Influence of ectoparasites on hematological parameters of wild and cultured dusky grouper from Southeastern Brazil
Keywords:
Epinephelus marginatus, blood, parasites, Pseudorhabdosynochus, NeobenedeniaAbstract
This study evaluated the occurrence of ectoparasites and its influence on the blood parameters of wild and cultured dusky grouper Epinephelus marginatus from Southeastern Brazil. Hematological and parasitological analyses were made on 147 groupers, obtained from wild (n = 73) and aquaculture origins (n = 74), during cold (n = 70) and hot (n= 77) seasons between July 2009 and June 2010. Two species of ectoparasites were identified: Pseudorhabdosynochus beverleyburtonae (Monogenea: Diplectanidae) on the gills and Neobenedenia melleni (Monogenea: Capsalidae) on the body surface of the fish. Positive and negative correlations between mean abundances of N. melleni and P. beverleyburtonae, respectively, with red blood cells were observed in fish from both origins during hot season. Positive correlations between mean abundances of P. beverleyburtonae and thrombocytes in fish from both origins and negative correlations between mean abundance of N. melleni in cultured fish and thrombocytes were observed during hot season. Also during hot season, positive correlations between total count of white blood cells and mean abundance of N. melleni in cultured fish were found. This study demonstrates that parasitism by N. melleni and P. beverleyburtonae had influence on hematological parameters of wild and cultured dusky grouper E. marginatus in Southeastern Brazil.
References
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BUSH A.O.; LFFERTY K.D.; JEFFREY M.I.; SHOSTAK A.W. 1997 Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83(4): 575-583.
CARNEVIA, D. 1993 Enfermedades de los peces ornamentales. Bucuresti: Agrovet. S.A. 319p.
EIRAS, J.C.; TAKEMOTO, R.M.; PAVANELLI, G.C. 2006. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. Maringá: Eduem. 199 p.
FUJIMOTO, R.Y.; SANTANA, C.A.; CARVALHO, W.L.C.; DINIZ, D.G.; BARROS, Z.M.N.; VARELLA, J.E.A.; GUIMARíES, M.D.F. 2009 Hematologia e parasitas metazoários de camurim (Centropomus undecimalis, Bloch, 1792) na região bragantina, Bragança-Pará. Boletim do Instituto de Pesca, 35(3): 441-450.
GHIRALDELLI, L.; MARTINS, M.L.; YAMASHITA, M.M.; JERÔNIMO, G.T. 2006 Hematologia de Oreochromis niloticus (Cichlidae) e Cyprinus carpio (Cyprinidae) mantidos em diferentes condições de manejo e alimentação no Estado de Santa Catarina, Brasil. Acta Scientiarum. Biological Sciences, 28(4): 319-325.
GOLDENFARB, P.B.; BOWYER, F.P.; HALL, E.; BROSIUS, E. 1971 Reproductibility in the hematology laboratory: the microhematocrit determination. American Journal of Clinical Pathology, 56(1): 35-39.
GUITANG, W. 1998 Changes in blood cells of Tiger puffer Takifugu rubripes caused by infection with the monogenean Heterobothrium okamotoi. Acta Hydrobiologica Sinica, 22: 83-88.
GUL, B.Y.; GAO, Z.X.; QIAN, X.Q.; WANG, W.M. 2011 Haematological and serum biochemical
characterization and comparison of wild and cultured northern snakehead (Channa argus
Cantor, 1842). Journal of Applied Ichthyology,27(1): 122-128.
HIRAZAWA, N.; TAKANO, R.; HAGIWARA, H.;NOGUCHI, M.; NARITA, M. 2010 The influence
of different water temperatures on Neobenedenia girellae (Monogenea) infection, parasite growth, egg production and emerging second generation on amberjack Seriola dumerili (Carangidae) and the histopathological effect of this parasite on fish skin. Aquaculture, 299(1-4): 2-7.
ISHIKAWA, N.M.; RANZANI-PAIVA, M.J.T.; LOMBARDI, J.V. 2008 Metodologia para quantificação de leucócitos totais em peixe, Oreochromis niloticus. Archives of Veterinary Science, 13(1): 54-63.
IWAMA, G. and NAKANISHI, T. 1996 The fish immune system. California: Academic Press. 379p.
JAHN, TL. and KUHN, LR. 1932 The life history of Epibdella melleni Maccallum, 1927, a monogenetic trematode parasitic on marine fishes. Biological Bulletin, 62(1): 89-111.
