi.org/10.1017/S0031182003004...
; Takemoto et al., 2005TAKEMOTO, R.M., PAVANELLI, G.C., LIZAMA, M.A.P., LUQUE, J.L. and POULIN, R., 2005. Host density as a major determinat of endoparasite species richness in fishes of floodplain of the upper Parana River, Brazil. Journal of Helminthology, vol. 79, pp. 75-84. PMid:15831117. http://dx.doi.org/10.1079/JOH2004264.
http://dx.doi.org/10.1079/JOH2004264...
; Poulin, 2006POULIN, R., 2006. Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors. International Journal for Parasitology, vol. 36, no. 8, pp. 877-885. PMid:16620823. http://dx.doi.org/10.1016/j.ijpara.2006.02.021.
http://dx.doi.org/10.1016/j.ijpara.2006....
).

Table 1
Values for the physical and chemical water parameters measured during the experimental period.

Forty-one specimens of P. mesopotamicus with mean total weight 1.13 Kg (0.690-1.726 ± 0.264 Kg) and mean total length 35.07 cm (30-41 ± 2.493 cm) were examined for monogenoideans. All the fish examined were parasitized with at least one species of Monogenoidea. Four species were collected: Anacanthorus penilabiatus, Anacanthorus toledoensis, Mymarothecium ianwhitingtoni and Mymarothecium viatorum (as shown in Table 2). A. toledoensis was the species with higher rates of prevalence, mean intensity and mean abundance. The other three species have high rates of prevalence, but low values of mean intensity and mean abundance: A. penilabiatus; M. viatorum; M. ianwhittingtoni.

Table 2
Prevalence (P%), mean intensity (MI), mean abundance (MA) range (R), intensity (I) and confidence interval (CI) of monogenoideans parasites of farmed fish, P. mesopotamicus of the reservoir of the Itaipu Hydroelectric Power Station, Paraná River, state of Paraná, Brazil.

