ISSN 2318-9673 r1.ufrrj.br/lcc/Coccidia

The ruby-crowned Tachyphonus coronatus Vieillot (Passeri- formes: Thraupidae): a new host for Isospora navarroi Berto, Flau- sino, Luz, Ferreira, Lopes, 2009 (Apicomplexa: Eimeriidae)

Bruno do Bomfim Lopes | Bruno Pereira Berto | Hermes Ribeiro Luz | Gideão da Silva Galvão | Ildemar Ferreira | Carlos Wilson Gomes Lopes

Submetido em 13.08.2013 Aceito em 21.08.2013

Abstract Lopes BB, Berto BP, Luz HR, Gal- Resumo Este estudo relata tiês-pretos Tachy- vão GS, Lopes CWG. 2013. The ruby- phonus coronatus Vieillot parasitados por crowned tanager Tachyphonus coronatus Isospora navarroi Berto, Flausino, Luz, Fer- Vieillot (Passeriformes: Thraupidae): a reira, Lopes, 2009. Este coccídio foi original- new host for Isospora navarroi Berto, Flau- mente descrita parasitando o tiê-sangue Ram- sino, Luz, Ferreira, Lopes, 2009 (Apicom- phocelus bresilius dorsalis Sclater e, posteri- plexa: Eimeriidae). [O tiê-preto Tachypho- ormente, o sanhaço-do-coqueiro Thraupis nus coronatus Vieillot (Passeriformes: Thrau- palmarum Wied, no entanto, nunca foi descri- pidae): Um novo hospedeiro para Isospora to em outros hospedeiros. Seus oocistos são navarroi Berto, Flausino, Luz, Ferreira, Lo- esféricos a sub-esféricos, 21.0 × 20.6 µm, com pes, 2009 (Apicomplexa: Eimeriidae)] Cocci- parede dupla e lisa. Micrópila, resíduo e grâ- dia 1, 2-5. Departamento de Biologia , nulo polar estão ausentes. Os esporocistos são Instituto de Biologia, Universidade Federal elipsoidais, 15.2 × 9.3 µm. O corpo de Stieda Rural do Rio de Janeiro. BR-465 km 7, é achatado e o corpo substieda é pequeno e 23897-970 Seropédica, RJ, Brasil. E-mail: delicado. O resíduo do esporocisto é compos- [email protected] to de grânulos dispersos, que, algumas vezes, This study report ruby-crowned Ta- formam um anel. Os esporozoítos são vermi- chyphonus coronatus Vieillot parasitized by formes, com corpo refrátil posterior robusto Isospora navarroi Berto, Flausino, Luz, Fer- reira, Lopes, 2009. This coccidium was origi- BB Lopes nally described parasitizing the Brazilian ta- Biólogo Autônomo associado ao Laboratório de nager Ramphocelus bresilius dorsalis Sclater Coccídios e Coccidioses, Universidade Federal and thereafter from the palm tanager Thraupis Rural do Rio de Janeiro (UFRRJ). E-mail: [email protected] palmarum Wied; however it has never been described in other hosts. Its oocysts are spher- BP Berto  | I Ferreira ical to subspherical, 21.0 × 20.6 µm, with a Departamento de Biologia Animal, Instituto de smooth, bilayered wall. Micropyle, oocyst Biologia, UFRRJ, BR-465 km 7, 23897-970 Sero- residuum and polar granule were absent. The pédica, RJ, Brasil. E-mail: [email protected] sporocysts are ellipsoidal, 15.2 × 9.3 µm. The [email protected] Stieda body is flattened and the substieda body is small and delicate. The sporocyst HR Luz | GS Galvão residuum is composed of scattered granules, Curso de Pós-Graduação em Ciências Veteriná- which sometimes, turns into a ring form. The rias, UFRRJ. E-mail: [email protected] sporozoites are vermiform, with a robust and [email protected] elongate posterior refractile body. CWG Lopes Keywords Morphology, sporulated oocysts, Departamento de Parasitologia Animal, Instituto de Veterinária, UFRRJ. CNPq fellowship. Coccidia, Thraupidae, Passeriformes, Maram- E-mail: [email protected] baia Island.

