Syst Parasitol (2011) 78:73–80 DOI 10.1007/s11230-010-9278-3
Isospora bocamontensis n. sp. (Apicomplexa: Eimeriidae) from the yellow cardinal Gubernatrix cristata (Vieillot) (Passeriformes: Emberizidae) in South America Larissa Q. Pereira • Bruno P. Berto • Walter Flausino • Maristela Lovato • Carlos W. G. Lopes
Received: 25 July 2010 / Accepted: 2 October 2010 Ó Springer Science+Business Media B.V. 2010
Abstract A new coccidian species (Protozoa: Apicomplexa: Eimeriidae) is reported from the endangered yellow cardinal Gubernatrix cristata (Vieillot) in southern Brazil. Isospora bocamontensis n. sp. has oo¨cysts which are subspheroidal, measure 32.1 9 28.9 lm and have a smooth, bilayered wall c.1.5 lm thick. The micropyle and the oo¨cyst residuum are absent, but a polar granule is sometimes present. Its sporocysts are ellipsoidal and 17.3 9 12.2 lm in size and contain a half-moon-shaped Stieda body, a prominent, homogeneous substieda body; and a sporocyst L. Q. Pereira Curso de Po´s-Graduac¸a˜o em Medicina Veterina´ria, Universidade Federal de Santa Maria (UFSM), Camobi, Santa Maria, RS 97105-900, Brazil e-mail:
[email protected] B. P. Berto 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] B. P. Berto e-mail:
[email protected] W. Flausino e-mail:
[email protected] M. Lovato Departamento de Medicina Veterina´ria Preventiva, Centro de Cieˆncias Rurais, UFSM, Camobi, Santa Maria, RS 97105-900, Brazil e-mail:
[email protected]
residuum composed of a compact mass of granules. The sporozoites have one refractile body and a nucleus.
Introduction The yellow cardinal Gubernatrix cristata (Vieillot) is a member of the avian family Emberizidae (Sick, 1997; CBRO, 2009). In the past, this species was commonly observed in Argentina and Uruguay, whereas Brazil only has records of wild specimens from the state of Rio Grande do Sul. Currently, it has a population of less than 300 specimens in Argentina and Uruguay (Collar et al., 1992). In Rio Grande do Sul, it has been reported locally in the Serra do Sudeste region and along the border with Uruguay, and its habitat includes open areas with scattered trees, hedges and espinilho parkland (Belton, 1994). The illegal capture of this species and habitat loss probably caused the decrease in its population, and, therefore, the International Union for Conservation of Nature and Natural Resources (IUCN) lists G. cristata as Endangered (Collar et al., 1992; Pessino & Tittarelli, 2006). Coccidiosis caused by species of Isospora Schneider, 1881, has been described in birds of the family Emberizidae worldwide; however, those coccidia described in the Americas can be considered more important, since there is little likelihood of transmission among non-sympatric passerines that inhabit
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distant continents (McQuistion & Wilson, 1988, 1989; McQuistion, 1990; Carvalho-Filho et al., 2005; Berto et al., 2009a). The current study describes a coccidian species infecting the yellow cardinal G. cristata in the district of Boca do Monte, city of Santa Maria, Rio Grande do Sul State, Brazil.
Materials and methods Faecal samples were collected from 14 birds acquired from a breeder located in the district of Boca do Monte, city of Santa Maria (29°380 32.2500 S, 53°550 44.6200 W), Rio Grande do Sul State, Brazil. Birds were held in individual cages and faecal samples were collected in the late afternoon immediately after defecation and placed in plastic vials containing 2.5% potassium dichromate solution (K2Cr2O7) 1:6 (w/v). Samples were carried to the Laborato´rio de Coccı´dios e Coccidioses located at the Universidade Federal Rural do Rio de Janeiro
Syst Parasitol (2011) 78:73–80
(UFRRJ). Samples were placed in a thin layer (c.5 mm) of 2.5% K2Cr2O7 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 & 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. Photomicrographs were taken using a digital camera (Sony CD Mavica MVC-CD250). Size ranges are shown in parentheses followed by the average and shape index (L/W ratio). Abbreviations: T, total number of measurements; M, micropyle; OR, oo¨cyst residuum; PG, polar granule; SB, Stieda body; SSB, substieda body; PSB, parastieda body; SR, sporocyst residuum; SZ, sporozoite; SRB, refractile body; N, nucleus; L, length; W, width.
