Two new Isospora species from Brazilian tanager (Ramphocelus bresilius dorsalis) of South America

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Parasitol Res (2009) 105:635–639 DOI 10.1007/s00436-009-1432-y

ORIGINAL PAPER

Two new Isospora species from Brazilian tanager (Ramphocelus bresilius dorsalis) of South America Bruno P. Berto & Walter Flausino & Hermes Ribeiro Luz & Ildemar Ferreira & Carlos W. G. Lopes

Received: 23 October 2008 / Accepted: 24 March 2009 / Published online: 28 April 2009 # Springer-Verlag 2009

Abstract Two new coccidian (Protozoa: Apicomplexa: Eimeriidae) species from the Brazilian tanager Ramphocelus bresilius dorsalis are reported in the current study. Isospora cadimi n. sp. oocysts are spheroidal to subspheroidal, 24.2×22.9 µm, with a smooth and bi-layered wall, ∼1.1 µm. Micropyle, oocyst residuum, and polar granule are absent. Sporocysts are broadly ovoidal, 16.9× 11.6 µm. Stieda and substieda bodies are present. Sporocyst residuum is present and sporozoites have refractile body and nucleus. Isospora navarroi n. sp. oocysts are spheroidal to sub-spheroidal, 21.4×20.6 µm, with a smooth and bilayered wall, ∼1.1 µm. Micropyle, oocyst residuum, and polar granule are absent. Sporocysts are ellipsoidal, 16.1× 10.2 µm. Stieda and substieda bodies are present. Sporocyst residuum is present and sporozoites have a robust posterior refractile body.

B. P. Berto Curso de Pós-Graduação em Ciências Veterinárias, Universidade Federal Rural do Rio de Janeiro (UFRRJ), Seropédica, RJ, Brazil e-mail: [email protected] W. Flausino (*) : C. W. G. Lopes (*) Departamento de Parasitologia Animal, Instituto de Veterinária, UFRRJ, BR-465 km 7, 23890-000 Seropédica, RJ, Brazil e-mail: [email protected] H. Ribeiro Luz : I. Ferreira Departamento de Biologia Animal, Instituto de Biologia, UFRRJ, BR-465 km 7, 23890-000 Seropédica, RJ, Brazil H. Ribeiro Luz e-mail: [email protected] I. Ferreira e-mail: [email protected]

Introduction The Brazilian tanager Ramphocelus bresilius dorsalis is a South American bird which belongs to the Thraupidae; the male bird is recognized by its beautiful red plumage (Sick 1997). The global distribution of this species is not known, however, it is thought to be restricted to Brazil and Argentina (Stotz et al. 1996). Although isosporid coccidia have been reported from birds in the Thraupidae since the beginning of the twentieth century, the majority of species have been described in the last two decades. Boughton et al. (1938) recovered isosporoid oocysts from feces of four Andean tanagers: (1) the southern palm tanager, Thraupis palmarum; (2) the magpie tanager, Cissopis leveriana; (3) the southern silver-beaked tanager, Ramphocelus carbo; and (4) the Brazilian tanager, R. b. dorsalis. All of these coccidia were obtained from captured birds in zoos, but none have been described or named. I. thraupis Lainson 1994; I. andesensis Templar et al. 2004; and Isospora irisidornisi Metzelaars et al. 2005 were described in the palm tanager, T. palmarum, in the common bush tanager Chloropingus ophthalmicus, and in the yellow-throated tanager Iridosornis analis, respectively (Lainson 1994; Templar et al. 2004; Metzelaars et al. 2005). Finally, coccidia parasitizing R. b. dorsalis were reported recently by Berto et al. (2008) when they described the sporulated oocysts of three distinct species: Isospora tiesangui Berto et al. 2008; Isospora marambaiensis Berto et al. 2008; and Isospora sepetibensis Berto et al. 2008. The current study describes two new Isospora species infecting the Brazilian tanager R. b. dorsalis in Marambaia Island, Rio de Janeiro State, Brazil.

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Materials and methods Three Brazilian tanagers were captured using nets on Marambaia Island (23° 04′ S and 43° 53′ W). They were kept in individual cages, and feces were collected immediately after defecation. After identification the birds were released, and the fecal samples were placed into plastic vials containing 2.5% (w/v) solution of K2Cr2O7 in 1:6 (v/v). Samples were carried to the Laboratório de Coccídios e Coccidioses located at Universidade Federal Rural do Rio de Janeiro (UFRRJ). Samples were placed in a thin layer (∼ 5 mm) of K2Cr2O7 2.5% solution in Petri plates, and incubated at 23–28°C for 10 days or until 70% of oocysts were sporulated. Oocysts were recovered by flotation in Sheather’s sugar solution (S.G. 1.20) and microscopically examined using the technique described by Duszynski and Wilber (1997). Morphological observations (micropyle [M], oocyst residuum [OR], polar granule [PG], Stieda body [SB], substieda body [SSB], parastieda body [PSB], sporocyst residuum [SR], sporozoite [SZ], refractile body [SRB], nucleus [N]) and measurements, in micrometers, were performed using a Carl Zeiss binocular microscope with apochromatic oil-immersion objective lens and ocular micrometer K-15X PZO (Poland). Line drawings were prepared using a binocular microscope Wild M-20 with drawing tube. Pictures were taken using a digital camera model CD Mavica MVC-CD250 Sony®. Size ranges are shown in parenthesis followed by average and shape index (L/W ratio).

