A DIAGNOSTIC TOOL TO IDENTIFY SPECIES OF THE GENUS Isospora SCHNEIDER, 1881 (APICOMPLEXA: EIMERIIDAE) BASED ON SPORULATED OOCYSTS FROM THAUPIDAE FAMILY (AVES: PASSERIFORMES): A DICHOTOMOUS KEY*
UMA FERRAMENTA DE DIAGNÓSTICO PARA IDENTIFICAR ESPÉCIES DE Isospora SCHNEIDER, 1881 (APICOMPLEXA: EIMERIIDAE) DA FAMÍLIA THAUPIDAE (AVES: PASSERIFORMES) COM BASE EM OOCISTOS ESPORULADOS: UMA CHAVE DICOTÔMICA
Bruno Pereira Berto1, Hermes Ribeiro Luz2, Ildemar Ferreira3, Walter Flausino4 and Carlos Wilson Gomes Lopes5
ABSTRACT. Berto B.P., Luz, H.B., Ferreira I., Flausino W. & Lopes C.W.G. A diagnostic tool to identify species of the genus Isospora Schneider, 1881 (Apicomplexa: Eimeriidae) based on sporulated oocysts from Thaupidae family (Aves: Passeriformes): a dichotomous key [Uma ferramenta de diagnóstico para identificar espécies de Isospora Schneider, 1881 (Apicomplexa: Eimeriidae) da família Thaupidae (Aves: Passeriformes): uma chave dicotômica]. Revista Brasileira de Medicina Veterinária, 32(3):182-186, 2010. Laboratório de Coccídios e Coccidioses, Departamento de Parasitologia Animal, Instituto de Veterinária, Universidade Federal Rural do Rio de Janeiro, BR 465 km 7, Seropédica, RJ 23890-000, Brasil. E-mail: [email protected] The birds of the Thraupidae family, similar to other passerine birds can be infected by coccidia, and the genus Isospora can be considered the most relevant. Isospora thraupis, I. andesensis, I. irisidornisi, I. tiesangui, I. marambaiensis, I. sepetibensis, I. cadimi, I. navarroi, I. ramphoceli, I. sanhaci, I. sayacae and I. silvasouzai were described from thraupids of South American and considering that these birds are sympatric hosts of other birds that inhabit South, North and Central Americas, it is concluded that these parasites should be widely dispersed in the America Continent. In this sense, this paper proposes to provide scientific background and a dichotomous key to assist in the identification of sporulated oocysts of the genus Isospora from passerine birds of the Thraupidae family. KEY WORDS. Sporulated oocysts, dichotomous key, Passeriformes, South America. RESUMO. As aves da família Thraupidae, de forma Isospora pode ser considerado o mais relevante. Isospora semelhante a outras aves da ordem Passeriformes, po- thraupis, I. andesensis, I. irisidornisi, I. tiesangui, I. dem ser parasitadas por coccídios, sendo que o gênero marambaiensis, I. sepetibensis, I. cadimi, I. navarroi,
*Received on July 12, 2010 Accepted on August 12, 2010 1Biólogo. Dr. CsVs, Laboratório de Coccídios e Coccidioses (LCC), Departamento de Parasitologia Animal (DPA), Instituto de Veterinária (IV), Universidade Federal Rural do Rio de Janeiro (UFRRJ), BR 465 km 7, Seropédica, RJ 23890-000, Brasil. E-mail: [email protected] 2Biólogo. Curso de Pós-Graduação em Ciências Veterinárias, UFRRJ, BR 465 km 7, Seropédica, RJ 23890-000. E-mail: [email protected] . CAPES Scholarship. 3Biólogo. Dr. Ecol. Laboratório de Ornitologia, Departamento de Biologia Animal, Instituto de Biologia, UFRRJ, BR 465 km 7, Seropédica, RJ 23890-000, Brazil. E-mail: [email protected] 4Biólogo. PhD. LCC, DPA, IV, UFRRJ. BR 465 km 7, Seropédica, RJ 23890-000. E-mail: [email protected] - CNPq fellowship. 5Médico-veterinário. PhD, LD, LCC, DPA, IV, UFRRJ, BR 465 km 7, Seropédica, RJ 23890-000, Brasil. E-mail: [email protected] - CNPq fellowship.