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Lopes et al. e alongado. Universidade Federal do Rio de Janeiro. Sam- ples were placed in a thin layer (c.5 mm) of Palavras-chave Morfologia, oocistos esporu- K2Cr2O7 2.5% solution in Petri plates and lados, Coccidia, Thraupidae, Passeriformes, incubated at 23-28°C for 10 days or until 70% Ilha da Marambaia. of the oocysts were sporulated. Oocysts were recovered by flotation in Sheather’s sugar Introduction solution (S.G. 1.20) and examined micro- scopically using the technique described by The ruby-crowned tanager Tachyphonus Duszynski & Wilber (1997). Morphological coronatus Vieillot is an endemic thraupid observations and measurements, given in mi- from South America. It habits in Argentina, crometers (ìm), were made using a Carl Zeiss Brazil and Paraguay. Its distribution and eco- binocular microscope with an apochromatic logical niches are similar to the others tana- oil immersion objective lens and an ocular gers, as the Brazilian tanager Ramphocelus micrometer (K-15X PZO, Poland). Line draw- bresilius dorsalis Sclater and the palm tanager ings were prepared using a Wild M-20 bin- Thraupis palmarum Wied (Sick 1997, CBRO ocular microscope with a drawing tube. Pho- 2011, IUCN 2013). tomicrographs were taken using a digital cam- Recently, some coccidian parasites were era (Sony CD Mavica MVC-CD250). Size reported from on the Marambaia island. ranges are shown in parenthesis followed by From thraupids, six Isospora Schneider, 1881 average and shape index (L/W ratio). were recorded: (1) Isospora tiesangui Berto, Flausino, Luz, Ferreira, Lopes, 2008; (2) Isos- Results and discussion pora marambaiensis Berto, Flausino, Luz, Ferreira, Lopes, 2008; (3) Isospora sepetiben- Four ruby-crowned tanagers were exam- sis Berto, Flausino, Luz, Ferreira, Lopes, ined; being that one was positive for coccidia. 2008; (4) Isospora cadimi Berto, Flausino, Initially, the oocysts were nonsporulated, Luz, Ferreira, Lopes, 2009; (5) Isospora na- while 70% sporulated by day three. varroi Berto, Flausino, Luz, Ferreira, Lopes, The identified oocysts (Fig. 1) were 2009 and (6) Isospora ramphoceli Berto, spherical to subspherical, 21.0 (20-22) × 20.6 Flausino, Luz, Ferreira, Lopes, 2010. All (20-21) µm, with shape-index of 1.02. Oocyst these species were described from the Brazil- wall bi-layered and smooth, 1.1μm. Micro- ian tanager R.b. dorsalis (Berto et al. 2008, pyle, oocyst residuum and polar granule are 2009, 2010a); however, I. tiesangui was re- absent. Sporocysts ellipsoidal, 15.2 (15-16) × ported from the palm tanager T. palmarum 9.3 (9-10) µm, with shape-index of with 1.63. and blue dacnis Dacnis cayana Linnaeus and Stieda body flattened, 0.5 high × 1.5 wide. I. navarroi was reported from the palm tana- Substieda body small and delicate, 1.0 high × ger T. palmarum (Berto et al. 2010b, 2011b). 2.5 wide. Parastieda body absent. Sporocyst The aim of this study was to report one residuum composed of scattered granules, more host for I. tiesangui in Marambaia Is- which sometimes, turns into a ring form. land: the ruby-crowned tanager T. coronatus. Sporozoites vermiform, with a robust and elongate posterior refractile body. Materials and methods These oocysts had the same characteristic features of the oocysts of I. navarroi de- Four ruby-crowned tanagers were captured scribed from R.b. dorsalis and T. palmarum using nets at Marambaia Island (23°04’S, on Marambaia Island. Therefore, in the cur- 43°53’W) in the State of Rio de Janeiro. They rent study, a new host for I. navarroi is re- were kept in individual cages, and feces were corded, once that feature-similar oocysts were collected immediately after defecation. After recovered from the ruby-crowned tanager T. identification, the birds were released and the coronatus. fecal samples were placed in plastic vials con- taining 2.5% potassium dichromate solution Acknowledgements (K2Cr2O7) 1:6 (v/v). Samples were carried to the Laboratório de Coccídios e Coccidioses, This study was supported by grants from

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Fig. 1. Sporulated oöcysts of Isospora navarroi recovered from ruby-crowned tanagers Tachyphonus coronatus: Composite line drawing (a) and photomicrographs. Scale-bar: 10 µm.

the Fundação Carlos Chagas Filho de Amparo Lopes CWG. Isospora ramphoceli n. sp. à Pesquisa do Estado do Rio de Janeiro (FA- (Apicomplexa: Eimeriidae) from the Brazi- PERJ) to B. P. Berto (E-26/110.987/2013). lian tanager (Aves: Passeriformes: Thrau- We also thank the Brazilian Navy, in special pidae) Ramphocelus bresilius dorsalis S- to the command of CADIM (Centro de Ade- clater, 1855. Zootaxa, 2650, 57-62, 2010a. stramento da Ilha da Marambaia) that allowed Berto BP, Luz HR, Ferreira I, Flausino W, us to access the Marambaia Island, located in Lopes CWG. Two new hosts for Isospora Rio de Janeiro State, Brazil, and use some of tiesangui Berto, Flausino, Luz, Ferreira & the facilities of CADIM during the field work. Lopes. Revista Brasileira de Medicina Ve- terinária, 32, 169-171, 2010b. References Berto BP, Flausino W, McIntosh D, Lopes CWG. Coccidia of New World - Berto BP, Flausino W, Luz HR, Ferreira I, birds (Aves: Passeriformes): a review of Lopes CWG. Three New Coccidian Para- Eimeria Schneider, 1875 and Isospora sites of Brazilian Tanager (Ramphocelus- Schneider, 1881 (Apicomplexa: Eimerii- bresilius dorsalis) from South America. dae). Systematic Parasitology, 80, 159- Acta Protozoologica, 47, 77-81, 2008. 204, 2011a. Berto BP, Flausino W, Luz HR, Ferreira I, Berto BP, Luz HR, Flausino W, Teixeira- Lopes CWG. Two new Isospora species Filho WL, Ferreira I, Lopes CWG. Isospo- from Brazilian tanager (Ramphocelus bre- roid Coccidia (Apicomplexa: Eimeriidae) silius dorsalis) of South America. Parasi- parasites of tanagers (Passeriformes: tology Research, 105, 635-639, 2009. Thraupidae) from the Marambaia Island, Berto BP, Flausino W, Luz HR, Ferreira I, Brazil. Pesquisa Veterinária Brasileira,

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31, 798-805, 2011b. 333-336, 1997. CBRO. Lista das aves do Brasil. Rio de Janei- IUCN. International Union for Conservation ro: Comitê Brasileiro de Registros Ornito- of Nature and Natural Resources. 2013. lógicos, 2011. Duszynski DW, Wilber PG. A guideline for http://www.iucnredlist.org [15-08-2013] the preparation of species descriptions in Sick H. Ornitologia Brasileira. Rio de Janeiro: the Eimeridae. Journal of Parasitology, 83, Nova Fronteira, 1997.

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