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Revista Brasileira de Parasitologia Veterinária

Print version ISSN 0103-846XOn-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.26 no.2 Jaboticabal Apr./June 2017  Epub Apr 13, 2017

https://doi.org/10.1590/s1984-29612017006 

Short Communication

Isospora albicollis (Apicomplexa: Eimeriidae) in thrushes Turdus spp. (Passeriformes: Turdidae), in southeastern Brazil

Isospora albicollis (Apicomplexa: Eimeriidae) em sabiás Turdus spp. (Passeriformes: Turdidae), no sudeste Brasileiro

Irlane Faria de Pinho1 

Lidiane Maria da Silva1 

Mariana Borges Rodrigues1 

Mariana de Souza Oliveira2 

Bruno do Bomfim Lopes3 

Hermes Ribeiro Luz4 

Ildemar Ferreira5 

Carlos Wilson Gomes Lopes4 

Bruno Pereira Berto5  * 

1Programa de Pós-graduação em Ciências Veterinárias, Universidade Federal Rural do Rio de Janeiro – UFRRJ, Campus Seropédica, Seropédica, RJ, Brasil

2Programa de Pós-graduação em Biologia Animal, Universidade Federal Rural do Rio de Janeiro – UFRRJ, Campus Seropédica, Seropédica, RJ, Brasil

3Programa de Pós-graduação em Ciência, Tecnologia e Inovação em Agropecuária, Universidade Federal Rural do Rio de Janeiro – UFRRJ, Campus Seropédica, Seropédica, RJ, Brasil

4Departamento de Parasitologia Animal, Instituto de Veterinária, Universidade Federal Rural do Rio de Janeiro – UFRRJ, Campus Seropédica, Seropédica, RJ, Brasil

5Departamento de Biologia Animal, Instituto de Ciências Biológicas e da Saúde, Universidade Federal Rural do Rio de Janeiro – UFRRJ, Campus Seropédica, Seropédica, RJ, Brasil


Abstract

The aim of the present study was to report and describe Isospora albicollis Lainson and Shaw, 1989 parasitizing a white-necked thrush Turdus albicollis Vieillot, 1818 and a pale-breasted thrush Turdus leucomelas Vieillot, 1818 in two different localities: the Itatiaia National Park and Cacaria, in southeastern Brazil. The oocysts identified were ovoidal, 24.4 × 19.7 μm, with a smooth, bilayered wall, around 1.4 μm thick. Oocyst residuum was absent, but a micropyle and a polar granule were present. The sporocysts were ellipsoidal, 15.4 × 10.1 μm. The Stieda body was knob-like to rounded and the sub-Stieda body was prominent and wide. Sporocyst residuum was present, usually as a cluster of granules that appear to be membrane-bounded. The sporozoites were vermiform with one posterior refractile body and a centrally located nucleus. Besides recording the new host T. leucomelas, the identification of I. albicollis in the Itatiaia National Park and Cacaria, in southeastern Brazil, provide records of new localities for its parasitism, and reveals the wide distribution and dispersion of this coccidium in Brazil.

Keywords:  Coccidia; oocysts; Taxonomy; Ecology; Parque Nacional do Itatiaia; Cacaria

Resumo

O objetivo do presente estudo foi relatar e descrever Isospora albicollis Lainson e Shaw, 1989, parasitando um sabiá-coleira Turdus albicollis Vieillot, 1818 e um sabiá-barranco Turdus leucomelas Vieillot 1818, em duas localidades diferentes: Parque Nacional do Itatiaia e Cacaria, no Sudeste do Brasil. Os oocistos identificados foram ovóides, 24,4 × 19,7 μm, com uma parede lisa e dupla, com cerca de 1,4 μm de espessura. Resíduo do oocisto foi ausente, mas uma micrópila e um grânulo polar foram presentes. Esporocistos elipsoidais, 15,4 × 10,1 μm, corpo de Stieda em forma de botão a arredondado e corpo de sub-Stieda proeminente e largo. Resíduo do esporocisto presente, usualmente como um aglomerado de grânulos que parecem estar envolvidos por uma membrana. Esporozoítos vermiformes com um corpo refráctil posterior e um núcleo centralizado. Além de registrar o novo hospedeiro T. leucomelas, a identificação de I. albicollis no Parque Nacional de Itatiaia e Cacaria, no Sudeste do Brasil, fornece registros de novas localidades para seu parasitismo e revela a ampla distribuição e dispersão desse coccídio no Brasil.