182 Rev. Bras. Med. Vet., 32(3):182-186, jul/set 2010 A diagnostic tool to identify species of the genus Isospora Schneider, 1881
I. ramphoceli, I. sanhaci, I. sayacae e I. silvasouzai Pallas, 1764, and the Brazilian tanager, R. b. dorsalis. foram descritas de traupídeos sul-americanos e conside- However, all were reported from captured birds in zoos rando que estas aves hospedeiras são simpátricas à ou- and none of the coccidia were described or named. tras aves que habitam às Américas do Sul, do Norte e Isospora thraupis Lainson, 1994 is considered the Central, conclui-se que estes parasitos devem dispersa- first species described in the Thraupidae family. The se amplamente pelo Américas. Neste sentido, este traba- oocysts that provided this description were recovered lho propõe fornecer embasamento científico e uma chave from feces of palm tanagers, T. palmarum, from Amazon dicotômica que auxilie na identificação dos oocistos es- (Lainson, 1994). porulados de coccídios do gênero Isospora parasitos de Templar et al. (2004) described I. andesensis aves Passeriformes da família Thraupidae. Templar, McQuistion & Capparella, 2004 from the PALAVRAS-CHAVE: Oocistos, chave dicotômica, common bush tanager Chlorospingus ophthalmicus Du Passeriformes, América do Sul. Bus de Gisignies, 1847 and Metzelaars et al. (2005) described I. irisidornisi Metzelaars, Spaargaren, INTRODUCTION McQuistion & Capparella, 2005 from the yellow- The Thraupidae family belongs to the order Passeri- throated tanager, Iridosornis analis Tschudi, 1844. Both formes and definitely contributes to the high concept of studies were conducted on birds of Peru. beauty that has the Brazilian avifauna. Among the Recently, Berto et al. (2008; 2009a; 2009b; thraupids with intense and varied colorful, stand out the 2010) described nine Isospora species from Brazilian tanagers of the genus Tangara Brisson, 1760, the thraupids: (1) Isospora tiesangui Berto, Flausino, honeycreepers of the genus Cyanerpes Oberholser, Luz, Ferreira & Lopes, 2008; (2) Isospora 1899, the dacnis of the genus Dacnis Cuvier, 1816, the marambaiensis Berto, Flausino, Luz, Ferreira & manakins of the genus Chiroxiphia Cabanis, 1847 and Lopes, 2008; (3) Isospora sepetibensis Berto, the Brazilian tanager Ramphocelus bresilius dorsalis Flausino, Luz, Ferreira & Lopes, 2008; (4) Isospora Sclater, 1855 (Sick, 1997; CBRO, 2009; IUCN, 2009). cadimi Berto, Flausino, Luz, Ferreira & Lopes, Similar to other passerine birds, the thraupids can be 2009; (5) Isospora navarroi Berto, Flausino, Luz, infected by coccidia, being that the genus Isospora Ferreira & Lopes, 2009; and (6) Isospora Schneider, 1881 can be considered the most relevant. ramphoceli Berto, Flausino, Luz, Ferreira & Lopes, The coccidiosis is diagnosed by observation of oocysts 2010 from R. b. dorsalis of Marambaia Island, Rio in feces, which are exogenous forms of these parasites de Janeiro, Brazil, and (7) Isospora sanhaci Berto, (Soulsby, 1987; Lainson, 1994; Duszynski & Wilber, Balthazar, Flausino & Lopes, 2009; (8) Isospora 1997; Templar et al., 2004; Metzelaars et al., 2005; sayacae Berto, Balthazar, Flausino & Lopes, 2009; Berto et al. 2008; 2009a; 2009b; 2010). and (9) Isospora silvasouzai Berto, Balthazar, Considering the recent reports on new species of Flausino & Lopes, 2009 from sayaca tnagers T. Isospora parasitizing thraupids in Brazil should be concluded sayaca of