Isospora canaria Box, 1975 (Apicomplexa: Eimeriidae) from canaries Serinus canaria Linnaeus (Passeriformes: Fringillidae) in Brazil Bruno P. Berto, Ildemar Ferreira, Walter Flausino, Walter L. Teixeira-Filho & Carlos W. G. Lopes Systematic Parasitology An International Journal ISSN 0165-5752 Volume 85 Number 1 Syst Parasitol (2013) 85:49-53 DOI 10.1007/s11230-012-9402-7
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Author's personal copy Syst Parasitol (2013) 85:49–53 DOI 10.1007/s11230-012-9402-7
Isospora canaria Box, 1975 (Apicomplexa: Eimeriidae) from canaries Serinus canaria Linnaeus (Passeriformes: Fringillidae) in Brazil Bruno P. Berto • Ildemar Ferreira • Walter Flausino • Walter L. Teixeira-Filho Carlos W. G. Lopes
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Received: 31 October 2012 / Accepted: 17 December 2012 Ó Springer Science+Business Media Dordrecht 2013
Abstract Isospora canaria Box, 1975 (Protozoa, Apicomplexa, Eimeriidae) is reported and described from canaries Serinus canaria (Linnaeus) in southeast Brazil. Its oo¨cysts are subspheroidal to ellipsoidal, 24.4 9 22.2 lm, with smooth, bilayered wall, *1.2 lm. The micropyle and the oo¨cyst residuum are absent, but a polar granule is present. The sporocysts are lemonshaped, 17.6 9 10.6 lm. The Stieda body is nipplelike, and substieda body is prominent and homogeneous. The sporocyst residuum is composed of scattered granules. The sporozoite has anterior and posterior refractile bodies and a nucleus. The report of this coccidium recovered from exotic canaries in
B. P. Berto (&) I. Ferreira Departamento de Biologia Animal, Instituto de Biologia, Universidade Federal Rural do Rio de Janeiro (UFRRJ), BR-465 km 7, Serope´dica, RJ 23890-000, Brazil e-mail:
[email protected] I. Ferreira e-mail:
[email protected] W. Flausino W. L. Teixeira-Filho C. W. G. Lopes Departamento de Parasitologia Animal, Instituto de Veterina´ria, UFRRJ, BR-465 km 7, Serope´dica, RJ 23890-000, Brazil e-mail:
[email protected] W. L. Teixeira-Filho e-mail:
[email protected] C. W. G. Lopes e-mail:
[email protected]
South America is relevant to native passerines, mainly to Carduelis yarrellii, which are listed as vulnerable species by IUCN (International Union for Conservation of Nature and Natural Resources).
Introduction The canary, Serinus canaria (Linnaeus), is a fringillid bird from the Canary Islands. This species is bred virtually in all countries because of their colours and vocal repertoire. In Brazil, the captive breeding has been widely practised (Sick, 1997; IUCN, 2012). Coccidia of Isospora Schneider, 1881 were largely reported from fringillid birds of the New World (Berto et al., 2011a). Among them, Isospora canaria Box, 1975 and Isospora serini (Araga˜o, 1933) Box, 1975 were described and subsequently re-described during studies of the intra- and extra-intestinal life-cycles in canaries, S. canaria, in the USA (Box, 1975, 1981). The current study describes, in more detail, oo¨cysts of I. canaria infecting canaries, S. canaria, bred in captivity in Rio de Janeiro, Brazil.
Materials and methods Faecal samples were collected from 15 birds from a breeder located in the city of Rio de Janeiro (22°540 3.5300 S; 43°160 4600 W), Rio de Janeiro State, Brazil. Birds were held in individual cages and faecal
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samples were collected in late afternoon immediately after defecation and placed in plastic vials containing 2.5% potassium dichromate solution (K2Cr2O7) 1:6 (w/v). Samples were carried to the Laborato´rio de Coccı´dios e Coccidioses (Universidade Federal Rural do Rio de Janeiro, UFRRJ). Samples were placed in a thin layer (c.5 mm) of 2.5% K2Cr2O7 solution in Petri plates and incubated at 23–28°C for 10 days or until 70% of the oo¨cysts were sporulated. Oo¨cysts were recovered by flotation in Sheather’s sugar solution (S.G. 1.20) and examined microscopically using the technique described by Duszynski & Wilber (1997). Morphological observations and measurements, given in micrometres, were made using a Carl Zeiss binocular microscope with an apochromatic oil immersion objective lens and an ocular micrometer (K-15X PZO. Poland). Line drawings were prepared using a Wild M-20 binocular microscope with a drawing tube. Photomicrographs were taken using a digital camera (Sony CD Mavica MVC-CD250). Size ranges are shown in parenthesis followed by average and shape index (L/W ratio). Abbreviations: micropyle [M], oo¨cyst residuum [OR], polar granule [PG], Stieda body [SB], substieda body [SSB], parastieda body [PSB], sporocyst residuum [SR], sporozoite [SZ], refractile body [SRB], nucleus [N], length [L] and width [W].