Palavras-chave:  Coccidia; oocistos; Taxonomia; Ecologia; Parque Nacional do Itatiaia; Cacaria

Introduction

The thrushes Turdus spp. are passerines of the Turdidae family widely distributed in South America. In Brazil, they are abundant in the Atlantic and Amazon forests, preferentially inhabiting damp areas of taller trees on hillslopes, but also found near the ground feeding on small fruits and insects (SICK, 1997; IUCN, 2012).

Infections caused by isosporoid coccidia in Passeriformes are very common and are associated with several factors. As in most types of coccidiosis, there is a balance between the parasite and its host, but parasitism may possibly lead to cell death in the host during parasite development, causing clinical signs of variable severity. This evolution may arise when there is an imbalance, mainly associated with low immunity in the host (MARQUES et al., 2011).

Among the several Isospora spp. recorded in Turdidae worldwide, Isospora tucuruiensis Lainson and Shaw, 1989, Isospora albicollis Lainson and Shaw, 1989, and Isospora massardi Lopes, Berto, Luz, Galvão, Ferreira and Lopes, 2014, have been described from the white-necked thrush Turdus albicollis Vieillot, 1818; however, no species has been described or reported from the pale-breasted thrush Turdus leucomelas Vieillot, 1818. Lopes et al. (2014) described I. massardi from white-necked thrushes on Marambaia Island in the state of Rio de Janeiro, whereas Lainson & Shaw (1989) described I. albicollis and I. tucuruiensis from white-necked thrushes on Tocantins Island in the state of Pará, Brazil.

In this context, the aim of the present study was to report and describe I. albicollis from T. albicollis in the Itatiaia National Park and T. leucomelas in Cacaria, in southeastern Brazil.

Materials and Methods

Two expeditions were conducted in two different localities in southeastern Brazil: (1) Itatiaia National Park (22° 27' 38” S, 44° 35' 34” W), 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 (ICMBIO, 2016); and (2) Cacaria (22° 42' 51” S, 43° 50' 38” W) at the Municipality of Piraí in the State of the Rio de Janeiro.

Three specimens of T. albicollis were caught in the expedition to the Itatiaia National Park in March 2015, and two specimens of T. leucomelas were caught in the expedition to Cacaria in June 2016. The thrushes were caught using mist nets, kept in individual boxes and feces were collected immediately after defecation. After identification of the species, the thrushes were photographed and released. The stool samples were placed in centrifuge tubes containing 2.5% potassium dichromate (K2Cr2O7) solution at 1:6 (v/v). The samples were taken 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) where they were incubated at room temperature for one week. Oocysts were isolated by means of flotation in Sheather’s sugar solution (specific gravity, 1.20) and were examined under a microscope using the technique described by Duszynski & Wilber (1997) and Berto et al. (2014). Morphological observations, line drawings, photomicrographs and measurements were made using an Olympus BX binocular microscope coupled to a digital camera (Eurocam 5.0). Line drawings were edited using two software applications from CorelDRAW® (Corel Draw Graphics Suite, version 11.0, Corel Corporation, Canada), i.e. Corel DRAW and Corel PHOTO-PAINT. All measurements were made in micrometers and are presented as the range followed by the mean in parentheses. Field-collecting permits were issued to B.P. Berto and C.W.G. Lopes by SISBIO/ICMBio (licenses 42798-1; 45200-1) and CEUA/UFRRJ (protocols IV-036/2014; ICBS-008/2015).

