New Isospora and Host Species in Brazilian Passerines

ABSTRACT

Normal passerines (n=216) were evaluated for oocysts of Isospora in feces at the Triage Center for Wild Animals (CETAS, IBAMA, Belo Horizonte; August 21 to September 21, 2012). The positive samples with oocysts represented 13.0% of Cardinalidae (n=23), 11.2% of Emberizidae (n=107), 50% of Icteridae (n=10) and 60.3% of Thraupidae (n=68). The probability of fecal oocysts attributable to the host in Thraupidae is higher than in Cardinalidae, Emberizidae, Fringillidae and Turdidae, but similar to Icteridae. No oocysts were found in Fringillidae and Turdidae. Within Thraupidae, Isospora was for the first time described in Paroaria dominicana and Schistochlamys ruficapillus and within Icteridae, in Gnorimopsar chopi. Saltator similis presented a higher risk, 66.9% greater than Lanio pileatus and Sporophila caerulescens and with a 27.9% greater probability than Sporophila nigricolis. The new coccidian species described were Isospora dominicana [ellipsoid oocysts, 25 (30-20) x 25 (28-20) µm] in Paroaria dominicana; Isospora beagai [ovoid oocysts, 28 (32-17) x 25 (29-16) µm] and Isospora ferri [ellipsoid oocysts, 20 (22-16) x 18 (22-15) µm] in Saltator similis; Isospora ruficapillus [spheric to subspherical oocysts, 25 (26-23) x 24 (25-21) µm] in Schistochlamys ruficapillus; and Isospora chopi [spherical to sub-spherical oocysts, 24.5 x 22 (30-20 x 25-20) µm] and Isospora gnorimopsar [sub-spherical to ovoid oocysts, 27 x 23 (32-22 x 28-20) µm] in Gnorimopsar chopi. The morphometry and features were compared with previously described Isospora in passerines. New coccidian species and new passerine hosts are described for Isospora and recommends for constant monitoring during rehabilitation, especially for the hosts of Thraupidae and Icteridae.

Keywords:
Apicomplexa; Gnorimopsar chopi; Isospora chopi; Isospora gnorimopsar; Paroaria dominicana; Isospora dominicana; Saltator similis; Isospora beagai; Isospora ferri; Schistochlamys ruficapillus; Isospora ruficapillus

Coccidiosis in the order Passeriformes is caused mostly by the genus Isospora (Page & Haddad, 1995; Duszynski et al., 2018; Freitas et al., 2002; Marietto-Gonçalves et al., 2009; Brown et al., 2010; Costa et al., 2010; Berto et al., 2011a) and may result in important clinical impacts for passerines during captivity (Page and Haddad, 1995; Friend and Frason, 1999; Brown et al., 2010; Berto et al., 2011a). In fact, infection by Isospora represents the most relevant parasitic disease for captive birds (Vilela et al., 2009; Costa et al., 2010; Keeler et al., 2011; Pereira et al., 2011) and demands diagnostic surveillance and strategic or curative medication to reduce losses (Freitas et al., 2002; Yabsley, 2008; Marietto-Gonçalves et al., 2009). In contrast, subclinical infection (coccidiosis) is the most common form of infection in the wild, representing a minor health impact in free-living birds (Upton et al., 1995). However, most species of coccidians, especially of wild birds, are yet to be described (Moore & Clayton, 1997; Lederberg, 1998; Freitas et al., 2002; Wobeser, 2008). In captive birds, a fatal disease outbreak by Isospora icterus was reported in Brazil in a group of a native icterid passerine Icterus jamacaii (Campo oriole or Troupial) (Marques et al., 2011).

Twenty-one South-American passerine species are described as hosts for the genus Isospora, however, only 19 out of the 1073 species of Brazilian passerines have been studied for the occurrence of Isospora or other coccidians (Sick, 1997; Berto et al., 2011a; CBRO, 2014).