Fig. 1 Line drawings of Isospora bocamontensis n. sp.: a. sporulated oo¨cyst; b–d. variations of the Stieda and substieda bodies. Scale-bar: a, 10 lm; b–d, 5 lm
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Syst Parasitol (2011) 78:73–80
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Isospora bocamontensis n. sp. Type-host: Gubernatrix cristata (Vieillot) (Aves: Passeriformes: Emberizidae). Type-material: Half of the oo¨cysts are preserved in 10% aqueous buffered formalin (v/v) and the other half in 70% ethanol. Both samples are deposited in the Parasitology Collection, Department of Animal Parasitology, UFRRJ, located in Serope´dica, Rio de Janeiro, Brazil. Phototypes and line drawings are deposited at the same location. The repository number is P-37/2010. Type-locality: 29°380 32.2500 S, 53°550 44.6200 W; Boca do Monte, city of Santa Maria, Rio Grande do Sul, Brazil. Prevalence: 8/14 birds infected (57%). Sporulation time: Seven days (by which time 70% of the oo¨cysts were sporulated under the conditions used in this study). Site: Recovered from faeces; site not investigated. Etymology: The specific epithet is derived from the district of origin of the type-host. Description (Figs. 1, 2) Sporulated oo¨cyst Oo¨cyst shape (T = 20) subspheroidal; number of walls 2; wall thickness 1.5 (1–2); outer wall smooth. c.2/3 of total thickness; L 9 W = 32.1 9 28.9 (27–34 9 26–32), with L/W ratio 1.1 (1.0–1.2); M and OR absent; PG usually absent, but unique, ellipsoidal granule sometimes present (35%; 7 of 20 oo¨cysts had PG). Sporocyst and sporozoites Sporocyst shape (T = 20) ellipsoidal; L 9 W = 17.3 9 12.2 (16–19 9 11–13); L/W ratio 1.4 (1.3–1.5); SB present, half-moon-shaped, 0.7 high 9 2.3 wide; SSB present, prominent, homogeneous, 2.1 high 9 3.7 wide; PSB absent; SR present, composed of compact mass of granules; SZ with single posterior SRB and centrally located N.
Discussion 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. In the family Emberizidae,
Fig. 2 Micrographs of sporulated oo¨cysts (a–c) of Isospora bocamontensis n. sp. Scale-bar: 10 lm
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123 Carvalho-Filho Sub-spheroidal 17.3 9 16.5 1.1 (1.0–1.2) Bi-layered, et al. (2005) (14–20 9 14–20) *1.0 Carvalho-Filho Sub-spheroidal 17.4 9 16.8 1.0 (1.0–1.2) Bi-layered, et al. (2005) (16–19 9 14–19) *1.2
Silva et al. (2006)
G. fortis
Tiaris fuliginosa Ball & Daszak Sub-spheroidal 27.1 9 23.8 (Wied) (1997) (25–30 9 21–27) Carvalho-Filho Sub-spheroidal 21.6 9 20.1 1.0 (1.0–1.1) Bi-layered, et al. (2005) (19–23 9 18–23) *1.3
Geospiza fortis Gould
Sporophila caerulescens (Vieillot)
I. tiaris Ball & Daszak, 1997
I. sporophilae CarvalhoFilho, Meireles, Ribeiro & Lopes, 2005
I. teixeirafilhoi Carvalho- S. caerulescens Filho, Meireles, Ribeiro & Lopes, 2005
O. angolensis
I. daphnensis McQuistion, 1990