Results Three Brazilian tanagers were examined; of which one shed oocysts in the feces. Initially, the oocysts were nonsporulated, by day 3, 70% had sporulated. Isospora cadimi n. sp. (Figs. 1a–c and 3a, b) Fig. 1 Line drawings of Isospora cadimi, a new coccidium species recovered from the Brazilian tanager Ramphocelus bresilius dorsalis. a sporulated oocyst with its respective variations of b, c detached Stieda and substieda bodies. Scale-bar 10 µm for oocysts; and 5 µm for Stieda and substieda bodies

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Description of sporulated oocyst Oocyst shape (N=15) spheroidal to sub-spheroidal; number of walls: two; wall thickness: 1.1 (1.0–1.3); outer wall smooth, about 2/3 of total thickness; L×W, 24.2×22.9 (22–26×21–24), with L/W ratio, 1.1 (1.0–11); M, OR, PG, all absent. Description of sporocyst and sporozoites Sporocyst shape (N=15): broadly ovoidal, tapering toward 1 end; L×W, 16.9×11.6 (15–18×10–13); L/W ratio, 1.5 (1.3–1.6); SB: present, nipple-like, 0.8 high×2.0 wide; SSB: prominent and uniquely compartmentalized; a central, denser portion is as wide (∼1.9) as the SB, then tapers to cone-like shape ∼1.6 high; there are two wing-like structures on either side of this cone that, together, are 2.5 high×4.2 wide; PSB: absent; SR: present; SR characteristics: composed of many scattered granules of different sizes; SZ: vermiform with one large, posterior SRB and a centrally located N.

Taxonomic summary Type-host R. b. dorsalis Linnaeus, 1766 (Aves: Passeriformes: Thraupidae). Type-material Oocysts stored in 10% aqueous buffered formalin (v/v), and deposited in the Parasitology Collection, in the Department of Animal Parasitology, at UFRRJ, located in Seropédica, Rio de Janeiro, Brazil. Phototypes and line drawings are deposited at the same location. The repository number is P-28/2008. Type-locality Marambaia Island (23° 04′ S and 43° 53′ W), Rio de Janeiro, Brazil. Sporulation time Three days. Site of infection Not investigated.

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Fig. 2 Line drawings of I. navarroi, a new coccidium species recovered from the Brazilian tanager Ramphocelus bresilius dorsalis. a sporulated oocyst with its respective variations of b, c, d detached Stieda and substieda bodies. Scale-bar 10 µm for oocysts; and 5 µm for Stieda and substieda bodies

Prevalence 33% (one of three examined birds). Etymology The specific epitaph is a homage to the Brazilian Navy, in special the command of CADIM (Centro de Adestramento da Ilha da Marambaia), that is located in Marambaia Island, Rio de Janeiro State, Brazil.

Fig. 3 Photographs of sporulated oocysts of new coccidia species recovered from the Brazilian tanager Ramphocelus bresilius dorsalis. a, b Isospora cadimi and c, d Isospora navarroi. Scale-bar 10 µm

Remarks The I. cadimi oocysts can be easily distinguished by the size, shape of the SB and SSB, and the absence of PG. I. thraupis, described by Lainson (1994), has sporocysts with SSB smaller than those in I. cadimi, while I. andesensis has triangular-shaped SB with no evident SSB (Templar et al. 2004). The oocysts of I. irisidornisi differ

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from I. cadimi oocysts due to the presence of PG (Metzelaars et al. 2005). I. tiesangui described by Berto et al. (2008) presents sporocysts with a large and noncompartmentalized SSB. Also, I. sepetibensis presents PG, while I. marambaiensis oocysts are larger than I. cadimi oocysts (Berto et al. 2008). Isospora navarroi n. sp. (Figs. 2a–d and 3c, d) Description of sporulated oocyst Oocyst shape (N=17) spheroidal to sub-spheroidal; number of walls: two; wall thickness: 1.1 (0.9-1.1); outer wall smooth, about 2/3 of total thickness; L×W: 21.4×20.6 (19–24×18–23), with L/W ratio: 1.0 (1.0–11); M, OR, PG: all absent. Description of sporocyst and sporozoites: Sporocyst shape (N=17): ellipsoidal; L×W: 16.1×10.2 (14–19×9– 12); L/W ratio: 1.6 (1.4–1.7); SB: present, flattened, 0.5 high×1.7 wide; SSB: present, small, slight, 1.2 high×2.3 wide; PSB: absent; SR: present; SR characteristics: composed of scattered granules, which sometimes, turns into a ring form; SZ: vermiform, with a robust and elongate posterior SRB. Taxonomic summary Type-host R. b. dorsalis Linnaeus, 1766 (Aves: Passeriformes: Thraupidae). Type-material Oocysts stored in 10% aqueous buffered formalin (v/v), and deposited in the Parasitology Collection, in the Department of Animal Parasitology, at UFRRJ, located in Seropédica, Rio de Janeiro, Brazil. Phototypes and line drawings are deposited at the same location. The repository number is P-29/2008. Type-locality Marambaia Island (23° 04′ S and 43° 53′ W), Rio de Janeiro, Brazil. Sporulation time Three days. Site of infection Not investigated. Prevalence 33% (one of three examined birds). Etymology The specific epitaph is derived from the family name of a Brazilian parasitologist, Dr. Italmar Teodorico Navarro, given in his honor for his contribution to the study of protozoa. Remarks The I. navarroi oocysts can be easily distinguished by the size, shape of SB, SSB and SRB, and the absence of PG. I. cadimi presents nipple-like SB and