The Thraupidae and Icteridae member species are the most frequently sampled among those admitted at the wild animal triage centers in Brazil (Centros de Triagem de Animais Silvestres, CETAS) due to illegal trade (Ferreira & Glock, 2004; Borges et al., 2006; Pagano et al., 2009; Santos et al., 2011; Vilela, 2012; CBRO, 2014) and also because most species are declining in population (IUCN, 2018). According to Vilela (2012), and considering the new classification of species (CBRO, 2014), 61% of all Brazilian passerines at the triage centers belong to Thraupidae. This study describes 5 new host species of Isospora, from Thraupidae: (Paroaria dominicana, Schistoclamys ruficapillus and Sporophila nigricolis), of Cardinalidae (Cyanoloxia brisonii) and of Icteridae (Gnorimopsar chopi), and 2 new species of Isospora in the previously known host Saltator similis.

We describe the occurrence of oocystis of Isospora in passerines of families Thraupidae, Cardinalidae, Emberizidae, Fringillidae and Turdidae, and evaluate new and previously described host species, with the characterization of oocysts by morphometry and structural features.

MATERIALS AND METHODS

Birds and sampling

Fecal samples (n = 216) of clinically healthy passerines of six taxonomic families were evaluated: Cardinalidae, Emberizidae, Fringillidae, Icteridae, Thraupidae, and Turdidae. The occurrence of coccidia was evaluated for all passerines at rehabilitation in the Wild Animal Triage Center of Belo Horizonte (CETAS/BH), Brazil, from August 21^st to September 21^st, 2012 (Table I).

Table I
Passeriormes evaluated and individuals with oocysts in feces.

Family	Scientific name	Common name	Positive	Negative	Total	% Positive
Cardinalidae			3	20
	Cyanoloxia brisonii		3	20	23	13.0
Emberizidae			12	95	107	11.2
	Sicalis flaveola	Canário da terra verdadeiro	7	33	40	17.5
	Sporophila angolensis	Curió	0	3	3	0.0
	Sporophila caerulescens	Coleirinho	4	9	13	30.7
	Sporophila frontalis	Pixoxó	0	1	1	0,0
	Sporophila lineola	Bigodinho	0	4	4	0.0
	Sporophila maximiliani	Bicudo	0	3	3	0.0
	Sporophila nigricolis	Baiano	1	34	35	2.8
	Sporophila plumbea	Patativa	0	1	1	0.0
	Zonotrichia capensis	Tico tico	0	7	7	0.0
Fringillidae
	Sporagra magellanica	Pintassilgo	0	4	4	0.0
Icteridae			5	5	10	50.0
	Gnorimopsar chopi	Graúna	5	4	9	55.5
	Icterus jamacaii	Corrupião	0	1	1	0.0
Thraupidae			41	27	68	60.3
	Lanio pileatus	Tico tico rei cinza	0	3	3	0.0
	Paroaria dominicana	Cardeal do nordeste	4	3	7	57.1
	Saltator similis	Trinca ferro verdadeiro	36	18	54	33.3
	Saltatriculla atricollis	Bico de pimenta	0	2	2	0.0
	Schistochlamys ruficapillus	Bico de veludo	1	1	2	50.0
Turdidae			0	4	4	0
	Turdus amaurochalinus	Sabiá poca	0	1	1	0.0
	Turdus rufiventris	Sabiá laranjeira	0	3	3	0.0
Total			61	155	216	28.24

The study was registered at the SISBIO (Sistema de Autorização e Informação em Biodiversidade (SISBIO) do Instituto Chico Mendes de Conservação da Biodiversidade) at under number 35825-1 and at the ethics committee on animal research (CETEA-UFMG) under number 126/2013.