Syst Parasitol (2013) 85:49–53
Locality: 22°540 3.5300 S; 43°160 4600 W, Rio de Janeiro, Brazil. Prevalence: 6/15 birds infected (40%). Sporulation time: Ten days. Site: Not investigated. Description (Figs. 1a–f, 2a–b) Sporulated oo¨cyst Oo¨cyst shape (n = 50) sub-spheroidal to ellipsoidal; number of walls 2; wall thickness 1.2 (1.0–1.3); outer wall smooth, c.2/3 of total thickness; L 9 W = 24.4 9 22.2 (21-27 9 19-25), with L/W ratio = 1.1 (1.0–1.2); M and OR absent; PG present, frequently as a unique sub-spheroidal granule. Sporocyst and sporozoites Sporocyst shape (n = 50) lemon-shaped; L 9 W = 17.6 9 10.6 (16–20 9 10–12); L/W ratio = 1.6 (1.6–1.8); SB present, nipple-like, *1 (0.5–1) high 9 *2 (1.5–2.5) wide; SSB present, prominent, homogeneous, *1.5 (1–2) high 9 *3 (2.5–3.5) wide; PSB absent; SR present, composed of a cluster of scattered granules; SZ with anterior and posterior SRB and centrally located N.
Discussion Results Fifteen canaries were examined; six of them shed oo¨cysts in the faeces. Initially, the oo¨cysts were nonsporulated, but approximately 70% of the oo¨cysts were sporulated at day 10 (under the conditions used in this study). Isospora canaria Box, 1975 Host: Serinus canaria (Linnaeus) (Aves, Passeriformes, Fringillidae). Material: One-half of the oo¨cysts are kept in 10% aqueous buffered formalin (v/v), and the other half in 70% ethanol. Both samples were deposited in the Parasitology Collection, in the Department of Animal Parasitology, at UFRRJ, located in Serope´dica, Rio de Janeiro, Brazil. Phototypes and line drawings are deposited at the same location. The repository number is P-42/2012.
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The concept of intra-familial specificity of Isospora spp. of passerine birds has been maintained during the preceding years (Berto et al., 2011a). In this context, the presence of coccidia of exotic passerines in South America is relevant to native passerines since transmission could occur from breeders of canaries in wild areas. Two species of fringillid birds, Carduelis magellanica (Vieillot) and Carduelis yarrellii (Audubon), are native in South America, including Brazil. The presence of C. yarrellii is more relevant, since this species is listed as vulnerable by the IUCN (IUCN, 2012). Moreover, a hybrid species (called ‘pintagol’ in Brazil) from the crossing in captivity of male C. magellanica with female S. canaria should enhance the possibility of transmission of I. canaria to native passerines. In this study, the morphology of the oo¨cysts of I. canaria was described in detail, thus providing evidence for structures and patterns underemphasized by Box (1975), such as the shape of the sporocysts
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Fig. 1 Line drawings of Isospora canaria: a. sporulated oo¨cyst; b–d. variations of the Stieda and substieda bodies; e–f. variations of the posterior end of the sporocysts. Scale-bar: 10 lm
Fig. 2 Micrographs of sporulated oo¨cysts (a–b) of Isospora canaria. Scale-bar: 10 lm
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Compact and diffuse prominent, homogeneous, *1.5 9 3 nipple-like, *1 9 2 17.6 9 10.6 (16–20 9 10–12) Sub-spheroidal to ellipsoidal Present study
24.4 9 22.2 (21–27 9 19–25)
1.13
Present
Lemonshaped
Compact *2 9 3 nipple-like, *1 9 2 18.1 9 11.5 (17–22 9 10–13) 1.1 (1.0–1.1) 24.6 9 21.8 (17–30 9 17–30) Sub-spheroidal Box (1975)
Shape index Measurements (lm) References
Present
Lemonshaped
Residuum Stieda body Measurements (lm) Shape Shape
Polar granule
Sporocysts Oo¨cysts
Substieda body
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Table 1 Comparative morphology of Isospora canaria recovered from canaries Serinus canaria reported from Box (1975) and the present study
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with a tapered posterior end and the variations of the Stieda and substieda bodies (SBs and SSBs, respectively). The Fig. 1b–d and e–f evince the variations of the Stieda and substieda bodies, as well as the posterior end of the sporocysts. These variations had been reported in some studies, originally by Grulet et al. (1982) and recently by Coelho et al. (2011a, b), Berto et al. (2011a, b, c) and Pereira et al. (2011), as being possibly the result of the sporulation process, the position of the SZ inside of the sporocyst, or the position of the oo¨cyst and sporocyst under the coverslip. Table 1 compares all morphological and morphometric characteristics of the oo¨cysts of I. canaria reported by Box (1975) with the oo¨cysts recovered in this study. Based on all morphological features mentioned and compared in this study, the described specimens are identified as I. canaria obtained from canaries S. canaria bred in captivity in Brazil. Acknowledgments The authors are thankful to the breeder of the canaries located in Rio de Janeiro, Brazil, for permitting and assisting the material collection.