Our results, compared with other studies, showed variations in the mean abundance and mean intensity of monogenoidean (as shown in Table 3). Lizama et al. (2007)LIZAMA, M.A.P., TAKEMOTO, R.M., RANZANI-PAIVA, M.J.T., AYROSA, L.M.S. and PAVANELLI, G.C., 2007. Relação parasito-hospedeiro em peixes de piscicultura da região de Assis, estado de São Paulo, Brasil. 2. Piaractus mesopotamicus (Holmberg, 1887). Acta Scientiarum Biological Sciences, vol. 29, pp. 437-445. http://dx.doi.org/10.4025/actascibiolsci.v29i2.594.
http://dx.doi.org/10.4025/actascibiolsci...
, Tavares-Dias et al. (2008)TAVARES‐DIAS, M., MORAES, F.R. and MARTINS, M.L., 2008. Hematological assessment in four Brazilian teleost fish with parasitic infections collected in feefishing from Franca, São Paulo, Brazil. Boletim do Instituto de Pesca, vol. 34, pp. 189-196., Franceschini et al. (2013)FRANCESCHINI, L., ZAGO, A.C., SCHALCH, S.H.C., GARCIA, F., ROMERA, D.M. and SILVA, R., 2013. Parasitic infections of . Piaractus mesopotamicus and hybrid (P. mesopotamicus x Piaractus brachypomus) cultured in BrazilRevista Brasileira de Parasitologia Veterinária, vol. 22, no. 3, pp. 407-414. PMid:24142174. http://dx.doi.org/10.1590/S1984-29612013000300015.
http://dx.doi.org/10.1590/S1984-29612013...
and Jerônimo et al. (2014)JERÔNIMO, G.T., PÁDUA, S.B., BAMPI, D., GONÇALVES, E.L.T., GARCIA, P., ISHIKAWA, M.M. and MARTINS, M.L., 2014. Haematological and histhological analysis in South American fish Piaractus mesopotamicus parasitized by monogenean (Dactylogyridae). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 74, no. 4, pp. 1000-1006. PMid:25627614. http://dx.doi.org/10.1590/1519-6984.09513.
http://dx.doi.org/10.1590/1519-6984.0951...
reported the prevalence indexes for A. penilabiatus in P. mesopotamicus in fish farming (P = 81.1%; 76%; 77.3%; 100%, respectively) that were similar to what was reported in this study (P = 97.5%), but higher from the studies of Martins and Romero (1996)MARTINS, M.L. and ROMERO, N.G., 1996. Efectos del parasitismo sobre el tejido branquial em peces cultivados: Estudio parasitologico e histopatologico. Revista Brasileira de Zoologia, vol. 13, no. 2, pp. 489-500. http://dx.doi.org/10.1590/S0101-81751996000200017.
http://dx.doi.org/10.1590/S0101-81751996...
and Cohen and Kohn (2009)COHEN, S.C. and KOHN, A., 2009. On Dactylogyridae (Monogenea) of four species of characid fishes from Brazil. Check List, vol. 5, no. 2, pp. 351-356. http://dx.doi.org/10.15560/5.2.351.
http://dx.doi.org/10.15560/5.2.351...
(P = 33.3%; 50%, respectively). Considering mean intensity and mean abundance, Franceschini et al. (2013)FRANCESCHINI, L., ZAGO, A.C., SCHALCH, S.H.C., GARCIA, F., ROMERA, D.M. and SILVA, R., 2013. Parasitic infections of . Piaractus mesopotamicus and hybrid (P. mesopotamicus x Piaractus brachypomus) cultured in BrazilRevista Brasileira de Parasitologia Veterinária, vol. 22, no. 3, pp. 407-414. PMid:24142174. http://dx.doi.org/10.1590/S1984-29612013000300015.
http://dx.doi.org/10.1590/S1984-29612013...
(MI = 22.4; MA = 17.3) and Cohen and Kohn (2009)COHEN, S.C. and KOHN, A., 2009. On Dactylogyridae (Monogenea) of four species of characid fishes from Brazil. Check List, vol. 5, no. 2, pp. 351-356. http://dx.doi.org/10.15560/5.2.351.
http://dx.doi.org/10.15560/5.2.351...
(MI = 23.6; MA = 11.8) demonstrated similar results for A. penilabiatus, while other studies register higher values: (Lizama et al. (2007)LIZAMA, M.A.P., TAKEMOTO, R.M., RANZANI-PAIVA, M.J.T., AYROSA, L.M.S. and PAVANELLI, G.C., 2007. Relação parasito-hospedeiro em peixes de piscicultura da região de Assis, estado de São Paulo, Brasil. 2. Piaractus mesopotamicus (Holmberg, 1887). Acta Scientiarum Biological Sciences, vol. 29, pp. 437-445. http://dx.doi.org/10.4025/actascibiolsci.v29i2.594.
http://dx.doi.org/10.4025/actascibiolsci...
MI = 166,3/ MA = 134,9; Tavares-Dias et al. (2008)TAVARES‐DIAS, M., MORAES, F.R. and MARTINS, M.L., 2008. Hematological assessment in four Brazilian teleost fish with parasitic infections collected in feefishing from Franca, São Paulo, Brazil. Boletim do Instituto de Pesca, vol. 34, pp. 189-196. MI = 2,287.6 and Jerônimo et al. (2014)JERÔNIMO, G.T., PÁDUA, S.B., BAMPI, D., GONÇALVES, E.L.T., GARCIA, P., ISHIKAWA, M.M. and MARTINS, M.L., 2014. Haematological and histhological analysis in South American fish Piaractus mesopotamicus parasitized by monogenean (Dactylogyridae). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 74, no. 4, pp. 1000-1006. PMid:25627614. http://dx.doi.org/10.1590/1519-6984.09513.
http://dx.doi.org/10.1590/1519-6984.0951...
MI=316.3 (cold season); 2,742.3 (hot season) ; MA = 316.3 (cold season); 2,742.3 (hot season).

Table 3
Dispersion index (DI) and d statistical of the monogenoideans parasites of farmed fish, P. mesopotamicus of the reservoir of the Itaipu Hydroelectric Power Station, Paraná River, state of Paraná, Brazil.

