Coccidiose hepática em <i>Serrasalmus rhombeus</i> Linnaeus, 1766 da Amazônia paraense: aspectos morfológicos e histopatológicos

Oliveira, Jhonata Eduard Farias de; Figueredo, Rayline Thaimenne Alves; Sindeaux-Neto, José Ledamir; Vilhena, Maria do Perpétuo Socorro Progene; Berrêdo, José Francisco; Matos, Edilson; Velasco, Michele

Jhonata Eduard Farias de Oliveira

Programa de Pós-graduação em Aquicultura e Recursos Aquáticos Tropicais, Universidade Federal Rural da Amazônia –UFRA, Belém, PA, Brasil

Rayline Thaimenne Alves Figueredo

Programa de Pós-graduação em Biologia Animal, Universidade Estadual de Campinas – UNICAMP, Campinas, SP, Brasil

José Ledamir Sindeaux-Neto

Laboratório de Pesquisa Carlos Azevedo, Universidade Federal Rural da Amazônia – UFRA, Belém, PA, Brasil

Maria do Perpétuo Socorro Progene Vilhena

Universidade Federal Rural da Amazônia – UFRA, Tomé-Açu, PA, Brasil

José Francisco Berrêdo

Museu Paraense Emílio Goeldi, Belém, PA, Brasil

Edilson Matos

Programa de Pós-graduação em Aquicultura e Recursos Aquáticos Tropicais, Universidade Federal Rural da Amazônia –UFRA, Belém, PA, Brasil

Laboratório de Pesquisa Carlos Azevedo, Universidade Federal Rural da Amazônia – UFRA, Belém, PA, Brasil

Michele Velasco ^**Corresponding author: Michele Velasco Oliveira da Silva. E-mail: michele.velasco.mv@gmail.com

Universidade Federal Rural da Amazônia – UFRA Paragominas, Paragominas, PA, Brasil

https://orcid.org/0000-0002-5642-5361

*Corresponding author: Michele Velasco Oliveira da Silva. E-mail: michele.velasco.mv@gmail.com

Figuras (6)
Tabelas (1)

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Figure 1
Light microscope images of infection by Calyptospora sp. in Serrasalmus rhombeus. A: Clusters of Calyptospora sp. oocysts in the liver; B: The arrowhead indicates sporocysts inside oocysts; C: Highlight of the sporocyst structure, with sporozoites (SZ) and membranous veil (arrowhead).

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Figure 2
Scanning electron microscopy micrographs of Calyptospora sp. in the liver of Serrasalmus rhombeus. A: Oocysts (oc) composed of 4 sporocysts (arrow). B-D: Sporocyst (sp), with emphasis on the suture (s) and sporopods (spp).

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Figure 3
Schematic drawings of the oocyst and sporocyst, respectively. A: Oocyst containing 4 sporocysts, each surrounded by a membranous veil (arrow) and containing two sporozoites (sz); B: Details of the external structure of the sporocysts, with the presence of a suture (s) and sporopods (spp).

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Figure 4
Principal component analysis (PCA). Oocyst length (OL); Sporocyst length (SL); length-to-width ratio of oocyst to sporocyst (L:W).

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Figure 5
Dendogram of similarity. 1– Calyptospora sp.; 2– C. tucunarensis; 3– C. spinosa; 4– C. serrasalmi ¹; 5– C. serrasalmi ²; 6– C. paranaidji; 7– C. gonzaguensis; 8– Calyptospora sp.¹; 9– Calyptospora sp.²; 10– Calyptospora sp.³; 11– Calyptospora sp.⁴

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Figure 6
Histological sections of Serrasalmus rhombeus liver infected by Calyptospora sp. Oocysts (OC) disseminated in the liver tissue close to blood vessels (*), with the presence of fibroblasts (arrowhead) and mononuclear cell infiltrate (I) (6A, C and E). 6B and 6F indicate melanomacrophages (MM) around oocysts. 6D reveals widespread necrosis, liver degeneration (arrowhead), and the presence of red blood cells (*) in microphotographs of ZN stained tissue.

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Table 1
Morphometric comparison of Calyptospora spp. oocysts and sporocysts described in fish species from Brazil.