References Berto, B. P., Flausino, W., McIntosh, D., Teixeira-Filho, & Lopes, C. W. G. (2011a). Coccidia of New World passerine birds (Aves: Passeriformes): a review of Eimeria Schneider, 1875 and Isospora Schneider, 1881 (Apicomplexa: Eimeriidae). Systematic Parasitology, 80, 159–204. Berto, B. P., Flausino, W., Luz, H. R., Ferreira, I., & Lopes, C. W. G. (2011b). Isospora coerebae n. sp. (Apicomplexa: Eimeriidae) from the bananaquit Coereba flaveola (Passeriformes: Coerebidae) in South America. Revista Brasileira de Parasitologia Veterina´ria, 20, 22–26. Berto, B. P., Luz, H. R., Flausino, W., Teixeira-Filho, W. L., Ferreira, I., & Lopes, C. W. G. (2011c). Isosporoid coccidia (Apicomplexa: Eimeriidae) parasites of tanagers (Passeriformes: Thraupidae) from the Marambaia Island, Brazil. Pesquisa Veterina´ria Brasileira, 31, 798–805. Box, E. D. (1975). Exogenous stages of Isospora serini (Araga˜o) and Isospora canaria sp. n. in the canary (Serinus canarius L.). Journal of Protozoology, 22, 165–169. Box, E. D. (1981). Isospora as an extraintestinal parasite of passerine birds. Journal of Protozoology, 28, 244–246. Coelho, C. D., Berto, B. P., Neves, D. M., Oliveira, V. M., Flausino, W., & Lopes, C. W. G. (2011a). Isospora mimusi n. sp. (Apicomplexa: Eimeriidae) from the tropical mockingbird Mimus gilvus in South America. Acta Protozoologica, 50, 137–140. Coelho, C. D., Berto, B. P., Neves, D. M., Oliveira, V. M., Flausino, W., & Lopes, C. W. G. (2011b). Two new Isospora species from the saffron finch, Sicalis flaveola in Brazil. Acta Parasitologica, 56, 239–244.
Author's personal copy Syst Parasitol (2013) 85:49–53 Duszynski, D., & Wilber, P. (1997). A guideline for the preparation of species descriptions in the Eimeriidae. Journal of Parasitology, 83, 333–336. Grulet, O., Landau, I., & Baccam, D. (1982). Les Isospora du Moineau domestique; multiplicite des especes. Annales de Parasitologie Humaine et Compare´e, 57, 209–235. IUCN (2012). International Union for Conservation of Nature and Natural Resources. http://www.iucnredlist.org. Cited 04 Out., 2012.
53 Pereira, L. Q., Berto, B. P., Flausino, W., Lovato, M., & Lopes, C. W. G. (2011). Isospora bocamontensis n. sp. (Apicomplexa: Eimeriidae) from the yellow cardinal Gubernatrix cristata (Vieillot) (Passeriformes: Emberizidae) in South America. Systematic Parasitology, 78, 73–80. Sick, H. (1997). Ornitologia Brasileira. Rio de Janeiro: Nova Fronteira, 862 pp.
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