I. flausinoi CarvalhoS. caerulescens Filho, Meireles, Ribeiro & Lopes, 2005
Oryzoborus angolensis (Linnaeus)
I. geospizae McQuistion & Wilson, 1989
I. curio Silva, Litera´k & Koudela, 2006
I. braziliensis Silva, Litera´k & Koudela, 2006
Silva et al. (2006)
McQuistion (1990)
McQuistion & Wilson (1989)
McQuistion & Wilson (1988)
25.4 9 21.1 (21–30 9 17–23)
1.2
One-layered, Present, 1 *1.0 to 4
1.1
Bi-layered, *1.0
27.3 9 23.6 1.2 (1.0–1.3) Bi-layered, (22–30 9 20–27) *1.5
Absent
Present
Present
Present
Present
Present
Sub-spheroidal 17.8 9 16.9 1.1 (1.0–1.1) One-layered, Absent (16–19 9 16–18) *1.0
Sub-spheroidal 24.6 9 23.6 1.0 (1.0–1.2) Bi-layered, (22–26 9 22–25) *1.5
Ellipsoidal
Sub-spheroidal 15.5 9 14.5 1.1 (1.0–1.1) One-layered, Present (13–17 9 12–17) *1.0
Ellipsoidal
One-layered, Absent *1.0
C. parvulus
1.0
Present
Absent
Polar granule
Ovoid
Ovoid
13.2 9 10.9 (15–17 9 10–13)
11.7 9 8.1 (9–14 9 6–9)
14.9 9 10.7 (12–18 9 8–12)
15.1 9 10.7 (13–17 9 8–13)
14.7 9 10.8 (12–17 9 9–12)
15.2 9 10.2 (15–16 9 9–11)
10 9 7.5 (10–12 9 6–9)
15 9 10 (14–15 9 9–11)
14 9 9.5 (13–15 9 8–10)
15.4 9 11.5 (14–17 9 11–12)
15 9 9.7 (13–16 9 9–10)
15.2 9 10.0 (14–17 9 8–12)
Measurements (lm)
Ellipsoidal 13.2 9 10.8 (12–14 9 9–12)
Ovoid
Ovoid
Pyriform
Ovoid
Ovoid
Ovoid
Ovoid
Pyriform
Ovoid
One-layered, Present, Pyriform *1.0 10 to 20
one-layered, *1.0
I. temeraria McQuistion & Wilson, 1988
Sub-spheroidal 20.4 9 20.1 (20–23 9 18–23)
1.1
1.0
McQuistion & Wilson (1988)
Sub-spheroidal 25.3 9 24.2 (24–27 9 23–25)
Sub-spheroidal 21.8 9 20.9 (20–24 9 19–23)
C. parvulus
McQuistion & Wilson (1988)
Sub-spheroidal 22.3 9 21.4 1.1 (1.0–1.1) Bi-layered, (19–26 9 18–24) *1.8
I. exigua McQuistion & Wilson, 1988
Camarhynchus parvulus (Gould)
I. rotunda McQuistion & Wilson, 1988
Upton et al. (1985)
Wall (lm)
Shape
Shape index
Shape
Measurements (lm)
Sporocysts
Oo¨cysts
McQuistion & Wilson (1988)
Paroaria coronata (Miller)
I. paroariae Upton, Current & Clubb, 1985
References
I. fragmenta McQuistion C. parvulus & Wilson, 1988
Host
Coccidia
Table 1 Comparative morphology of Isospora bocamontensis n. sp. and Isospora spp. recorded from emberizid birds of the Americas
Flattened
Present
Knob-like
Rounded
Knob-like
Prominent
Nipple-like
Rounded
Knob-like
Small
Knob-like
Knob-like
Small
Stieda body
Residuum
Compact
Compact
Compact
Absent
Absent
Absent
Absent
Absent
Diffuse
Diffuse
Compact
Compact
Compact
Prominent Diffuse
Small
Small
Prominent Compact
Small
Prominent Compact
Prominent Compact
Prominent Compact
Substieda body
76 Syst Parasitol (2011) 78:73–80
Berto et al. Sub-spheroidal 25.7 9 24.3 1.1 (1.0–1.1) Bi-layered, (2009a) (24–27 9 23–25) *1.3 Berto et al. Sub-spheroidal 24.2 9 22.0 1.1 (1.0–1.1) Bi-layered, (2009a) or ovoid (23–26 9 21–23) *1.2 Balthazar et al. (2009)
S. frontalis
S. frontalis
Zonotrichia capensis (Mu¨ller)
Gubernatrix cristata (Vieillot)