All fecal samples were collected non-invasively from birds that were kept in individual cages throughout the study. Upon arrival, white paper sheets were left overnight on the bottom of the cages to collect feces the following morning. Samples were immediately examined at microscopy and subjected to flotation in saturated NaCl for microscopy on a slide with coverslip (100, 400 and 1,000x). Oocyst positive samples were partially transferred to an aerated flask with 2.5% potassium dichromate solution (22 C) at 1:5 for sporulation (sporogony) for 1 week. Sporulated oocysts of each bird were subjected to morphologic and morphometric evaluation in a Zeiss Axioscop 40 microscope (Carl Zeiss Microscopy GmbH, Göttingen, Germany), equipped with digital imaging, according to the Duszynski & Wilber (1997) protocol. Images were captured using a Canon G10 digital camera (Canon S Tower 2-16-6, Konan MINATO-KU, Tokyo, Japan), a 52mm adaptor tube and Axiovision 4.8 software with a Sony Vaio VPCSB35FB (Sony Brasil, São Paulo, SP, Brazil). Only viable oocysts, showing the complete development of sporocysts and sporozoites were evaluated. The numerical data were evaluated for sampling normality and homogeneity (ANOVA). The morphological features and morphometrical values were evaluated in an entirely random design (ERD) (Mann-Whitney, ANOVA) and the specific correlations were verified for the data of each individual. For Saltator similis, data were further evaluated for distribution normality and homogeneity of sampling error (Mann-Whitney, ANOVA) and specific correlation to determine the 2 coccidian species (Sampaio, 2007).

RESULTS

Fecal samples detected positive for oocysts were from Cyanoloxia brisonii (Cardinalidae), Sicalis flaveola, Sporophila caerulescens and Sporophila nigricolis (Emberizidae), Gnorimopsar chopi (Icteridae), and Schistoclamys ruficapillus, Paroaria dominicana, Saltator similis, and Sporophila nigricolis (Thraupidae). Samples from Fringillidae and Turdidae were negative (Table I). All sporulated oocysts obtained were typical of the Isospora and were further characterized.

DESCRIPTIONS

Isospora dominicana n. sp.

Description of the sporulated oocyst: spherical to subspherical oocysts, 25 x 25 µm (20-28 x 20-30 µm) (n=50); morphometric index (MI, length /width) 1.0 (1.0 - 1.2); smooth bilayered wall (1 µm in thickness); absences of micropyle, polar granule and sporocyst residuum (Table II).

Table II
Comparative morphometry (µm) of oocysts and sporocysts, and morphological features of species of genus Isospora described in family Thraupidae (Aves: Passeriformes: Thraupidae).