Results

Three white-necked thrushes T. albicollis and two pale-breasted thrushes T. leucomelas were caught and their fecal samples were examined. One of each species shed oocysts that were identified as I. albicollis.

Isospora albicollis Lainson and Shaw, 1989

(Figures 1, 2A-D)

Figure 1 Composite line drawing of a sporulated oocyst of Isospora albicollis from thrushes Turdus spp. in southeastern Brazil. Scale-bar: 10 µm. 

Figure 2 Photomicrographs of sporulated oocysts of Isospora albicollis from the white-necked thrush Turdus albicollis (A-C) and from the pale-breasted thrush Turdus leucomelas (D) in southeastern Brazil. Scale-bar: 10 µm. 

Hosts: white-necked thrush Turdus albicollis Vieillot, 1818 (Passeriformes: Turdidae); pale-breasted thrush Turdus leucomelas Vieillot, 1818 (Passeriformes: Turdidae).

Material examined: Oocysts in 70% ethanol, photomicrographs and line drawings have been deposited and are available (http://r1.ufrrj.br/labicoc/colecao.html) in the Parasitology Collection of the Laboratório de Biologia de Coccídios, at UFRRJ, located in Seropédica, Rio de Janeiro, Brazil. Photographs of the host specimens have been deposited in the same collection. The repository number is 67/2016.

Diagnosis: According to Duszynski & Wilber (1997) and Berto et al. (2011), a coccidian species should be compared in detail with coccidian species that are feature-similar and belong to the same host family. Among all coccidian species recorded from Turdidae in the New and Old Worlds (BERTO et al., 2011; CARDOZO et al., 2015), only I. albicollis has a micropyle, which is a very uncommon characteristic feature in Isospora spp. In addition, all the morphological and morphometric characteristics of the oocysts observed in the present study were very similar to those of the original description of the oocysts of I. albicollis by Lainson & Shaw (1989), and were observed from the same host species. Thus, the oocysts shed by T. albicollis and T. leucomelas in the current study were easily identified as I. albicollis.

Description: Oocyst shape (n = 11) ovoidal; 23-26 × 18-22 (24.4 × 19.7) length/width (L/W) ratio 1.2-1.4 (1.24). Wall bilayered, 1.2-1.6 (1.4) thick, outer layer smooth, around two-thirds of total thickness. Micropyle present, without micropyle cap or wrinkles; however, generally with slight invagination of the inner layer. Oocyst residuum absent; but one polar granule present. Sporocysts (n = 11), ellipsoidal, 14-17 × 9-11 (15.4 × 10.1); L/W ratio 1.5-1.6 (1.52). Stieda body present, knob-like to rounded, 1.7 high, 1.3 wide; sub-Stieda body present, prominent and wide, 1.5 high, 3.1 wide; para-Stieda body absent. Sporocyst residuum present, usually as a cluster of granules that appear to be membrane-bounded. Sporozoite vermiform with one posterior refractile body and a centrally located nucleus.

Localities: Itatiaia National Park (22° 27’ 38” S, 44° 35’ 34” W) and Cacaria (22° 42’ 51” S, 43° 50’ 38” W), southeastern Brazil.

Prevalence: 2 of 5 (40%).

Discussion

Passerines establish a dynamic ecosystem beyond the physical aspects of diversity and behavioral biology, and perform several functions in the environment such as biological control of ants and ticks and seed dispersal (SEKERCIOGLU, 2006). In addition, these birds are host to a wide variety of parasites, which develop an adaptive mode of life in the body and can cause severe diseases that have an impact on the host’s survival and reproduction and can affect various aspects of the host’s life (DOLNIK et al., 2009).