Teresópolis, Rio de Janeiro, Brazil. that these parasites are dispersed widely by South, North The comparative morphology and morphometry of and Central America, once that the South American birds, the oocysts of these Isospora species parasites of which were described coccidia, are sympatric with other the Thraupidae family can be observed in Figure 1 birds inhabiting the American continent. and Table 1. Thus, this paper aims to provide scientific background and a dichotomous key to assist in the identification of Dichotomous key for identification of Isospora from oocysts of Isospora parasites of passerine birds of the Thraupidae family Thraupidae family. After observing the morphological and morphome- tric features of oocysts of Isospora from Thraupidae Isospora from Thraupidae family family was able to accomplish a dichotomous key. These To date, 12 species of coccidia have been described should be useful in the differentiation and identification parasitizing birds of the Thraupidae family. of species, however, must observe all the structures in The first report are made for Boughton et al. (1938) detail, including those not cited in the dichotomous key, when coccidia was recoverd of four Andean tanagers, and compare them with the drawings and micrographs the southern palm tanager, Thraupis palmarum Wied, of the species description, as other characteristics may 1823, the magpie tanager, Cissopis leverianus Gmelin, arise due to evolutionary adaptation or new species 1788, the southern silver-beaked tanager, R. carbo can be observed.
Rev. Bras. Med. Vet., 32(3):182-186, jul/set 2010 183 Bruno Pereira Berto et al.
Figure 1. Comparative morphology and morphometry of Isospora spp. recorded from Thaupidae family: Isospora thraupis (Lainson, 1994) (a), I. andesensis Templar et al. (2004) (b), I. irisidornisi Metzelaars et al. (2005) (c), I. tiesangui (d), I. marambaiensis (e), I. sepetibensis (f), I. cadimi (g), I. navarroi (h), I. ramphoceli (i), I. sanhaci (j), I. sayacae (l), e I. silvasouzai (m).
184 Rev. Bras. Med. Vet., 32(3):182-186, jul/set 2010 A diagnostic tool to identify species of the genus Isospora Schneider, 1881
A dichotomous key is proposed as follows: diffuse diffuse diffuse diffuse diffuse diffuse diffuse diffuse diffuse 1a. Polar granule present ...... 2 compact diffuse or 1b. Polar granule absent ...... 3 2a. Sporocyst ellipsoidal or pear-shaped ...... 4 with large body large, ubstieda Residuum absent 2b. Sporocyst ovoid ...... 5 prominent prominent compartment collar-shaped 3a. Sporocyst height of less than 20 μm ...... 6 3b. Sporocyst height of greater than 20 μm ...... 7 4a. Stieda body knob-like and substieda body prominent tieda S granule delicate small compact delicate small compact flattenedknob-like small flattened flattened small knob-like prominent nipplelike nipplelike
prominent ...... I. sepetibensis buble-shaped 4b. Stieda body delicate and small substieda body ...... I. silvasouzai
body 5a. Stieda body triangular and substieda body absent 17.0×9.9 14.1×8.513.6×9.0 triangular 14.2x9.2 23.4×11.8 17.6×10.5 7-19x11-13) (9-17×8-11) (13-15×8-9)
