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Coccidial Dispersion Across New World Marsupials: Klossiella Tejerai

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Coccidial Dispersion Across New World Marsupials: Klossiella Tejerai Syst Parasitol (2014) 89:83–89 DOI 10.1007/s11230-014-9510-7 Coccidial dispersion across New World marsupials: Klossiella tejerai Scorza, Torrealba & Dagert, 1957 (Apicomplexa: Adeleorina) from the Brazilian common opossum Didelphis aurita (Wied-Neuwied) (Mammalia: Didelphimorphia) Caroline Spitz dos Santos • Bruno Pereira Berto • Bruno do Bomfim Lopes • Matheus Dias Cordeiro • Adivaldo Henrique da Fonseca • Walter Leira Teixeira Filho • Carlos Wilson Gomes Lopes Received: 11 June 2014 / Accepted: 14 July 2014 Ó Springer Science+Business Media Dordrecht 2014 Abstract Klossiella tejerai Scorza, Torrealba & recovered from urine samples were ellipsoidal, Dagert, 1957 is a primitive coccidian parasite reported 20.4 9 12.7 lm, with sporocyst residuum composed from the New World marsupials Didelphis marsupialis of scattered spherules and c.13 sporozoites per sporo- (Linnaeus) and Marmosa demerarae (Thomas). The cyst, with refractile bodies and nucleus. Macrogametes, current work describes K. tejerai from the Brazilian microgametes, sporonts, sporoblasts/sporocysts were common opossum Didelphis aurita (Wied-Neuwied) in identified within parasitophorous vacuoles of epithelial Southeastern Brazil, evidencing the coccidial dispersion cells located near the renal corticomedullary junction. across opossums of the same family. The sporocysts Didelphis marsupialis should not have transmitted K. tejerai to D. aurita because they are not sympatric; however M. demerarae is sympatric with D. marsupialis C. S. dos Santos Á M. D. Cordeiro and D. aurita. Therefore, D. aurita becomes the third Curso de Po´s-Graduac¸a˜o em Cieˆncias Veterina´rias, host species for K. tejerai in South America. Universidade Federal Rural do Rio de Janeiro (UFRRJ), BR-465 km 7, 23897-970 Serope´dica, RJ, Brazil & B. P. Berto ( ) Introduction Departamento de Biologia Animal, Instituto de Biologia, UFRRJ, BR-465 km 7, 23897-970 Serope´dica, RJ, Brazil e-mail: [email protected] Opossums in the New World represent 99 different species. The vast majority of these (95 species, 96%) B. do Bomfim Lopes inhabits South America. Didelphis spp. are common in Programa de Po´s-graduac¸a˜o em Cieˆncia, Tecnologia e Inovac¸a˜o em Agropecua´ria, UFRRJ, BR-465 km 7, South America; however, one of the six species, 23897-970 Serope´dica, RJ, Brazil Didelphis virginiana (Kerr) has distribution in North and Central Americas (IUCN, 2014). A. H. da Fonseca Didelphis spp. became epidemiologically relevant Departamento de Epidemiologia e Sau´de Pu´blica, Instituto de Veterina´ria, UFRRJ, BR-465 km 7, in the New World when they were identified as 23897-970 Serope´dica, RJ, Brazil definitive hosts for some coccidian parasites of the genus Sarcocystis Lankester, 1882. Among these W. L. T. Filho Á C. W. G. Lopes Sarcocystis spp., Sarcocystis neurona Dubey, Davis, Departamento de Parasitologia Animal, Instituto de Veterina´ria, UFRRJ, BR-465 km 7, Speer, Bowman, Lahunta, Granstrom, Topper, Hamir, 23897-970 Serope´dica, RJ, Brazil Cummings & Suter, 1991 is recognised as the 123 84 Syst Parasitol (2014) 89:83–89 et al., 1976) and from the woolly mouse opossum Marmosa demerarae (Thomas) in Guyana (Boulard, 1975). The present study describes K. tejerai infecting