Research Article |
Corresponding author: Bruno P. Berto ( berto.ufrrj@gmail.com ) Academic editor: Marcus V. Domingues
© 2018 Irlane F. de Pinho, Lidiane M. da Silva, Mariana B. Rodrigues, Bruno do B. Lopes, Mariana S. Oliveira, Hermes R. Luz, Ildemar Ferreira, Carlos Wilson G. Lopes, Bruno P. Berto.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
de Pinho IF, da Silva LM, Rodrigues MB, Lopes BB, Oliveira MS, Luz HR, Ferreira I, Lopes CWG, Berto BP (2018) Isospora machadoae sp. nov. (Protozoa: Apicomplexa: Eimeriidae), a new coccidian species from white-necked thrushes Turdus albicolis (Passeriformes: Turdidae) of South America. Zoologia 35: 1-4. https://doi.org/10.3897/zoologia.35.e24570
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A new coccidian species parasitizing white-necked thrushes Turdus albicollis Vieillot, 1818 is described from the Parque Nacional do Itatiaia, in Southeastern Brazil. Isospora machadoae sp. nov. has oocysts that are sub-spherical, 22.2 × 21.2 µm, with bilayered wall, ~1.3 μm thick. Outer layer is rough with micropyle and micropyle cap. Oocyst residuum is absent, but one or two polar granules are present. Sporocysts are ellipsoidal, 13.3 × 9.7 µm. The Stieda body is flattened to half-moon-shaped and substieda body rounded. Sporocyst residuum is present, composed of scattered spherules of different sizes. Sporozoites are vermiform with a refractile body and a nucleus. These parasitized thrushes had no apparent clinical signs of coccidiosis or high densities of oocysts in feces. This condition may be associated with a specific low pathogenicity of I. machadoae sp. nov. and/or with the conserved habitat of these birds, which ensures the ecological niches and thus the immunocompetence to wildlife.
Taxonomy, coccidia , oocysts, wild birds, Parque Nacional do Itatiaia
Brazil has a wide and diverse avifauna, with more than 1,900 species (
White-necked thrushes Turdus albicollis Vieillot, 1818 are birds found in several South American countries (
Similarly to other vertebrates, birds can be parasitized by coccidia, which are predominantly protozoan parasites of the intestine, and may be associated with behavioral and physiological changes, morbidity and mortality in different species of birds (
The coccidia have feco-oral transmission and can be identified and described by exogenous forms shed in the feces: the oocysts (
The aim of this study was to examine the feces from white-necked thrushes T. albicollis to determine what coccidian parasites were present. These white-necked thrushes were captured in and around the Parque Nacional do Itatiaia, in Southeastern Brazil.
Three expeditions were conducted in two localities in Southeastern Brazil: (1) Parque Nacional do Itatiaia, a protected area with a high degree of vulnerability, located in the Serra da Mantiqueira on the border of the States of Rio de Janeiro, Minas Gerais and São Paulo; and (2) Visconde de Mauá, which is a district near the Parque Nacional do Itatiaia boundary. Sampling occurred in March 2015 and October 2016 in the Parque Nacional do Itatiaia (22°27'38"S, 44°35'34"W), and March 2016 in Visconde de Mauá (22°19'46"S, 44°32'11"W). A total of eleven T. albicollis (seven from the Parque Nacional do Itatiaia and four from Visconde de Mauá) were captured. The birds were kept in individual boxes and feces collected immediately after defecation. After identification of the species, the bird was photographed and released and stool samples were placed in centrifuge tubes containing a potassium dichromate 2.5% (K2Cr2O7) solution at 1:6 (v/v). Samples were carried to the Laboratório de Biologia de Coccídios, Departamento de Biologia Animal, Instituto de Ciências Biológicas e da Saúde, Universidade Federal Rural do Rio de Janeiro (UFRRJ). Samples were incubated at room temperature for 10 days or until ~70 % of the oocysts were sporulated. Oocysts were isolated by flotation in Sheather’s sugar solution (Specific gravity: 1.20) and examined microscopically using the technique described by
Fecal samples of four of the eleven white-necked thrushes examined had oocysts with morphotype still unreported in the scientific literature, and it is bellow described as a new species.
Among all coccidian species recorded from Turdidae in the New World, only I. machadoae sp. nov. has an oocyst wall rough with micropyle and micropyle cap, which are very uncommon characteristic features in Isospora spp. from Passeriformes (Table
Oocyst (n = 35) spherical to sub-spherical, 21–24 × 20–23 (22.2 × 21.2); length/width (L/W) ratio 1.0–1.2 (1.1). Wall bi-layered, 1.2–1.5 (1.3) thick, outer layer rough, with 2/3 of total thickness. Micropyle present with 7.0 wide. Micropyle cap present with slight protrusion, but barely discernible in some oocysts (Figs
White-necked thrush Turdus albicollis Vieillot, 1818 (Aves: Passeriformes: Turdidae).