JERÔNIMO, G.T.; SPECK, G.M.; GONí"¡ALVES, E.L.T.; MARTINS, M.L. 2011 Seasonal variation on the parasitic communities of Nile Tilapia cultured in three regions in Southern Brazil. Brazilian Journal of Biology, 71(2): 1-9.
KEARN, G.C.; OGAWA, K.; MAENO, Y. 1992 Hatching patterns of the monogenean parasites
Benedenia seriolae and Heteraxine heterocerca from the skin and gills, respectively, of the same host fish, Seriola quinqueradiata. Zoological Science, 9:451-455.
KOZINSKA, A.; ANTYCHOWICZ, J.; KOSTRZEWA, P. 1999 Relationship between the thrombocyte
activity and the susceptibility of the carp (Cyprinus carpio l.) to Aeromonas hydrophila infection in different seasons. Bulletin of the Veterinary Institute in Pulawy, 43(1): 63-69.
LECKLIN, T. and NIKINMAA, M. 1998 Erythropoiesis in Arctic charr is not stimulated by anaemia.
Journal of Fish Biology, 53(6): 1169í 1177.
MARTINS, M.L.; TAVARES-DIAS, M.; FUJIMOTO, R.Y.; ONAKA, E.M.; NOMURA, D.T. 2004 Haematological alterations of Leporinus macrocephalus (Osteichthyes: Anostomidae)naturally infected by Goezia leporini (Nematoda: Anisakidae) in fish pond. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 56(5): 640-646.
MORAES, F.R. and MARTINS, M.L. 2004 Condições predisponentes e principais enfermidades de
teleósteos em piscicultura intensiva. In: CYRINO, J.E.P.; URBINATI, E.C.; FRACALOSSI,D.M.; CASTAGNOLLI, N. (eds). Tópicos especiais em piscicultura de água doce tropical intensiva. São Paulo: TecArt. p.343-383.
PEDDIE, S.; ZOU, J.; SECOMBES, C.J. 2002 Immunostimulation in the rainbow trout (Oncorhynchus mykiss) following intraperitoneal administration of Ergosan. Veterinary Immunology and Immunopathology, 86(1-2): 101-113.
PICKERING, A.D. 1986 Changes in blood cell composition of the brown trout, Salmo trutta L.,
during the spawning season. Journal of Fish Biology, 29(3): 335-347.
RANZANI- PAIVA, M.J. and GODINHO, H.M. 1983 Sobre células sanguíneas e contagem diferencial
de leucócitos e eritroblastos em curimbatá,Prochilodus scrofa Steindachner, 1881 (Osteichthyes, Cypriniforms, Prochilodontidae). Revista Brasileira de Biologia, 43(3): 331-338.
RANZANI-PAIVA, M.J.T. and SILVA-SOUZA, A.T. 2004 Hematologia de Peixes Brasileiros. In: RANZANI-PAIVA, M.J.T.; TAKEMOTO, R.M.; LIZAMA, M.L.A.P. (eds). Sanidade de Organismos
Aquáticos. p.89-120.
RANZANI-PAIVA, M.J.T.; SANTOS, A.A.; DIAS, D.C.; SERIANI, R.; EGAMI, M.I. 2008
Hematological and phagocytic response of the fat snook, Centropomus parallelus, reared in net
cages, before and after inoculation with Sacharomyces ceresivisiae. Bioikos, 22(1): 29-35.
REICZIGEL, J. and RÓZSA, L. 2005 Quantitative Parasitology 3.0., Budapest, Hungary, Available
at: <http://www.zoologia.hu/qp/qp.html>Access on: Aug. 02. 2011.
ROSENFELD, G. 1947 Corante pancrômico para hematologia e citologia clínica. Nova combinação dos componentes do MayGrünwald e do giemsa num só corante de emprego rápido. Memória do Instituto Butantan, 20: 329-334.
SANTOS, C.P.; BUCHMANN, K.; GIBSON, D.I. 2000 Pseudorhabdosynochus spp. (Monogenea: Diplectanidae) from the gills of Epinephelus spp. in Brazilian waters. Systematic Parasitology, 45(2):145-153.
SILVEIRA, R. and FAJER, E. 1988 Influencia de los ectoparásitos presentes en Oreochromis aureus en cultivo intensivo sobre el conteo diferencial de las células sanguíneas. Boletín Técnico de
Acuicultura, n. 6, 10p.