The monogenoidean species reported in this study was also present in closely related fish species (as shown in Table 4). A. penilabiatus was reported in P. brachypomus, in hybrids P. mesopotamicus x C. macropomum and in P. mesopotamicus x P. brachypomus (Cohen and Kohn, 2009COHEN, S.C. and KOHN, A., 2009. On Dactylogyridae (Monogenea) of four species of characid fishes from Brazil. Check List, vol. 5, no. 2, pp. 351-356. http://dx.doi.org/10.15560/5.2.351.
http://dx.doi.org/10.15560/5.2.351...
; Tavares-Dias et al., 2008TAVARES‐DIAS, M., MORAES, F.R. and MARTINS, M.L., 2008. Hematological assessment in four Brazilian teleost fish with parasitic infections collected in feefishing from Franca, São Paulo, Brazil. Boletim do Instituto de Pesca, vol. 34, pp. 189-196.; Franceschini et al., 2003). In the studies of Franceschini et al. (2013)FRANCESCHINI, L., ZAGO, A.C., SCHALCH, S.H.C., GARCIA, F., ROMERA, D.M. and SILVA, R., 2013. Parasitic infections of . Piaractus mesopotamicus and hybrid (P. mesopotamicus x Piaractus brachypomus) cultured in BrazilRevista Brasileira de Parasitologia Veterinária, vol. 22, no. 3, pp. 407-414. PMid:24142174. http://dx.doi.org/10.1590/S1984-29612013000300015.
http://dx.doi.org/10.1590/S1984-29612013...
(P. mesopotamicus x P. brachypomus) and Tavares-Dias et al. (2008)TAVARES‐DIAS, M., MORAES, F.R. and MARTINS, M.L., 2008. Hematological assessment in four Brazilian teleost fish with parasitic infections collected in feefishing from Franca, São Paulo, Brazil. Boletim do Instituto de Pesca, vol. 34, pp. 189-196. (P. mesopotamicus x C. macropomum) studies, the prevalence of A. penilabiatus was lower than in the present study. However, the prevalence presented by Cohen and Kohn (2009)COHEN, S.C. and KOHN, A., 2009. On Dactylogyridae (Monogenea) of four species of characid fishes from Brazil. Check List, vol. 5, no. 2, pp. 351-356. http://dx.doi.org/10.15560/5.2.351.
http://dx.doi.org/10.15560/5.2.351...
for P. brachypomus was similar with our results for P. mesopotamicus. Considering the mean intensity, the hybrid examined by Tavares-Dias et al. (2008)TAVARES‐DIAS, M., MORAES, F.R. and MARTINS, M.L., 2008. Hematological assessment in four Brazilian teleost fish with parasitic infections collected in feefishing from Franca, São Paulo, Brazil. Boletim do Instituto de Pesca, vol. 34, pp. 189-196. showed high values than in the present study, while Cohen and Kohn (2009)COHEN, S.C. and KOHN, A., 2009. On Dactylogyridae (Monogenea) of four species of characid fishes from Brazil. Check List, vol. 5, no. 2, pp. 351-356. http://dx.doi.org/10.15560/5.2.351.
http://dx.doi.org/10.15560/5.2.351...
and Franceschini et al. (2013)FRANCESCHINI, L., ZAGO, A.C., SCHALCH, S.H.C., GARCIA, F., ROMERA, D.M. and SILVA, R., 2013. Parasitic infections of . Piaractus mesopotamicus and hybrid (P. mesopotamicus x Piaractus brachypomus) cultured in BrazilRevista Brasileira de Parasitologia Veterinária, vol. 22, no. 3, pp. 407-414. PMid:24142174. http://dx.doi.org/10.1590/S1984-29612013000300015.
http://dx.doi.org/10.1590/S1984-29612013...
found similar values in mean intensity and mean abundance in P. brachypomus and in the hybrid P. mesopotamicus x P. brachypomus, respectively.

Table 4
Values of Spearman’s rank correlation coefficient (rs) and Pearson's correlation coefficient (r) obtained in relations between total length of hosts and abundance and prevalence of monogenoideans parasites of farmed fish, P. mesopotamicus of the reservoir of the Itaipu Hydroelectric Power Station, Paraná River, state of Paraná, Brazil.

