New species of Eimeria Schneider, 1875 and Isospora Schneider ...

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Schneider, 1881 (Apicomplexa: Eimeriidae) from the short-crested flycatcher Myiarchus ferox (Gmelin). (Passeriformes: Tyrannidae) in South America. Bruno P.
Syst Parasitol (2009) 74:75–80 DOI 10.1007/s11230-009-9197-3

New species of Eimeria Schneider, 1875 and Isospora Schneider, 1881 (Apicomplexa: Eimeriidae) from the short-crested flycatcher Myiarchus ferox (Gmelin) (Passeriformes: Tyrannidae) in South America Bruno P. Berto Æ Hermes Ribeiro Luz Æ Walter Flausino Æ Ildemar Ferreira Æ Carlos W. G. Lopes Received: 21 March 2009 / Accepted: 19 May 2009 Ó Springer Science+Business Media B.V. 2009

Abstract In the current study, two new coccidian species (Protozoa: Apicomplexa: Eimeriidae) obtained from short-crested flycatcher Myiarchus ferox (Gmelin) are reported from Brazil. Isospora feroxis n. sp. has oo¨cysts which are spheroidal to subspheroidal, 18.7 9 18.0 lm, with a smooth and bilayered wall, c. 1.2 lm. The micropyle and oo¨cyst residuum are absent, but two polar granules are present. Its sporocysts are broadly ellipsoidal and 11.7 9 8.5 lm. Stieda and substieda bodies are B. P. Berto Curso de Po´s-Graduac¸a˜o em Cieˆncias Veterina´rias, Universidade Federal Rural do Rio de Janeiro (UFRRJ), Serope´dica, RJ, Brazil e-mail: [email protected] H. Ribeiro Luz  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 H. Ribeiro Luz e-mail: [email protected] I. Ferreira e-mail: [email protected] W. Flausino  C. W. G. Lopes (&) Departamento de Parasitologia Animal, Instituto de Veterina´ria, Universidade Federal Rural do Rio de Janeiro (UFRRJ), BR-465 km 7, Serope´dica, RJ 23890-000, Brazil e-mail: [email protected] W. Flausino e-mail: [email protected]

present. A sporocyst residuum is present and the sporozoites have a refractile body and nucleus. Oo¨cysts of Eimeria sicki n. sp. are spheroidal to sub-spheroidal, 30.3 9 28.5 lm, with a smooth and bi-layered wall, c. 1.3 lm. The micropyle, oo¨cyst residuum and polar granule are absent. Its sporocysts are ellipsoidal, 18.4 9 10.0 lm. Stieda and substieda bodies are present. A sporocyst residuum is present and sporozoites have a refractile body and nucleus.

Introduction The short-crested flycatcher Myiarchus ferox (Gmelin) is a bird found in Argentina, Bolivia, Brazil, Colombia, Ecuador, French Guiana, Guyana, Paraguay, Peru, Suriname, Uruguay and Venezuela. The natural habitats of this bird are subtropical or tropical moist lowland forests and heavily degraded former forest (Sick, 1997; Bird & Butchart, 2008). This species occurs over large areas, with a global extent estimated on 12,000,000 km2. Although the global population size has not been quantified, it is believed to be large based on the species occurrence being described as ‘frequent’ in many areas (Stotz et al., 1996). Coccidiosis is a parasitic disease affecting the intestinal tract of animals and caused by coccidian protozoa. The disease is transmitted from one animal to another by contact with infected faeces. The primary symptom is diarrhoea, which may contain blood in severe cases. Most animals infected with

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coccidia are asymptomatic; however, young or immuno-compromised animals may suffer severe symptoms, including death (Soulsby, 1987). The two most frequently occurring genera of coccidia found in members of the order Passeriformes are Eimeria Schneider, 1875 and Isospora Schneider, 1881. In tyrannid birds coccidia have been reported since the beginning of the 20th Century. Boughton et al. (1938) and Kawazoe et al. (1989) recovered isosporoid oo¨cysts from faeces of the eastern phoebe Sayornis phoebe Latham and blue-billed black-tyrant Knipolegus cyanirostris Vieillot, respectively. These oo¨cysts, however, were not described or named. Only a single coccidium has been described parasitising tyrannids. Berto et al. (2008) described Eimeria divinolimai Berto, Flausino, Ferreira and Lopes, 2008 parasitising the rufous casiornis Casiornis rufus Vieillot in Brazil. The current study describes two new coccidian parasites species infecting the short-crested flycatcher M. ferox on Marambaia Island, Rio de Janeiro State, Brazil.

Materials and methods Four short-crested flycatchers were captured using nets in Marambaia Island (23°040 S, 43°530 W). They were kept in individual cages, and faeces were collected immediately after defecation. After identification, the birds were released and the faecal samples were placed in plastic vials containing 2.5% potassium dichromate solution (K2Cr2O7) 1:6 (v/v). Samples were carried to the Laborato´rio de Coccı´dios e Coccidioses located at the Universidade Federal Rural do Rio de Janeiro (UFRRJ). Samples were placed in a thin layer (c. 5 mm) of K2Cr2O7 2.5% 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 and 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. Micrographs were taken

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using a digital camera (Sony model CD Mavica MVC-CD250). Size ranges are shown in parenthesis followed by average and shape index (L/W ratio). Abbreviations: total number of measurements [T], 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].