SOPINSKA, A. 1984 Effect of physiological factors, stress, and disease on hematological parameters of carp, with a particular reference to leukocyte pattern. II. Hematological results of stress in carp. Acta Ichthyologica et Piscatoria, 14(1-2): 121-139.
TAVARES-DIAS, M. and FAUSTINO, C.D. 1998 Parí¢metros hematológicos da tilápia-do-Nilo
Oreochromis niloticus (Cichlidae) em cultivo extensivo. Ars Veterinária, 14(3): 254-263.
TAVARES-DIAS, M. and MORAES, F.R. 2004 Hematologia de peixes teleósteos. Ribeirão Preto:
Villimpress. 144 p.
TAVARES-DIAS, M.; SCHALCH, S.H.C.; MARTINS,M.L.; SILVA, E.D.; MORAES, F.R.; PERECIN, D.
1999 Hematologia de teleósteos brasileiros com infecção parasitária. I. Variáveis do Leporinus
macrocephalus Garavelo e Britski, 1988 (Anostomidae) e Piaractus mesopotamicus
Holmberg, 1887 (Characidae). Acta Scientiarum, 21(2): 337-342.
TAVARES-DIAS, M.; SCHALCH, S.H.C.; MARTINS, M.L.; ONAKAI, E.M.; MORAES, F.R. 2000
Haematological characteristics of Brazilian Teleosts: III. Parameters of the hybrid tambacu
(Piaractus mesopotamicus Holmberg x Colossoma macropomum Cuvier) (Osteichthyes, Characidae).Revista Brasileira de Zoologia, 17(4): 899-906.
TAVARES-DIAS, M.; BARCELLOS, J.F.M.;MARCON, J.L.; MENEZES, G.C.; ONO, E.A.;AFFONSO, E.G. 2007 Hematological and biochemical parameters for the pirarucu Arapaima gigas Schinz, 1822 (Osteoglossiformes,Arapaimatidae) in net cage culture. Electronic Journal of Ichthyology, 2: 61-68.
WHITTINGTON, I.D. and KEARN, G.C. 2011 Hatching strategies in monogenean
(Platyhelminth) parasites that facilitate host infection. Integrative and Comparative Biology,
51(1): 91-99.
WHITTINGTON, I.D. and HORTON, M.A. 1996 A revision of Neobenedenia Yamaguti, 1963
(Monogenea: Capsalidae) including a redescription of N. melleni (MacCallum, 1927)Yamaguti, 1963. Journal of Natural History, 30(8): 1113-1156.
YAMAGUTI, S. 1965 New monogenetic trematodes from Hawaiian fishes, I. Pacific Science, 19(1): 55-95.
ZHOU, X.; LI, M.; ABBAS, K.; WANG, W. 2009 Comparison of haematology and serum biochemistry of cultured and wild Dojo loach Misgurnus anguillicaudatus. Fish Physiology and Biochemistry, 35(3): 435-441.
Immunology, 2(3): 159-171.
BUSH A.O.; LFFERTY K.D.; JEFFREY M.I.; SHOSTAK A.W. 1997 Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83(4): 575-583.
CARNEVIA, D. 1993 Enfermedades de los peces ornamentales. Bucuresti: Agrovet. S.A. 319p.
EIRAS, J.C.; TAKEMOTO, R.M.; PAVANELLI, G.C. 2006. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. Maringá: Eduem. 199 p.
FUJIMOTO, R.Y.; SANTANA, C.A.; CARVALHO, W.L.C.; DINIZ, D.G.; BARROS, Z.M.N.; VARELLA, J.E.A.; GUIMARíES, M.D.F. 2009 Hematologia e parasitas metazoários de camurim (Centropomus undecimalis, Bloch, 1792) na região bragantina, Bragança-Pará. Boletim do Instituto de Pesca, 35(3): 441-450.
GHIRALDELLI, L.; MARTINS, M.L.; YAMASHITA, M.M.; JERÔNIMO, G.T. 2006 Hematologia de Oreochromis niloticus (Cichlidae) e Cyprinus carpio (Cyprinidae) mantidos em diferentes condições de manejo e alimentação no Estado de Santa Catarina, Brasil. Acta Scientiarum. Biological Sciences, 28(4): 319-325.
GOLDENFARB, P.B.; BOWYER, F.P.; HALL, E.; BROSIUS, E. 1971 Reproductibility in the hematology laboratory: the microhematocrit determination. American Journal of Clinical Pathology, 56(1): 35-39.