I. teresopoliensis Berto, Balthazar, Flausino & Lopes, 2009
I. chanchaoi Berto, Balthazar, Flausino & Lopes, 2009
I. ticoticoi Balthazar,Berto, Flausino & Lopes, 2009
I. bocamontensis n. sp.
Wall (lm)
Sporophila frontalis (Verreaux)
Shape index
I. frontalis Berto, Balthazar, Flausino & Lopes, 2009
Measurements (lm)
O. angolensis Silva et al. (2006)
Sub-spheroidal 32.1 9 28.9 1.0 (1.0–1.2) Bi-layered, to ellipsoidal (27–34 9 26–32) *1.5
Sub-spheroidal 23.3 9 22.4 1.1 (1.0–1.1) Bi-layered, (20–25 9 20–24) *1.2
Berto et al. Sub-spheroidal 27.9 9 26.9 1.0 (1.0–1.1) Bi-layered, (2009a) (27–29 9 25–28) *1.4
Present work
Polar granule
Usually absent
Usually absent
Present, 1 or 2
Absent
Present
Sub-spheroidal 24.3 9 19.8 1.2 (1.1–1.4) One-layered, Present to ellipsoidal (22–26 9 18–22) *1.5
Shape
I. paranaensis Silva, Litera´k & Koudela, 2006
References Oo¨cysts
Host
Coccidia
Table 1 continued
15.7 9 10.1 (14–18 9 8–12)
Measurements (lm)
18.8 9 11.2 (18–20 9 10–12)
Ellipsoidal 17.3 9 12.2 (16–19 9 11–13)
Ellipsoidal 17.0 9 10.8 (15–18 9 10–11)
Ellipsoidal 16.1 9 10.3 (15–17 9 10–11)
Ovoid
Ellipsoidal 19.6 9 11.1 (19–21 9 10–12)
Ovoid
Shape
Sporocysts
Compact
Diffuse
Diffuse
Compact
Residuum
Compact
Compartimented Diffuse
Small
Large
Delicate
Present
Substieda body
Half-moon- Prominent shaped
Nipple like
Nipple-like
Nipple-like
Knob-like
Present
Stieda body
Syst Parasitol (2011) 78:73–80 77
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123 Lainson (1994)
Thraupis palmarum (Wied)
Chlorospingus ophthalmicus (Du Bus de Gisignies)
I. thraupis Lainson, 1994
I. andesensis Templar, McQuistion & Capparella, 2004
R. b. dorsalis
R. b. dorsalis
I. marambaiensis Berto, Flausino, Luz, Ferreira & Lopes, 2008
I. sepetibensis Berto, Flausino, Luz, Ferreira & Lopes, 2008
29.4 9 27.9 1.0 Bi-layered (27–31 9 26–29) (1.0–1.1)
24.2 9 23.4 1.0 Bi-layered (22–26 9 21–26) (1.0–1.1)
1.2 Bi-layered 22.1 9 18.9 (20–25 9 16–23) (1.1–1.3)
22.6 9 18.7 1.2 Bi-layered (20–24 9 17–20) (1.1–1.3)
19.9 9 19.0 1.0 One(19–21 9 19–20) (1.0–1.1) layered
Berto et al. Sub-spherical (2009b)
R. b. dorsalis
Thraupis sayaca (Linnaeus)
T. sayaca
T. sayaca
Gubernatrix cristata (Vieillot)