(14-16x9-10) ...... I. andesensis (15-18×10-13) (14-18×10-13) rounded (21-24x12-14) (16-18x10-12) 5b. Stieda body bubble-shaped and substieda body collar-shaped ...... I. irisidornisi slightly Shape Measurements S ovoidal 16.9×11.6 ovoidal ovoidal ovoidal ovoidal ovoidal 17.7×11.5 6a. Stieda and substieda bodies delicate and barely ellipsoidalellipsoidal 16.1×10.2 16.0 × 11.4 ellipsoidal 22.6×13.0 ellipsoidal 16.9×11.0 pear-shaped pear-shaped bottle-shaped discernible ...... 8 6b. Stieda and substieda bodies discernible ...... 9 Polar absent absent absent absent absent absent absent present present present
present, 7a. Stieda body flattened and small substieda body recorded from Thraupidae family. recorded from ...... I. marambaiensis 7b. Stieda body prominent and large substieda body Wall Isospora bi-layered bi-layered bi-layered bi-layered bi-layered bi-layered bi-layered bi-layered bi-layered bi-layered bi-layered ...... I. sayacae one-layered absent 8a. Sporocyst ellipsoidal and sporozoites with a robust
Oocysts Sporocysts refractile body ...... I. navarroi (1.0-1.1) (1.0-1.1) (14-19×9-12) (1.0-1.1)(1.0-1.1)(1.0-1.2) or (15-19×9-11) (17-18×10-11) (1.0-1.1) (23-25×11-12) (1.0-1.1) (1.1-1.3) (1.1-1.3) (1.0-1.1) (1 (1.0-1.1) (1.0-1.2) 2 or 1 8a. Sporocyst pear-shaped and sporozoites with two refractile bodies ...... I. thraupis 9a. Stieda body flattened and substieda body rounded (µm) index (µm) ...... I. tiesangui 23.7×22.8 1.0 24.2×22.9 1.1 22.1×21.028.9×27.4 1.1 1.1 25.5×22.6 1.1 22.6×18.7 1.2 19.9x19.0 1.0 29.4×27.9 1.0 21.4 × 20.6 1.1 24.2 × 23.4 1.0 25.5 × 23.8 1.1 (22-26×21-24) (19-24×18-23) (22-26×21-24) (22-28×19-25) (19-24×17-23) (28-30×24-29) (19-21x19-20) (20-24×17-20) (20-25×16-23) (27-31x26-29) 9b. Stieda body nipplelike and substieda body prominent ...... I. sanhaci 9c. Stieda body prominent and knob-like and large
ovoidal 22.1×18.9 1.2 substieda body ...... I. ramphoceli spherical to sub-spherical sub-spherical sub-spherical sub-spherical sub-spherical sub-spherical sub-spherical sub-spherical sub- spherical sub- spherical sub- spherical 9d. Substieda body compartmentalized ...... I. cadimi
REFERENCES Berto B.P., Flausino W., Luz H.R., Ferreira I. & Lopes C.W.G.
Sclater, 1855Sclater, (22-26 x 21-26) Three New Coccidian Parasites of Brazilian Tanager (Ram- T. sayaca T. T. sayaca T. phocelus bresilius dorsalis) from South America. Acta Host species Shape Measurements Shape R. b. dorsalis R. b. dorsalis R. b. dorsalis R. b. dorsalis R. b. dorsalis Linnaeus, 1766 Thraupis sayaca
Iridosornis analis Protozool., 47:77-81, 2008. Thraupis palmarum dorsalis
Ramphocelus bresilius Berto B.P., Flausino W., Luz H.B., Ferreira I. & Lopes C.W.G.
Chlorospingus ophthalmicus Two new Isospora species from Brazilian tanager (Ram- phocelus bresilius dorsalis) of South America. Parasitol. Res., 105:635-639, 2009a. Berto B.P., Balthazar L.M.C., Flausino W. & Lopes C.W.G. New isosporoid coccidian parasites of sayaca tanager, Thraupis sayaca, from South America. Acta Parasitol., 54:90-94, 2009b. Berto B.P., Flausino W., Luz H.B., Ferreira I. & Lopes C.W.G.
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iridosornisi CBRO. Lista das aves do Brasil. Comitê Brasileiro de Regis-
I. navarroi I. ramphoceli I. cadimi Ferreira, Lopes, 2009 Ferreira, Lopes, 2009 Ferreira, Lopes, 2010 I. sayacae I. sanhaci I. silvasouzai I. andesensis I. Lainson, 19942004Capparella, McQuistion, McQuistion, Capparella, 2005I. tiesangui Du Bus de Gisignies, 1847 Tschudi, 1844 1821 Wied, I. thraupis Ferreira, Lopes, 2008 I. marambaiensis Isospora I. sepetibensis Ferreira, Lopes, 2008 Ferreira, Lopes, 2008ellipsoidal to (24-29 x 22-26)
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