GUITANG, W. 1998 Changes in blood cells of Tiger puffer Takifugu rubripes caused by infection with the monogenean Heterobothrium okamotoi. Acta Hydrobiologica Sinica, 22: 83-88.
GUL, B.Y.; GAO, Z.X.; QIAN, X.Q.; WANG, W.M. 2011 Haematological and serum biochemical
characterization and comparison of wild and cultured northern snakehead (Channa argus
Cantor, 1842). Journal of Applied Ichthyology,27(1): 122-128.
HIRAZAWA, N.; TAKANO, R.; HAGIWARA, H.;NOGUCHI, M.; NARITA, M. 2010 The influence
of different water temperatures on Neobenedenia girellae (Monogenea) infection, parasite growth, egg production and emerging second generation on amberjack Seriola dumerili (Carangidae) and the histopathological effect of this parasite on fish skin. Aquaculture, 299(1-4): 2-7.
ISHIKAWA, N.M.; RANZANI-PAIVA, M.J.T.; LOMBARDI, J.V. 2008 Metodologia para quantificação de leucócitos totais em peixe, Oreochromis niloticus. Archives of Veterinary Science, 13(1): 54-63.
IWAMA, G. and NAKANISHI, T. 1996 The fish immune system. California: Academic Press. 379p.
JAHN, TL. and KUHN, LR. 1932 The life history of Epibdella melleni Maccallum, 1927, a monogenetic trematode parasitic on marine fishes. Biological Bulletin, 62(1): 89-111.
JERÔNIMO, G.T.; SPECK, G.M.; GONí"¡ALVES, E.L.T.; MARTINS, M.L. 2011 Seasonal variation on the parasitic communities of Nile Tilapia cultured in three regions in Southern Brazil. Brazilian Journal of Biology, 71(2): 1-9.
KEARN, G.C.; OGAWA, K.; MAENO, Y. 1992 Hatching patterns of the monogenean parasites
Benedenia seriolae and Heteraxine heterocerca from the skin and gills, respectively, of the same host fish, Seriola quinqueradiata. Zoological Science, 9:451-455.
KOZINSKA, A.; ANTYCHOWICZ, J.; KOSTRZEWA, P. 1999 Relationship between the thrombocyte
activity and the susceptibility of the carp (Cyprinus carpio l.) to Aeromonas hydrophila infection in different seasons. Bulletin of the Veterinary Institute in Pulawy, 43(1): 63-69.
LECKLIN, T. and NIKINMAA, M. 1998 Erythropoiesis in Arctic charr is not stimulated by anaemia.
Journal of Fish Biology, 53(6): 1169í 1177.
MARTINS, M.L.; TAVARES-DIAS, M.; FUJIMOTO, R.Y.; ONAKA, E.M.; NOMURA, D.T. 2004 Haematological alterations of Leporinus macrocephalus (Osteichthyes: Anostomidae)naturally infected by Goezia leporini (Nematoda: Anisakidae) in fish pond. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 56(5): 640-646.
MORAES, F.R. and MARTINS, M.L. 2004 Condições predisponentes e principais enfermidades de
teleósteos em piscicultura intensiva. In: CYRINO, J.E.P.; URBINATI, E.C.; FRACALOSSI,D.M.; CASTAGNOLLI, N. (eds). Tópicos especiais em piscicultura de água doce tropical intensiva. São Paulo: TecArt. p.343-383.
PEDDIE, S.; ZOU, J.; SECOMBES, C.J. 2002 Immunostimulation in the rainbow trout (Oncorhynchus mykiss) following intraperitoneal administration of Ergosan. Veterinary Immunology and Immunopathology, 86(1-2): 101-113.
PICKERING, A.D. 1986 Changes in blood cell composition of the brown trout, Salmo trutta L.,
during the spawning season. Journal of Fish Biology, 29(3): 335-347.
RANZANI- PAIVA, M.J. and GODINHO, H.M. 1983 Sobre células sanguíneas e contagem diferencial
de leucócitos e eritroblastos em curimbatá,Prochilodus scrofa Steindachner, 1881 (Osteichthyes, Cypriniforms, Prochilodontidae). Revista Brasileira de Biologia, 43(3): 331-338.
RANZANI-PAIVA, M.J.T. and SILVA-SOUZA, A.T. 2004 Hematologia de Peixes Brasileiros. In: RANZANI-PAIVA, M.J.T.; TAKEMOTO, R.M.; LIZAMA, M.L.A.P. (eds). Sanidade de Organismos
Aquáticos. p.89-120.