I. navarroi Berto, Flausino, Luz, Ferreira & Lopes, 2009
I. sanhaci Berto, Balthazar, Flausino & Lopes, 2009
I. sayacae Berto, Balthazar, Flausino & Lopes, 2009
I. silvasouzai Berto, Balthazar, Flausino & Lopes, 2009
I. bocamontensis n. sp.
Present work
1.1 Bi-layered (1.0–1.1)
25.5 9 22.6 1.1 Bi-layered (22–28 9 19–25) (1.0–1.2)
28.9 9 27.4 1.1 Bi-layered (28–30 9 24–29) (1.0–1.1)
22.1 9 21.0 (19–24 917–23)
21.4 9 20.6 1.1 Bi-layered (19–24 9 18–23) (1.0–1.1)
24.2 9 22.9 1.1 Bi-layered (22–26 9 21–24) (1.0–1.1)
Present
Absent
Absent
Absent
Absent
Bubbleshaped
Pyriform
Bottleshaped
Ovoid
Nipplelike
17.6 9 10.5 Delicate (17–18 9 10–11)
Diffuse or compact
Diffuse
Diffuse
Diffuse
Diffuse
Compact
Residuum
Prominent
Small
Prominent
Small
Compact
Compact
Diffuse
Diffuse
Diffuse
With Diffuse compartment
Prominent
Small
Prominent
Collar-shaped
23.4 9 11.8 Prominent Large (23–25 9 11–12)
17.0 9 9.9 (15–19 9 9–11)
Flattened
16.9 9 11.6 Nipplelike (15–18 9 10–13) Ellipsoidal 16.1 9 10.2 (14–19 9 9–12)
Ovoid
Small
Substieda body
Triangular Absent
Delicate
17.7 9 11.5 Flattened (17–19 9 11–13)
13.6 9 9.0 (9–17 9 8–11)
14.1 9 8.5 (13–15 9 8–9)
14.2 9 9.2 (14–16 9 9–10)
Stieda body
Ellipsoidal 22.69 13.0 Flattened (21–24 9 12–14)
Ovoid
Ovoid
Ovoid
Pyriform
Measurements (lm)
Present, Ellipsoidal 16.9 9 11.0 Knob-like 1 or 2 (16–18 9 10–12)
Absent
Absent
Present
Present
Absent
Polar granule
Sub-spheroidal 32.1 9 28.9 1.0 Bi-layered, Usually Ellipsoidal 17.3 9 12.2 Halfto ellipsoidal (27–34 9 26–32) (1.0–1.2) *1.5 lm absent (16–19 9 11–13) moonshaped
Berto et al. Sub-spherical (2009c)
Berto et al. Sub-spherical (2009c)
Berto et al. Sub-spherical (2009b)
Berto et al. Sub-spherical (2009b)
I. cadimi Berto, Flausino, R. b. dorsalis Luz, Ferreira & Lopes, 2009
Berto et al. Sub-spherical 25.5 9 23.8 1.1 Bi-layered (2008) to ellipsoidal (24–29 9 22–26) (1.0–1.2)
Berto et al. Sub-spherical (2008)
Berto et al. Sub-spherical (2008)
Ramphocelus bresilius dorsalis Sclater
I. tiesangui Berto, Flausino, Luz, Ferreira & Lopes, 2008
Ovoid
Metzelaars et al. (2005)
Sub-spherical
Sub-spherical
Wall
Shape
Shape index
Shape
Measurements (lm)
Sporocysts
Oo¨cysts
I. iridosornisi Metzelaars, Iridosornis analis Spaargaren, (Tschudi) McQuistion & Capparella, 2005
Templar et al. (2004)
References
Host
Coccidia
Table 2 Comparative morphology of Isospora bocamontensis n. sp. and Isospora spp. recorded from thraupid birds of the Americas
78 Syst Parasitol (2011) 78:73–80
Syst Parasitol (2011) 78:73–80
numerous coccidia have been described; however, those described in South, North and Central Americas assume a greater importance in terms of comparison due to the higher probability of transmission between sympatric passerines. Table 1 shows all of the morphological and morphometric characteristics of the oo¨cysts of Isospora spp. reported from emberezid birds of the Americas. Isospora bocamontensis n. sp. presents oo¨cysts larger than those described by Upton et al. (1985), McQuistion & Wilson (1988), McQuistion & Wilson (1989), Carvalho-Filho et al. (2005), Silva et al. (2006), Berto et al. (2009a) and Balthazar et al. (2009). Only three species have similar dimensions to I. bocamontensis: I. daphnensis McQuistion, 1990; I. tiaris Ball & Daszak, 1997; and I. frontalis Berto, Balthazar & Flausino, Lopes, 2009. In all these the SSB is smaller than in I. bocamontensis. Furthermore, I. daphnensis and I. tiaris have ovoid sporocysts easily distinguishable from the ellipsoidal sporocysts of I. bocamontensis. I. frontalis can be distinguished by its elongate sporocyst and knob-like Stieda body. Most authors place the host species, Gubernatrix cristata, in the family Emberizidae; however, Burns & Racicot (2009), using mitochondrial DNA data to reconstruct the phylogeny of thraupids, reveal that it may belong to the family Thraupidae. Consequently, I. bocamontensis was also compared with Isospora spp. described from thraupids. Table 2 shows the morphological and morphometric characteristics of the oo¨cysts of Isospora spp. reported from thraupid birds of the Americas. I. bocamontensis presents oo¨cysts larger than those described by Lainson (1994), Templar et al. (2004), Metzelaars et al. (2005) and Berto et al. (2008, 2009b, c). Only two species share similar dimensions with I. bocamontensis: I. sayacae Berto, Balthazar, Flausino & Lopes, 2009, which can be distinguished from the new species by its bottle-shaped sporocyst; and I. marambaiensis Berto, Flausino, Luz, Ferreira & Lopes, 2008, which has a larger sporocyst, flattened Stieda body and small substieda body. Based on the morphometrical features outlined above, the coccidian species obtained from the yellow cardinal Gubernatrix cristata is considered as new to science. Acknowledgement We thank Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico (CNPq) for a scholarship to L.Q. Pereira.