Results Four short-crested flycatchers were examined, of which one shed oocysts in the feces. Initially, the oocysts were non-sporulated, but 70% sporulated by days five and seven.

Isospora feroxis n. sp. Type-host: Myiarchus ferox (Gmelin) (Aves: Passeriformes: Tyrannidae). Type-material: Oo¨cysts are kept in 10% aqueous buffered formalin (v/v) and 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-30/2009. Type-locality: Marambaia Island (23°040 S, 43°530 W), Rio de Janeiro, Brazil. Sporulation time: Five days. Site of infection: Not investigated. Etymology: The specific epitaph is derived from the specific name of the host, M. ferox. Description (Figs. 1a–d, 3c,d) Sporulated oo¨cyst Oo¨cyst shape (T = 10) spheroidal to sub-spheroidal; number of walls 2; wall thickness 1.2 (1–2); outer wall smooth, ca. 2/3 of total thickness; L 9 W = 18.7 9 18.0 (18–20 9 17–20), with L/W ratio = 1.1 (1.0–1.1); M and O: absent; P: present, usually 2. Sporocyst and sporozoites Sporocyst shape (T = 10) ovoidal; L 9 W = 11.7 9 8.5 (11–13 9 8–10); L/W ratio = 1.4 (1.0–1.5);

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Fig. 1 Line drawings of Isospora feroxis n. sp.: a. Sporulated oo¨cyst with variations (b–d) of the Stieda and substieda bodies. Scalebar: a, 10 lm; b–d, 5 lm

SB present, flattened, 0.3 high 9 1.2 wide; SSB present, prominent, 1.2 high 9 2.5 wide; PSB absent; SR present, composed of spherules of different sizes; SZ vermiform with 1 large, posterior SRB and centrally located N.

Etymology: The specific epitaph is derived from the family name of the ornithologist Dr Helmut Sick in recognition of his contribution to the systematics of Brazilian birds. Description (Figs. 2a–c, 3a,b)

Eimeria sicki n. sp. Type-host: Myiarchus ferox (Gmelin) (Aves: Passeriformes: Tyrannidae). Type-material: Oo¨cysts are kept in 10% aqueous buffered formalin (v/v) and 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-31/2009. Type-locality: Marambaia Island (23°040 S, 43°530 W), Rio de Janeiro, Brazil. Sporulation time: Seven days. Site of infection: Not investigated.

Sporulated oo¨cyst Oo¨cyst shape (T = 10) spheroidal to sub-spheroidal; number of walls 2; wall thickness 1.3 (1–2); outer wall smooth, c. 2/3 of total thickness; L 9 W = 30.3 9 28.5 (29–32 9 26–30), with L/W ratio = 1.1 (1.0–1.2); M, OR and PG all absent. Sporocyst and sporozoites Sporocyst shape (T = 10): ellipsoidal; L 9 W = 18.4 9 10.0 (18–19 9 9–11); L/W ratio = 1.8 (1.7–2.0); SB present, flattened, slight, 0.5 high 9 2.8 wide; SSB present, prominent, 2.4 high 9 3.0 wide; PSB absent; SR present, composed of many scattered granules and spherules of different sizes; SZ vermiform with 1 large, posterior SRB and a centrally located N.

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Fig. 2 Line drawings of Eimeria sicki n. sp.: a. Sporulated oo¨cyst variations (b, c) of the Stieda and substieda bodies. Scale-bar: a, 10 lm; b, c, 5 lm

Discussion In agreement with Grulet et al. (1982) and Berto et al. (2009), certain variations (Figs. 1b–d, 2b,c) also were observed in the SB and SSB. These variations are not significant enough to separate and describe them as new species, and could possibly be 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. According to Duszynski & Wilber (1997), a new coccidian species should be compared in detail with coccidian species that are feature-similar and belong to the same host family. Therefore, due to the lack of descriptions of isosporoid coccidian parasites from tyrannids, I. feroxis n. sp. was compared with species of feature-similar families. According to Prum (1990), Birdsley (2002) and Barber and Rice (2007), the

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Cotingidae and Pipridae are morphologically and phylogenetically similar to the Tyrannidae. From these families, only a single isosporoid coccidium has been described, i.e. I. araponga Dolezˇalova´, Torres Ferna´ndez & Modry´, 2004, as parasitising a bare-throated bellbird Procnias nudicollis (Vieillot) (see Dolezˇalova´ et al., 2004). I. araponga can easily be differentiated from I. feroxis because it presents ellipsoidal oo¨cysts, asymmetrical sporocysts and an indistinguishable SSB. It is necessary to compare E. sicki n. sp. with E. divinolimai, because it is the only eimeriid coccidium described from the families Tyrannidae, Cotingidae or Pipridae. This species has oo¨cysts smaller those of E. sicki and has no SSB. Based on their morphological features, both new coccidial species described above are considered as new to science. Isospora feroxis n. sp. represents the first Isospora species described from the Tyrannidae,

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Fig. 3 Micrographs of sporulated oo¨cysts: a, b. Eimeria sicki n. sp.; c, d. Isospora feroxis N. sp. Scale-bar: 10 lm

whereas Eimeria sicki n. sp. is the tenth eimerian species described from the order Passeriformes. Acknowledgements We are thankful to the Brazilian Navy, especially to the commander of CADIM (Centro de Adestramento da Ilha da Marambaia), who enabled our access to Marambaia Island. We are also grateful for the use of some of the facilities of CADIM during the fieldwork.

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