Coccidiosis is a parasitic disease affecting the intestinal tract of vertebrates caused by coccidian Protozoa. This infection in wild birds in a habitat with favorable stable conditions is rarely a significant problem; however, symptomatic disease may occur when natural factors (changes, reproduction, heat, cold, migration, etc.) and/or anthropogenic factors (habitat loss, pollution, urbanization, agricultural activities, etc.) have an impact, thus contributing towards stress and changing the birds’ behavior (ATKINSON et al., 2008). Coccidiosis may give rise to severe symptoms in young or immunocompromised birds, including death (SOULSBY, 1985; GIRAUDEAU et al., 2014). In this context, thrushes are potential models for observing the dynamics of Isospora spp. and the intensity of infection that is associated with several natural and anthropogenic environmental factors. Thrushes have high species richness, great diversity and wide geographic distribution. The species present greater or lesser adaptability to anthropogenic environments (SICK, 1997; CBRO, 2014).

Isospora albicollis was originally described from white-necked thrushes in the state of Pará by Lainson & Shaw (1989). The type locality, Tocantins Island, no longer exists because it was flooded as part of the Tucuruí hydroelectric scheme. The Itatiaia National Park and Cacaria, which are the new localities recorded in the present study are located at a distance of more than 2,800 km. In this regard, the wide distribution and dispersion of this coccidium in Brazil is noteworthy. Recently, Avendaño et al. (2013) investigated the dispersion of Turdus nudigenis Lafresnaye, 1848 in South America, and found that it migrated long distances. They suggested that the influence of the accelerated rate of habitat loss, fragmentation of natural forests and global warming might be having an effect regarding migration. In this manner, it can be seen that the wide distribution and migration of these species, combined with these predisposing factors, have promoted dispersion of I. albicollis, and probably other parasites, to other susceptible hosts in distant localities.

In conclusion, the present study identifies I. albicollis from the white-necked thrush T. albicollis and from the pale-breasted thrush T. leucomelas, in Itatiaia National Park and Cacaria respectively. Therefore, T. leucomelas becomes a new host for I. albicollis and the records of these new localities in southeastern Brazil reveals the wide distribution and dispersion of this coccidium in Brazil.

Acknowledgements

We are thankful to staff at the Parque Nacional do Itatiaia, mainly to the research coordinator Dr. Léo Nascimento; and the landowner at Cacaria in the Municipality of Piraí, RJ, that allowed us to access and use some facilities during the expeditions. This study was supported by grants from the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

References

Atkinson CT, Thomas NJ, Hunter DB. Parasitic diseases of wild birds. Oxford: Wiley-Blackwell; 2008. [ Links ]

Avendaño JE, Cortés-Herrera JO, Briceño-Lara ER, Rincón-Guarín DA. Crossing or bypassing the Andes: a commentary on recent range extensions of cis-Andean birds to the West of the Andes of Colombia. Orinoquia 2013; 17(2): 207-214. [ Links ]

Berto BP, Flausino W, McIntosh D, Teixeira-Filho WL, Lopes CWG. Coccidia of new world passerine birds (Aves: Passeriformes): a review of Eimeria Schneider, 1875 and Schneider, 1881 (Apicomplexa: Eimeriidae). IsosporaSyst Parasitol 2011; 80(3): 159-204. PMid:22002022. http://dx.doi.org/10.1007/s11230-011-9317-8. [ Links ]

Berto BP, McIntosh D, Lopes CWG. Studies on coccidian oocysts (Apicomplexa: Eucoccidiorida). Rev Bras Parasitol Vet 2014; 23(1): 1-15. PMid:24728354. http://dx.doi.org/10.1590/S1984-29612014001. [ Links ]

Cardozo SV, Berto BP, Fonseca IP, Tomás A, Thode FRPB, Lopes CWG. Characterisation of Isospora lusitanensis n. sp. (Apicomplexa: Eimeriidae) from the Eurasian blackbird Linnaeus (Passeriformes: Turdidae) in mainland Portugal. Turdus merulaSyst Parasitol 2015; 92(2): 171-179. PMid:26358076. http://dx.doi.org/10.1007/s11230-015-9590-z. [ Links ]