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References Ball, S., & Daszak, P. (1997). Isospora tiaris n. sp. (Apicomplexa: Eimeriidae) from the sooty grassquit (Tiaris fuliginosa), a passeriform bird of South America. Journal of Parasitology, 83, 465–466. Balthazar, L., Berto, B., Flausino, W., & Lopes, C. (2009). Isospora ticoticoi n. sp. (Apicomplexa: Eimeriidae) from the rufous-collared sparrow Zonotrichia capensis in South America. Acta Protozoologica, 48, 345–349. Belton, W. (1994). Aves do Rio Grande do Sul: distribuic¸a˜o e biologia. Sa˜o Leopoldo: Unisinos, 584 pp. Berto, B., Balthazar, L., Flausino, W., & Lopes, C. (2009a). Three new species of Isospora Schneider, 1881 (Apicomplexa: Eimeriidae) from the buffy-fronted seedeater Sporophila frontalis Verreaux, 1869 (Passeriformes: Emberizidae) from South America. Systematic Parasitology, 73, 65–69. Berto, B. P., Balthazar, L. M. C., Flausino, W., & Lopes, C. W. G. (2009b). New isosporoid coccidian parasites of sayaca tanager, Thraupis sayaca, from South America. Acta Parasitologica, 54, 90–94. Berto, B. P., Flausino, W., Luz, H. R., Ferreira, I., & Lopes, C. W. G. (2008). Three new coccidian parasites of Brazilian tanager (Ramphocelus bresilius dorsalis) from South America. Acta Protozoologica, 47, 77–81. Berto, B. P., Flausino, W., Luz, H. R., Ferreira, I., & Lopes, C. W. G. (2009c). Two new Isospora species from Brazilian tanager (Ramphocelus bresilius dorsalis) of South America. Parasitology Research, 105, 635–639. Burns, K., & Racicot, R. (2009). Molecular phylogenetics of a clade of lowland tanagers: implications for avian participation in the Great American Interchange. The Auk, 126, 635–648. Carvalho-Filho, P., Meireles, G., Ribeiro, C., & Lopes, C. (2005). Three new species of Isospora Schneider, 1881 (Apicomplexa: Eimeriidae) from the double-collared seed eater, Sporophila caerulescens (Passeriformes: Emberizidae), from Eastern Brazil. Memo´rias do Instituto Oswaldo Cruz, 100, 151–154. CBRO (2009). Lista das aves do Brasil. Rio de Janeiro: Comiteˆ Brasileiro de Registros Ornitolo´gicos, 32 pp. Collar, N., Gonzaga, L., Krabbe, N., Madron˜o-Nieto, A., Naranjo, L., Parker III, T., & Wege, D. (1992). Threatened birds of Americas: the ICBP/IUCN red data book. Cambridge: International Council for Bird Preservation, 1150 pp. Duszynski, D., & Wilber, P. (1997). A guideline for the preparation of species descriptions in the Eimeriidae. Journal of Parasitology, 83, 333–336. Lainson, R. (1994). Observations on some avian coccidia (Apicomplexa: Eimeriidae) in Amazonian Brazil. Memo´rias do Instituto Oswaldo Cruz, 89, 303–311. McQuistion, T. (1990). Isospora daphnensis n. sp. (Apicomplexa: Eimeriidae) from the medium ground finch (Geospiza fortis) from the Galapagos Island. Journal of Parasitology, 76, 30–32. McQuistion, T., & Wilson, M. (1988). Four new species of Isospora from the small tree finch (Camarhynchus parvulus) from the Galapagos Island. Journal of Eucaryotic Microbiology, 35, 98–99.
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