Type material. Phototypes, line drawing, half of the oocysts in 10 % aqueous buffered formalin (v/v) and the other half in 70 % ethanol are deposited at the Museu de Zoologia da Universidade Federal Rural do Rio de Janeiro, Brazil, under accession number MZURPTZ2017001. Phototypes and line drawings are also deposited and available (http://r1.ufrrj.br/labicoc/colecao.html) in the Parasitology Collection of the Laboratório de Biologia de Coccídios, at UFRRJ, under repository number P-70/2016. Photographs of the type-host specimen (symbiotype) are deposited in the same collection.
Parque Nacional do Itatiaia (22°27'38"S, 44°35'34"W), Southeastern Brazil.
Visconde de Mauá (22°19'46"S, 44°32'11"W), Southeastern Brazil.
The specific name is derived from the family name of a Brazilian parasitologist Dr Rosangela Zacarias Machado, given in her honor for her contribution to the study of Protozoa.
According to
Sporulated oocysts of Isospora machadoae sp. nov. recovered from Turdus albicolis from Brazil: (1) line drawing; (2) photomicrographs. Note the micropyle and micropyle cap (m/mc), nucleus (n), polar granule (pg), refractile body (rb), rough oocyst wall (row), Stieda (sb) and sub-Stieda bodies (ssb) and the sporocyst residuum (sr). Scale bar = 10 µm.
Comparative morphology of Isospora spp. recorded from Turdidae of the New World.
Coccidia | Hosts | References | Oocysts | Sporocysts | |||||||||||||
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Shape | Length (µm) | Width (µm) | L/W ratio | Wall | Micropyle | Micropyle cap | Polar granule | Shape | Length (µm) | Width (µm) | L/W ratio | Stieda body | Substieda body | Residuum | |||
Isospora phaeornis | Myadestes obscurus |
|
Ellipsoidal | 25–28 (27) | 18–20 (19) | – | Smooth | absent | Absent | Present | Ovoidal | 15–18 (16) | 10–11 (11) | – | Present | Present | Compact |
Isospora robini | Turdus migratorius |
|
Ellipsoidal or ovoid | 20–28 (23) | 16–22 (20) | (1.2) | Smooth | absent | Absent | Present | Ovoid | 10–17 (13.8) | 7–12 (9.0) | (1.5) | Nipple-like | Present, prominent | Compact |
Isospora tucuruiensis | Turdus albicollis |
|
Sub-spherical | 15–19 (17.3) | 14–19 (17.1) | – | Smooth | absent | Absent | Present, single, ~ 3 × 2 | Ellipsoidal | 10–13 (11.8) | 7–10 (8.4) | – | Nipple-like | Present, wide, ~ 0.5 × 1.5 | Diffuse or compact |
Isospora albicollis | T. albicollis |
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Ovoidal | 22–27 (24.5) | 19–24 (20.3) | – | Smooth | present | Absent | Present, single, ~ 2.5 × 2 | Ellipsoidal | 12–15 (16.0) | 8–10 (11.2) | – | Nipple-like to bubble-shaped | Present, wide, ~ 1.0 × 4 | Diffuse or compact |
Isospora zorzali | Catharus aurantiirostris |
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Round to slightly ovoid | 16–24 (19.7) | 15–21 (18.6) | (1.1) | Smooth | absent | Absent | Present,1 to 2 | Ovoidal | 11–18 (14.5) | 7–11 (8.5) | (1.7) | Nipple-like | Absent | Diffuse or compact |
Isospora massardi | T. albicollis |
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Sub-spherical | 15–21 (18.6) | 14–19 (17.7) | 1.0–1.1 (1.1) | Smooth | absent | Absent | Present, 2 ellipsoidal Granules, 1.5 × 0.5 | Ovoidal | 13–16 (14.8) | 8–11 (9.3) | 1.4–1.8 (1.6) | Knob-like to rounded, 1 × 2 | Present, rounded, 1.5 × 3.5 | Diffuse |
Isospora machadoae | T. albicollis | Current work | Sub-spherical | 21–24 (22.2) | 20–23 (21.2) | 1.0–1.2 (1.1) | Rough | present | Present | Present, 1 to 2, sub-spherical and robust | Ellipsoidal | 12–14 (13.3) | 9–11 (9.7) | 1.2–1.5 (1.4) | Present, flattened to half-moon-shaped, 0.5 × 1.5 | Present, rounded, 1.5 × 2.5 | Diffuse |
This study was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ). Field-collecting permits were issued to B.P. Berto and C.W.G. Lopes by SISBIO/ICMBio (licenses 42798-1, 45200-1, 49605-1) and CEUA/UFRRJ (protocols IV-036/2014, ICBS-269 008/2015). We are thankful to staff at the Parque Nacional do Itatiaia, mainly to the research coordinator Léo Nascimento, that allowed us to access and use some facilities during the expeditions.