Species	OD	L:W	Shape	Sporocyst (µm)		CS/IS	References
Species	OD	L:W	Shape	Length	Width	CS/IS	References
Calyptospora sp.	17.4 (1.0)	2.1	Pyriform	8.3 (1.1)	4.3 (0.8)	Pará/Liver	This study
Calyptospora tucunarensis	24.3 (2.1)	2.9	Ellipsoidal	8.3 (1.3)	3.7 (1.1)	Ceará/Liver	(Békési & Molnár, 1991Békési L, Molnár K. Calyptospora tucunarensis n. sp. (Apicomplexa: Sporozoea) from the liver of tucunare Cichla ocellaris in Brazil. Syst Parasitol 1991; 18(2): 127-132. http://dx.doi.org/10.1007/BF00017665. http://dx.doi.org/10.1007/BF00017665... )
Calyptospora spinosa	22.3 (1.6)	2.4	Ellipsoidal	9.3 (0.4)	3.8 (0.4)	Pará/Liver, Gonads and ovary.	(Azevedo et al., 1993Azevedo C, Matos P, Matos E. Morphological data of Calyptospora spinosa n. sp. (Apicomplexa, Calyptosporidae) parasite of Crenicichla lepidota Heckel, 1840 (Teleostei) from Amazon River. Eur J Protistol 1993; 29(2): 171-175. http://dx.doi.org/10.1016/S0932-4739(11)80270-1. PMid:23195539. https://doi.org/10.1016/S0932-4739(11)80... )
Calyptospora serrasalmi ¹	23.5 (2.1)	2.2	Pyriform	10.7 (1.1)	5.5 (0.5)	Amazonas and Pernambuco/Liver	(Cheung et al., 1986Cheung PJ, Nigrelli RF, Ruggieri GD. Calyptospora serrasalmi sp. nov. (Coccidia: Calyptosporidae) from liver of the black piranha, Serrasalmus niger Schomburgk. J Aquaricult Aquat Sci 1986; 4(3): 54-57.)
Calyptospora serrasalmi²	25.4 (0.6)	2.2	Pyriform	11.7 (1)	5.9 (0.4)	Pará/Liver	(Casal et al., 2007Casal G, Padovan I, Matos E, Padovan P, Matos P, Guimarães A, et al. Morphological and ultrastructural redescription of Calyptospora serrasalmi Cheung, Nigrelli & Ruggieri, 1986 (Apicomplexa: Calyptosporidae), a parasite found in two new host species of the genus Serrasalmus. Braz J Morphol Sci 2007; 101(1): 11-16.)
Calyptospora paranaidji	22.1 (1.5)	2.3	Pyriform	9.7 (0.5)	4.6 (0.6)	Maranhão/Liver	(Da Silva et al., 2019Da Silva MF, Da Silva DT, Giese EG, Hamoy IG, Matos E. Morphology and Phylogeny of Calyptospora paranaidji n. sp. (Eimeriorina: Calyptosporidae), an Apicomplexan Parasite of the Hepatic Tissue of Cichla piquiti Kullander & Ferreira, 2006, From a Reservoir in the Brazilian Amazon Region. J Eukaryot Microbiol 2019; 66(4): 608-616. http://dx.doi.org/10.1111/jeu.12707. PMid:30548108. https://doi.org/10.1111/jeu.12707... )
Calyptospora gonzaguensis	19.6 (1.4)	2.1	Pyriform	9.2 (0.6)	3.9 (0.2)	Maranhão/Liver, gall bladder and fatty tissue	(Silva et al., 2020Silva MF, Orlanda JFF, Aráujo-Costa MJ, Hamoy I, Matos E. Hepatic coccidiosis in Triportheus angulatus Spix & Agassiz, 1829 (Characiformes: Triportheidae), a tropical fish from the eastern Brazilian Amazon, with the description of a new species of Calyptospora (Apicomplexa: Calyptosporidae). J Eukaryot Microbiol 2020; 67(3): 352-358. http://dx.doi.org/10.1111/jeu.12785. PMid:31943507. http://dx.doi.org/10.1111/jeu.12785... )
Calyptospora sp. 1	20.8	2.3	Pyriform	8.9	4.1	Pará/Liver	(Silva et al., 2012Silva MC, Clemente SCS, Júnior JAP, Silva MVO, Matos ER. Calyptospora sp. in Brachyplatystoma vaillantii trapped at the Vigia, State of Pará, Brazil. Rev Bras Parasitol Vet 2012; 21(2): 176-178. http://dx.doi.org/10.1590/S1984-29612012000200020. PMid:22832762. http://dx.doi.org/10.1590/S1984-29612012... )
Calyptospora sp. 2	24.5	2.1	Ellipsoidal	11.5	4.5	Minas Gerais /Liver and Intestines	(Albuquerque & Brasil-Sato, 2010Albuquerque MC, Brasil-Sato MC. First report of Calyptospora sp. (Apicomplexa, Calyptosporidae) in forage characid fish from the Três Marias Reservoir, São Francisco Basin, Brazil. Eur J Protistol 2010; 46(2): 150-152. http://dx.doi.org/10.1016/j.ejop.2009.12.005. PMid:20163938. http://dx.doi.org/10.1016/j.ejop.2009.12... )
Calyptospora sp. 3	21.2	2.3	Pyriform	9.2	3.1	Manaus/ Hepatopancreas	(Santiago et al., 2012Santiago H, Corrêa JL, Tortelly R, Menezes RC, Matos P, Matos E. Morphology and histopathology of Calyptospora sp. (Apicomplexa: Calyptosporidae) in speckled peacock bass, Cichla temensis Humboldt, 1821 (Perciformes: Cichlidae), from the Marajó-Açu River, Marajó Island, Brazil. Parasitol Res 2012; 110(6): 2569-2572. http://dx.doi.org/10.1007/s00436-011-2770-0. PMid:22200958. http://dx.doi.org/10.1007/s00436-011-277... )
Calyptospora sp. 4	19.0	2.1	Pyriform	9	4	Brazil/ Liver	(Bonar et al., 2006Bonar CJ, Poynton SH, Schulman FY, Rietcheck RL, Garner MM. Hepatic Calyptospora sp. (Apicomplexa) infection in a wild-born, aquarium-held clutch of juvenile arapaima Arapaima gigas (Osteoglossidae). Dis Aquat Organ 2006; 70(1-2): 81-92. http://dx.doi.org/10.3354/dao070081. PMid:16875394. http://dx.doi.org/10.3354/dao070081... )

[1] *Corresponding author: Michele Velasco Oliveira da Silva. E-mail: michele.velasco.mv@gmail.com

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Coccidiose hepática em Serrasalmus rhombeus Linnaeus, 1766 da Amazônia paraense: aspectos morfológicos e histopatológicos

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