Species	Host	Reference	Oocyst				Sporocyst
			Shape	Polar granule	Diameter (µm)		Morpho metric index	Shape	Diameter (µm)		Morpho metric index	Stieda body	Resíduum
					Major	Minor			Major	Minor		Shape Length x width (µm)
Isospora vanriperorum	Cardinalis cardinalis; Saltator similis	Levine et al. (1980); Lopes et al. (2007)	Subspherical	Present	23,1 (26-22)	22,4 (25-20)	1,04	Ovoid	16,3 (17-15)	10		Button shaped	Compact
I. paroariae	Paroaria coronate	Upton et al. (1985)		Absent	22,3 (26-19)	21,4 (24-18)	1,1		15,2 (17-14)	10 (12-8)	1,53
I. pityli	Saltator grossus saturates	McQuistion & Capparella (1992)	Subspherical	Absent	20,1 (21-20)	18,8 (20-17)	1,07	Ovoid	14,7 (17-12)	9,4 (11-8)	1,57	Mammilliform	Compact
I. formarum	S. g. grossus; S.g. saturatus	McQuistion & Capparella (1992)	Subspherical	Absent	24,6 (27-21)	23,5 (25-20)	1,1	Ovoid	15,7 (17-14)	11,3 (13-10)	1,4	Small, Mammilliform	Compact
I. saltatori	S. similis	Berto et al. (2008b)	Subspherical	Absent	18,3 (20-17)	17,9 (20-16)	1	Ovoid	13,4 (15-12)	8,9 (10-8)	1,5	Small, Mammilliform	Compact
I. trincaferri	S. similis	Berto et al. (2008b)	Subspherical	Present	26,2 (29-24)	23,6 (25-22)	1,1	Ovoid	17,5 (18-17)	11,5 (13-10)	1,5	Bubble shaped	Diffuse
I. thraupis	Thraupis palmarum melanoptera	Lainson (1994); Berto (2010)	Subspherical	Absent	19,9 (21-19)	19 (20-19)	1	Piriform	14,2 (16-14)	9,2 (10-9)	1,5	Delicate	Compact
I. andesensis	Chlorospingus ophtalmicus	Templar et al. (2004); Berto 2010)	Subspherical or ovoid	Present	22,6 (24-20)	18,7 (20-17)	1,2	Ovoid	14,1 (15-13)	8,5 (9-8)	1,7	Triangular, prominent	Diffuse
I. irisidornisi	Irisidornis analis	Metzelaars et al. (2005); Berto (2010)	Ovoid	Present	22,1 (25-20)	18,9 (23-16)	1,2	Ovoid	13,6 (17-9)	9 (11-8)	1,5	Bubble-shaped	Diffuse
I. tiesangui	Ramphocelus bresilius dorsalis; T. palmarum; Dacnis cayana	Berto et al. (2008a); Berto (2010)	Subspherical	Absent	24,2 (26-22)	23,4 (26-21)	1,03	Ovoid	17,7 (19-17)	11,5 (13-11)	1,54	Flat	Diffuse
I. marambaiensis	R. b. dorsalis	Berto et al. (2008a, 2010)	Subspherical	Absent	29,4 (31-27)	27,9 (29-26)	1	Ellipsoid	22,6 (24-21)	13 (14-12)		Flat	Diffuse
I. sepetibensis	R. b. dorsalis	Berto et al. (2008a, 2010)	Subspherical	Present 1 or 2	25,5 (29-24)	23,8 (26-22)	1,1	Ellipsoid	16,9 (18-16)	11 (12-10)		Button-shaped	Lateral
I. cadimi	R. b. dorsalis	Berto et al. (2009a, 2010)	Subspherical	Absent	24,2 (26-22)	22,9 (24-21)	1,1	Ovoid	16,9 (18-15)	11,6 (13-10)	1,5	Mammiliform	Diffuse
I. navarroi	R. b. dorsalis	Berto et al. (2009b, 2010)	Subspherical	Absent	21,4 (24-19)	20,6 (23-18)	1	Ellipsoid	16,1 (19-14)	10,2 (12-9)	1,6	Flat	Diffuse
I. ramphoceli	R. b. dorsalis	Berto et al (2010)	Subspherical	Absent	23,7 (26-22)	22,8 (24-21)	1,04	Ellipsoid or ovoid	16 (18-14)	11,4 (13-10)	1,41	Button-shaped	Diffuse
I. sanhaci	Thraupis sayaca	Berto et al. (2009c, 2010)	Subspherical	Absent	22,1 (24-19)	21 (23-17)	1	Ovoid	17 (19-15)	9,9 (11-9)	1,7	Mammilliform	Diffuse
I. silvasouzai	T. sayaca	Berto et al. (2009c, 2010)	Subspherical	Present	25,5 (28-22)	22,6 (25-19)	1,1	Piriform	17,6 (18-17)	10,5 (11-10)	1,7	Delicate	Compact
I. sayacae	T. sayaca	Berto et al. (2009c, 2010)	Subspherical	Absent	28,9 (30-28)	27,4 (29-24)	1,1	Bottle-shaped	23,4 (25-23)	11,8 (12-11)	2	Prominent	Diffuse
Isospora similisi	S. similis	Coelho et al. (2013)	Spheric to subspherical	Present	27,5 (29-26)	25,9 (28-24)	1,1	Ellipsoid or ovoid	17,4 (19-15)	12,2 (12-11)	1,4	Button-shaped	Diffuse
Isospora dominicana	Paroaria dominicana	Present study	Spheric to subspherical	Absent	25 (30-20)	25 (28-20)	1,04 (1,18-1)	Ellipsoid	17 (18-15)	11 (13-9)	1,5 (1,8-1,3)	Mammilliform 1 x 2	Absent
Isospora beagai	Saltator similis	Present study	Ovoid	Present	28 (32-17)	25 (29-16)	1,15 (1,5-1)	Ovoid	18 (23-12)	11 (15-9)	1,53 (2,2-1,23)	Prominent, Button-shaped 2 x 3	Compact
Isospora ferri	Saltator similis	Present study	Spheric to subspherical	Absent	20 (22-16)	18 (22-15)	1 (1,15-1)	Ellipsoid	14 (20-12)	8 (11-7)	1,6 (2,5-1,3)	Flat 1 x 2	Diffuse
Isospora ruficapillus	Schistochlamys ruficapillus	Present study	Spheric to subspherical	Absent	25 (26-23)	24 (25-21)	1,04 (1,09-1)	Ellipsoid	17 (18-16)	11 (11-10)	1,6 (1,63-1,45)	Flat, mammilliform 1 x 2	Diffuse

Description of the sporocyst: Ellipsoidal sporocysts, 11 x 17 µm (9-13 x 15-18 µm), SI 1.5 (1.3-1.8), flattened Stieda body (1 µm in height by 2 µm in width) and prominent substieda body (2 µm in height by 3 µm in width) (Table II).