In the present investigation, M. viatorum showed values of mean intensity and mean abundance similar to those found by Franceschini et al. (2013)FRANCESCHINI, L., ZAGO, A.C., SCHALCH, S.H.C., GARCIA, F., ROMERA, D.M. and SILVA, R., 2013. Parasitic infections of . Piaractus mesopotamicus and hybrid (P. mesopotamicus x Piaractus brachypomus) cultured in BrazilRevista Brasileira de Parasitologia Veterinária, vol. 22, no. 3, pp. 407-414. PMid:24142174. http://dx.doi.org/10.1590/S1984-29612013000300015.
http://dx.doi.org/10.1590/S1984-29612013...
(MI = 27.5; MA = 19.9), and different from Cohen and Kohn (2009)COHEN, S.C. and KOHN, A., 2009. On Dactylogyridae (Monogenea) of four species of characid fishes from Brazil. Check List, vol. 5, no. 2, pp. 351-356. http://dx.doi.org/10.15560/5.2.351.
http://dx.doi.org/10.15560/5.2.351...
(MI; MA = 277) from P. mesopotamicus.

Regarding the parasitism by M. viatorum on closely related fish of P. mesopotamicus, Cohen and Kohn (2009)COHEN, S.C. and KOHN, A., 2009. On Dactylogyridae (Monogenea) of four species of characid fishes from Brazil. Check List, vol. 5, no. 2, pp. 351-356. http://dx.doi.org/10.15560/5.2.351.
http://dx.doi.org/10.15560/5.2.351...
presented similar prevalence values for parasitism in the host P. brachypomus, however, in the study of Vásques (2014)VÁSQUES, N.Z.D., 2014. Índices parasitários en larvas, post larvas y alevinos de Piaractus brachypomus “Paco” en relación a los factores ambientales, en el centro de investigaciones Quistococha del Instituto de investigaciones de la Amazonia Peruana. Iquitos: Universidad Nacional de la Amazonía Peruana. 79 p. in the same host, these values were lower. Considering mean intensity and mean abundance, the studies of Cohen and Kohn (2009)COHEN, S.C. and KOHN, A., 2009. On Dactylogyridae (Monogenea) of four species of characid fishes from Brazil. Check List, vol. 5, no. 2, pp. 351-356. http://dx.doi.org/10.15560/5.2.351.
http://dx.doi.org/10.15560/5.2.351...
and Vásques (2014)VÁSQUES, N.Z.D., 2014. Índices parasitários en larvas, post larvas y alevinos de Piaractus brachypomus “Paco” en relación a los factores ambientales, en el centro de investigaciones Quistococha del Instituto de investigaciones de la Amazonia Peruana. Iquitos: Universidad Nacional de la Amazonía Peruana. 79 p. showed higher values. The prevalence of M. viatorum in hybrid (P. mesopotamicusx P. brachypomus) presented by Franceschini et al. (2013)FRANCESCHINI, L., ZAGO, A.C., SCHALCH, S.H.C., GARCIA, F., ROMERA, D.M. and SILVA, R., 2013. Parasitic infections of . Piaractus mesopotamicus and hybrid (P. mesopotamicus x Piaractus brachypomus) cultured in BrazilRevista Brasileira de Parasitologia Veterinária, vol. 22, no. 3, pp. 407-414. PMid:24142174. http://dx.doi.org/10.1590/S1984-29612013000300015.
http://dx.doi.org/10.1590/S1984-29612013...
showed similarity, while the mean intensity and mean abundance values were considerably higher than those from the present study. These differences are due to changes in the management of farming systems and susceptibility to infection of cultured individuals. The high indexes in farming mainly occurs due the Monogenoidea have a direct life cycle and their transmission could be facilitated by proximity between hosts (Bagge et al., 2004BAGGE, A.M., POULIN, R. and VALTONEN, E.T., 2004. Fish population size, and not density, as the determining factor of parasite infection: a case study. Parasitology, vol. 128, no. pt 3, pp. 305-313. PMid:15074879. http://dx.doi.org/10.1017/S0031182003004566.
http://dx.doi.org/10.1017/S0031182003004...
). These parasites in man-made environments, like aquaria and fish farms, multiply readily, sometimes killing their hosts (Rubio-Godoy, 2007RUBIO-GODOY, M., 2007. Fish host-monogenean parasite interactions, with special reference to Polyopisthocotylea. In: L.I. TERRAZAS. Advances in the immunology of parasitic deseases. Kerala: Signpost, pp. 91-109.).