RANZANI-PAIVA, M.J.T.; SANTOS, A.A.; DIAS, D.C.; SERIANI, R.; EGAMI, M.I. 2008
Hematological and phagocytic response of the fat snook, Centropomus parallelus, reared in net
cages, before and after inoculation with Sacharomyces ceresivisiae. Bioikos, 22(1): 29-35.
REICZIGEL, J. and RÓZSA, L. 2005 Quantitative Parasitology 3.0., Budapest, Hungary, Available
at: <http://www.zoologia.hu/qp/qp.html>Access on: Aug. 02. 2011.
ROSENFELD, G. 1947 Corante pancrômico para hematologia e citologia clínica. Nova combinação dos componentes do MayGrünwald e do giemsa num só corante de emprego rápido. Memória do Instituto Butantan, 20: 329-334.
SANTOS, C.P.; BUCHMANN, K.; GIBSON, D.I. 2000 Pseudorhabdosynochus spp. (Monogenea: Diplectanidae) from the gills of Epinephelus spp. in Brazilian waters. Systematic Parasitology, 45(2):145-153.
SILVEIRA, R. and FAJER, E. 1988 Influencia de los ectoparásitos presentes en Oreochromis aureus en cultivo intensivo sobre el conteo diferencial de las células sanguíneas. Boletín Técnico de
Acuicultura, n. 6, 10p.
SOPINSKA, A. 1984 Effect of physiological factors, stress, and disease on hematological parameters of carp, with a particular reference to leukocyte pattern. II. Hematological results of stress in carp. Acta Ichthyologica et Piscatoria, 14(1-2): 121-139.
TAVARES-DIAS, M. and FAUSTINO, C.D. 1998 Parí¢metros hematológicos da tilápia-do-Nilo
Oreochromis niloticus (Cichlidae) em cultivo extensivo. Ars Veterinária, 14(3): 254-263.
TAVARES-DIAS, M. and MORAES, F.R. 2004 Hematologia de peixes teleósteos. Ribeirão Preto:
Villimpress. 144 p.
TAVARES-DIAS, M.; SCHALCH, S.H.C.; MARTINS,M.L.; SILVA, E.D.; MORAES, F.R.; PERECIN, D.
1999 Hematologia de teleósteos brasileiros com infecção parasitária. I. Variáveis do Leporinus
macrocephalus Garavelo e Britski, 1988 (Anostomidae) e Piaractus mesopotamicus
Holmberg, 1887 (Characidae). Acta Scientiarum, 21(2): 337-342.
TAVARES-DIAS, M.; SCHALCH, S.H.C.; MARTINS, M.L.; ONAKAI, E.M.; MORAES, F.R. 2000
Haematological characteristics of Brazilian Teleosts: III. Parameters of the hybrid tambacu
(Piaractus mesopotamicus Holmberg x Colossoma macropomum Cuvier) (Osteichthyes, Characidae).Revista Brasileira de Zoologia, 17(4): 899-906.
TAVARES-DIAS, M.; BARCELLOS, J.F.M.;MARCON, J.L.; MENEZES, G.C.; ONO, E.A.;AFFONSO, E.G. 2007 Hematological and biochemical parameters for the pirarucu Arapaima gigas Schinz, 1822 (Osteoglossiformes,Arapaimatidae) in net cage culture. Electronic Journal of Ichthyology, 2: 61-68.
WHITTINGTON, I.D. and KEARN, G.C. 2011 Hatching strategies in monogenean
(Platyhelminth) parasites that facilitate host infection. Integrative and Comparative Biology,
51(1): 91-99.
WHITTINGTON, I.D. and HORTON, M.A. 1996 A revision of Neobenedenia Yamaguti, 1963
(Monogenea: Capsalidae) including a redescription of N. melleni (MacCallum, 1927)Yamaguti, 1963. Journal of Natural History, 30(8): 1113-1156.
YAMAGUTI, S. 1965 New monogenetic trematodes from Hawaiian fishes, I. Pacific Science, 19(1): 55-95.
ZHOU, X.; LI, M.; ABBAS, K.; WANG, W. 2009 Comparison of haematology and serum biochemistry of cultured and wild Dojo loach Misgurnus anguillicaudatus. Fish Physiology and Biochemistry, 35(3): 435-441.
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2018-11-18
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