a Brazilian common opossum Didelphis aurita (Wied- Neuwied) in Southeastern Brazil, evidencing the coccidial dispersion across opossums of the same family. Materials and methods Twenty opossums D. aurita were captured on and around the Campus of the Federal Rural University of Rio de Janeiro (Universidade Federal Rural do Rio de Janeiro – UFRRJ), located in the municipality of Serope´dica (22°440S, 43°420W), state of Rio de Janeiro, Brazil. The opossums were transported to the Veterinary Institute (Instituto de Veterina´ria – IV) at the UFRRJ, and were reared and fed in small enclo- sures approximately 1 9 1 m. Feed and water were administered ad libitum. The capture, maintenance and collection of samples was approved by UFRRJ Ethics Committee under protocol No. 255/2012 and author- ised by Brazilian Institute of Environment and Natural Renewable Resources (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renova´veis – IBAMA) under protocol # 34701-2. Sample pro- cessing and data analysis were conducted at the Laboratory of Coccidia and Coccidiosis (Laborato´rio Fig. 1 Urinary sporocysts of Klossiella tejerai from the de Coccı´dios e Coccidioses – LCC) located at UFRRJ. Brazilian common opossum Didelphis aurita. A, Composite Urine samples were collected and placed in plastic line drawing; B–C, Photomicrographs. Scale-bars:10lm vials. Sporocysts of Klossiella spp. were recovered by centrifugal sedimentation and examined microscopi- ethiological agent of equine protozoal myeloenceph- cally using the technique described by Duszynski & alitis (Dubey & Lindsay, 1998; Monteiro et al., 2013). Wilber (1997). The opossums positive for sporocysts Besides Sarcocystis spp., other coccidia infect of Klossiella spp. in urine were necropsied. Kidneys Didelphis spp., including Eimeria spp. (Teixeira were examined grossly and representative samples of et al., 2007) and Klossiella tejerai Scorza, Torrealba kidney tissue were collected into 10% neutral buffered & Dagert, 1957 (see Scorza et al., 1957). Klossiella formalin. Once fixed, these tissues were embedded in spp. have been reported from various marsupials, paraffin, sectioned at 4 lm, and stained routinely with primarily from Australian peramelids, petaurids and hematoxylin and eosin. Morphological observations, macropodids (Barker et al., 1975, 1985; Bennett et al., line drawing and photomicrographs were made using 2007). However, in the New World, only K. tejerai an Olympus BX binocular microscope coupled to a was described from Didelphis marsupialis (Linnaeus) digital camera Eurocam 5.0. All measurements are in in Venezuela (Scorza et al., 1957), and subsequently micrometres and are presented as the range followed reported from this host species in Panama (Edgcomb by the mean. 123 Syst Parasitol (2014) 89:83–89 85 Fig. 2 Photomicrographs of life-cycle stages of Klossiella tejerai in renal tissue from the Brazilian common opossum Didelphis aurita. A–B, Macrogametes contained within parasitophorous vacuoles; C, Macrogamete and microgamete in syzygy within parasitophorous vacuole; D–E, Early sporonts within parasitophorous vacuoles; F–G, Late budding sporonts within parasitophorous vacuoles; H, Oo¨cyst with free mature sporoblasts/sporocysts; I, Macrogamete (right) and early sporont (middle) within parasitophorous vacuoles and oo¨cyst with free mature sporoblasts/sporocysts (left). Scale-bars:10lm Results Locality: Brazil, State of Rio de Janeiro, Municipality of Serope´dica (22°440S, 43°420W). Twenty Brazilian common opossums were examined; Material studied: One-half of the sporocysts from one of them (5%) shed Klossiella-like sporocysts in urine samples are kept in 10% aqueous buffered the urine. The current description follows the guide- formalin (v/v) and the other half in 70% ethanol for lines of Duszynski & Wilber (1997) and Berto et al. future molecular studies, according Duszynski & (2014a) for the urinary sporocysts and the examples of Gardner (1991). Both samples and the renal tissue Scorza et al. (1957), Barker et al. (1975; 1985), slides were deposited in the Parasitology Collection of Gardiner et al. (1998) and Bennett et al. (2007) for the the Laborato´rio de Coccı´dios e Coccidioses, at nomenclature of tissue stages of Klossiella. UFRRJ, located at the Municipality of Seropedica in the State of Rio Janeiro, Brazil. Photovouchers and Klossiella tejerai Scorza, Torrealba & Dagert, 1957 line drawings are deposited and available (http://r1. ufrrj.br/lcc) as well. Photographs of the host specimen Host: Didelphis aurita Wied-Neuwied (Mammalia: are deposited in the same collection. The repository Didelphimorphia: Didelphidae). number is 53/2014. 123 86 Syst Parasitol (2014) 89:83–89 Table 1 Comparative morphology of Klossiella tejerai recovered from New World opossums Host Didelphis aurita (Wied- Didelphis marsupialis Marmosa demerarae D. marsupialis (L.) Neuwied) (L.) (Thomas) Reference Present study Scorza et al. (1957) Boulard (1975) Edgcomb et al. (1976) Macrogamete Shape Subspherical to ovoidal – Subspherical to ovoidal – Size 7–11 9 5–9 (8.6 9 7.2) (8 9 6) (12) 4–14 (9) Parasitophorous vacuole 14–29 9 14–22 –– – size (22.6 9 18.3) Microgamete Shape Subspheroidal to ovoidal – Ovoidal – Size 5–6 9 3–5 (5.3 9 3.8) (6 9 2) (9 9 6) – Sporont Shape Subspheroidal to irregular – – – Size 15–31 9 14–21 up to 27 – 25–39 (28) (21.3 9 16.4) Number of nuclei 8–13 (10) – – – Sporoblast/Sporocyst Shape Ellipsoidal – – – Size 10–13 9 6–9 (11.4 9 6.8) (12 9 9) (13.7 9 9) 14–17 (16) Number per oo¨cyst 12–30 (18) (18) 16–22 – Oo¨cyst Shape Irregular – – – Size 57–103 9 36–57 – (80 9 40) – (71.6 9 47.2) Urinary sporocysts/ sporozoites Shape Ellipsoidal – – – Size 19–22 9 12–14 –– – (20.4 9 12.7) Length/width ratio 1.5–1.8 (1.6) – – – Sporocyst residuum Granular and diffuse – Present – Number of sporozoites 12–14 (13) (12) 14–22 – Refractile body 2, refringent, in both ends – – – Nucleus Refringent and central – – – Site of infection: Epithelium of the renal tubules. Endogenous stages Endogenous stages in parasitophorous vacuoles within Description (Figs. 1, 2) renal epithelial cells located near the corticomedullary junction. Macrogametes subspheroidal to ovoidal, Exogenous stages 7–11 9 5–9 (8.6 9 7.2), with basophilic nucleus and Sporocysts ellipsoidal, 19–22 9 12–14 (20.4 9 12.7); contained within a subspheroidal to irregular parasitoph- length/width (L/W) ratio 1.5–1.8 (1.6) (Fig. 1). Spo- orous vacuole, 14–29 9 14–22 (22.6 9 18.3) (Fig. 2A– rocyst residuum present, composed of scattered B, I). Macrogamete in syzygy with microgametes in spherules. Sporozoites 12–14 (13), with anterior and some cases (Fig. 2C). Microgametes subspheroidal to posterior refractile bodies and central nucleus. ovoidal, 5–6 9 3–5 (5.3 9 3.8), with basophilic 123 Syst Parasitol (2014) 89:83–89 87 Fig. 3 Geographic ranges of some New World opossums, according IUCN (2014).
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