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compartmentalized SSB, while I. navarroi has flattened SB and small SSB; besides, SRB of SZ are more robust than in I. cadimi. Isospora thraupis can be distinguished from I. navarroi because it presents ellipsoidal sporocysts and a single robust SRB in SZ (Lainson 1994). Isospora andesensis has triangular-shaped SB with no evident SSB. I. irisidornisi oocysts presents PG (Metzelaars et al. 2005), and I. tiesangui, I. marambaiensis and I. sepetibensis differs from I. cadimi in that they have larger SSB, larger oocysts, and the presence of PG, respectively (Berto et al. 2008).

Discussion As observed in the current study, a few variations in SB and SSB (Figs. 1b–c and 2b–d) were also observed in sporocysts of I. cadimi and I navarroi according to Grulet et al. (1982); however, these variations are not significant enough to separate and describe them as new species. These variations could be possibly the result of the sporulation process, the position of the SZ inside of the sporocyst, or the position of the oocyst and sporocyst under the coverslip. According to Duszynski and Wilber (1997), new coccidian species should be compared in detail with coccidian species that are feature-similar and belong to the same host family. After descriptions reported by Berto et al. (2008), the comparative remarks in this study described specimens that are the fourth and fifth new coccidian species obtained from Brazilian tanager R. b. dorsalis. Duszynski and Wilber (1997) suggest that the specificity of coccidia is related to the host family. Thus, the description of new coccidian parasites from thraupid hosts provides significant information, once Brazil has 86 distinct thraupid species catalogued (CBRO 2007). The easiness of transmission of isosporoid coccidian and the geographic range of the host R. b. dorsalis could trigger the dissemination of these new coccidian species to sympatric thraupids in Brazil and Argentina and, successively, throughout the Americas. On the other hand, several isoporoid coccidia described from thraupids such as T. palmarum, C. ophthalmicus, and I. analis, have not been reported since their original descriptions (Stotz et al. 1996). Accordingly, T. palmarum is widely distributed in South America; C. ophthalmicus is distributed in South and Central America, and I. analis in Colombia, Ecuador, and Peru (Stotz et al. 1996). Acknowledgements We are thankful to the Brazilian Navy, especially to the command of CADIM (Centro de Adestramento da Ilha da Marambaia), that allowed us to access the Marambaia Island, located in Rio de Janeiro State, Brazil, and use some of the facilities of CADIM during the field work.

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References Berto BP, Flausino W, Luz HR, Ferreira I, Lopes CWG (2008) Three new coccidian parasites of Brazilian tanager (Ramphocelus bresilius dorsalis) from South America. Acta Protozool 47:77–81 Boughton DC, Boughton RB, Volk J (1938) Avian hosts of the genus Isospora (Coccidiidae). Ohio J Sci 38:149–163 CBRO (2007) Lista das aves do Brasil. Comitê Brasileiro de Registros Ornitológicos, Rio de Janeiro Duszynski D, Wilber P (1997) A guideline for the preparation of species descriptions in the Eimeridae. J Parasitol 83:333–336 Grulet O, Landau I, Baccam D (1982) Les Isospora du Moineau domestique; multiplicite des especes. Ann Parasit Hum Comp 57:209–235

639 Lainson R (1994) Observations on some avian coccidia (Apicomplexa: Eimeriidae) in Amazonian Brazil. Mem Inst Oswaldo Cruz 89:303–311 Metzelaars H, Spaargaren T, McQuistion TE, Capparella AP (2005) Isospora iridosornisi, a new coccidian parasite (Apicomplexa, Eimeriidae) from the yellow-throated tanager, Iridosornis analis of South America. Acta Parasitol 50:191–193 Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro Stotz DF, Fitzpatrick JW, Parker TA, Moskovits DK (1996) Neotropical birds: ecology and conservation. University of Chicago Press, Chicago Templar AC, McQuistion TE, Capparella AP (2004) A new coccidian parasite, Isospora andesensis, from the common bush tanager Chlorospingus ophthalmicus of South America. Acta Protozool 43:369–371

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