All the parasites of P. mesopotamicus showed the typical aggregated pattern of distribution (as shown in Table 5). Our results show that these parasites present the typical aggregated distribution pattern, in conformity with the most common pattern for metazoan parasite populations. Poulin (2013)POULIN, R., 2013. Explaining variability in parasite aggregation levels among host samples. Parasitology, vol. 140, no. 4, pp. 541-546. PMid:23343821. http://dx.doi.org/10.1017/S0031182012002053.
http://dx.doi.org/10.1017/S0031182012002...
pointed that firstly, heterogeneity among host individuals in terms of exposure to parasites, resulting from the uneven distribution of infective stages in space and time relative to hosts, can lead to parasite aggregation. Secondly, heterogeneity in numbers of parasites per host can result from either genetic or acquired variation in susceptibility to infection, arising from differences among hosts in behaviour or immune resistance. More knowledge about parasite and host biology is needed to improve the interpretation of these parasitological patterns, in an ecological framework incorporating pertinent environmental and biological information, as recommended by Marcogliese (2001)MARCOGLIESE, D.J., 2001. Pursuing parasites up the food chain: implications of food web structure and function on parasite communities in aquatic systems. Acta Parasitologica, vol. 46, pp. 82-93..

Table 5
Comparison between the values of prevalence (P%), mean intensity (MI), mean abundance (MA), range (R), total number (n) of monogenoideans parasites of different localities and quality water.

There was no correlation between abundance and total length of the hosts, and between prevalence and total length of the hosts (as shown in Table 6).

Table 6
Prevalence (P), Mean intensity (MI), Mean abundance (MA) and Total number of Anacanthoruspenilabiatus and Mymarothecium viatorum from different parental host species.

According Luque et al. (2003)LUQUE, J.L., ALVES, D.R. and RIBEIRO, R.S., 2003. Community ecology of the metazoan parasites of Banded Croaker, (Osteichthyes: Sciaenidae), from the coastal zone of the State of Rio de Janeiro, Brazil. Paralonchurus brasiliensisActa Scientiarum Biological Sciences, vol. 25, pp. 273-278. http://dx.doi.org/10.4025/actascibiolsci.v25i2.2009.
http://dx.doi.org/10.4025/actascibiolsci...
, the size of the host is not always correlated with prevalence and abundance of parasites. As pointed by Poulin (2000)POULIN, R., 2000. Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical causes. Journal of Fish Biology, vol. 56, no. 1, pp. 123-137. http://dx.doi.org/10.1111/j.1095-8649.2000.tb02090.x.
http://dx.doi.org/10.1111/j.1095-8649.20...
, this pattern cannot be generalized, because in many host-parasite systems the correlation is positive, but weak and non-significant. In the present study, no correlation was observed between the abundance and prevalence of the parasites and the total length of the hosts. This lack of correlation may be related to the low amplitude of the host length classes observed among the specimens examined. In cages this fact could happen frequently because the standardization of fish sizes. Similar results were observed in Plagiocion squamosissimus by Tavernari et al. (2005)TAVERNARI, F.C., BELLAY, S., TAKEMOTO, R.M., GUIDELLI, G.M., LIZAMA, M.A.P. and PAVANELLI, G.C., 2005. Ecological aspects of (Platyhelminthes, Monogenea) parasite of gills of . Diplectanum piscinariusPlagioscion squamosissimus (Osteichthyes, Sciaenidae) in the Upper Paraná River floodplain, BrazilActa Scientiarum, vol. 27, pp. 225-229., who reported that the non existence of correlation of the Monogenoidea number and their prevalence in relation to the size of the hosts might be due to uniformity of parasitism levels in relation to host length classes, along with the situation in which almost all the host samples were adult specimens.

4 Conclusions

This study showed high prevalence results in all the species, although the features of the cages were according recommended range when rearing tropical species. A. toledoensis, was the species with higher rates of prevalence, mean intensity and mean abundance. The other three species have high rates of prevalence, but low values of mean intensity and mean abundance. The Monogenoidea collected in P. mesopotamicus showed the typical aggregated distribution pattern, and the abundance and the prevalence did not shown any correlation with the total length of hosts.

Acknowledgements

We are grateful to the Itaipú Binational Hydroelectric Power Station for letting us examine the fish in their facilities and to the Coordination Office for Improvement of University-level Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nivel Superior) for a doctoral fellowship.

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Publication Dates

  • Publication in this collection
    25 May 2017
  • Date of issue
    Nov 2017

History

  • Received
    11 Jan 2016
  • Accepted
    19 July 2016
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