Comitê Brasileiro de Registros Ornitológicos – CBRO. Lista das aves do Brasil. Rio de Janeiro: CBRO; 2014. [ Links ]

Dolnik OV, Von Ronn JAC, Bensch S. sp. n. (Apicomplexa: Eimeriidae), a new coccidian parasite found in the Pied Flycatcher (. Isospora hypoleucaeFicedula hypoleuca)Parasitology 2009; 136(8): 841-845. PMid:19450377. http://dx.doi.org/10.1017/S0031182009006131. [ Links ]

Duszynski DW, Wilber P. A guideline for the preparation of species descriptions in the Eimeriidae. J Parasitol 1997; 83(2): 333-336. PMid:9105325. http://dx.doi.org/10.2307/3284470. [ Links ]

Giraudeau M, Mousel M, Earl S, McGraw K. Parasites in the city: degree of urbanization predicts poxvirus and coccidian infections in house finches (Haemorhous mexicanus). PLoS One 2014; 9(2): e86747. PMid:24503816. http://dx.doi.org/10.1371/journal.pone.0086747. [ Links ]

Instituto Chico Mendes de Conservação e Biodiversidade – ICMBIO. Unidades de Conservação: Parque Nacional de Itatiaia. Itatiaia; 2016. [cited 2016 Oct 17]. Available from: http://www.icmbio.gov.br/parnaitatiaia. [ Links ]

Lainson R, Shaw JJ. Two new species of and three new species of (Apicomplexa, Eimeriidae) from Brazilian mammals and birds. EimeriaIsosporaBull Mus Natl Hist Nat 1989; 11(2): 349-365. [ Links ]

Lopes BB, Berto BP, Luz HR, Galvão GS, Ferreira I, Lopes CWG. Isospora massardi sp. nov. (Apicomplexa: Eimeriidae) from the white-necked thrush (Passeriformes: Turdidae) from Brazil. Turdus albicollisActa Parasitol 2014; 59(2): 272-275. PMid:24827098. http://dx.doi.org/10.2478/s11686-014-0240-4. [ Links ]

Marques MV, Vilela DA, Andrade EA, Galvão CZ, Resende JS, Ferreira-Junior FC, et al. Fatal coccidiosis by Isospora icterus (Upton & Whitaker, 2000) in captive campo Troupial (Icterus jamacaii) in Brazil. J Zoo Wildl Med 2011; 42(4): 735-737. PMid:22204073. http://dx.doi.org/10.1638/2010-0229.1. [ Links ]

Sekercioglu CH. Increasing awareness of avian ecological function. Trends Ecol Evol 2006; 21(8): 464-471. PMid:16762448. http://dx.doi.org/10.1016/j.tree.2006.05.007. [ Links ]

Sick H. Ornitologia Brasileira. Brasília: Nova Fronteira; 1997. [ Links ]

Soulsby EJ. Advances in immunoparasitology. Vet Parasitol 1985; 18(4): 303-319. PMid:3911547. http://dx.doi.org/10.1016/0304-4017(85)90066-4. [ Links ]

The IUCN Red List of Threatened Species – IUCN. Turdus albicollis. Cambridge: IUCN; 2012 [cited 2016 Oct 17]. Available from: http://dx.doi.org/10.2305/IUCN.UK.2012-1.RLTS.T22708942A39741540.en. [ Links ]

Received: November 08, 2016; Accepted: February 06, 2017

*Corresponding autor: Bruno Pereira Berto. Departamento de Biologia Animal, Instituto de Ciências Biológicas e da Saúde, Universidade Federal Rural do Rio de Janeiro – UFRRJ, BR-465, Km 7, CEP 23897-000, Seropédica, RJ, Brasil. e-mail: berto.ufrrj@gmail.com

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