Figures 1, 2
Oocysts of Isospora dominicana recovered from Paroaria dominicana. Note the spheric to subspheric oocyst, absence of polar granule and oocyst residuum, flat Stieda body (arrow) and prominent substieda (arrow head).

Taxonomy summary

Host: Paroaria dominicana (Aves: Passeriformes: Thraupidae).

Geographical location and date: Samples obtained at the Wild Animal Triage Center of Belo Horizonte (CETAS/BH), Brazil, from August 21st to September 21st, 2012.

Site of infection: Undetermined.

Sporulation: Exogenous.

Frequency of detection: In 4/7 (57%).

Collection material Id. Dominicana: Refrigerated (4 - 8 ºC) for analysis and subsequently frozen feces; oocysts photomicrographs deposited at the Avian Diseases Laboratory, Veterinary College, UFMG.

Etymology: The name given to this species was based on its host name: Paroaria dominicana.

Remarks

Considering the absence of a polar granule found in the coccidian species, this species was similar to 12 others previously described in publications on Thraupidae Isospora marambaiensis, Isospora sepetibensis and Isospora tiesangui,Berto et al. (2008a) and Berto (2010), Isospora saltatori Berto et al. (2008b), Isospora cadimi and Isospora navarroi Berto et al. (2009a, 2009b), Isospora ramphoceli, Isospora sanhaci and Isospora sayacae Berto et al. (2009c, 2010), Isospora thraupisLainson (1994), Isospora formarum and Isospora pityliMcQuistion and Capparella (1992), and Isospora paroariaeUpton et al. (1985). Regarding the sporocyst residuum, it was absent for only the described species, in contrast to those compared with Isospora of Thraupidae (Table II). Despite such detail being considered sufficient for describing a new species (Duszynski & Wilber, 1997), further data were analyzed using a dichotomic key (Berto et al., 2010). Results indicated a new species characterized by the absence of polar granule, larger than 25µm in length, flat Stieda body, large and easily visible substieda body and no sporocyst residuum (Table II). The absence of sporocyst residuum was not previously described for Isospora of Passeriformes. Considering these exclusive characteristics, the new species was thereby named Isospora dominicana.

Table III
Morphometric comparisons of Isospora species described in passerines of family Icteridae (Aves: Passeriformes, Icteridae).

Species

Host

Reference

Oocyst

Sporocyst

Shape

Polar granule

Diameter (µm)

Morpho-metric Index

Shape

Diameter (µm)

Morphometric index

Stieda body

Residuum

Length (L)

Width (W)

Length (L)

Width (W)

Shape height x width (µm)

Isospora divitis

Dives atroviolaceus

Pellérdy (1967)

Sub-spheric

Absent

(30-22)

(28-20)

1.1

17

13

1.3

Conspicuous

Diffuse

Isospora cacici

Cacicus cela cela

Lainson (1994)

Sub-spheric

Present 1 or 2

26,5 (27,5-22,5)

23,7 (26,2-20)

1,1

Elongated

17,7 (18,75-17,5)

12,5 (13,75-11,25)

1,4

Prominent, cork shaped

Compact

Isospora belicosa

Sturnella belicosa

Upton et al.(1995)

Episoidal or ovoid

Present 1 or 2

29,4 (26,4-23,5)

23,5 (26,4-21)

1,2

Ellipsoidal

17,8 (18,6-16,8)

10,7 (11,2-10,2)

1,67

Large

Diffuse

Isospora icterus

Icterus icterus

Upton & Whitaker (2000)

Sub-spheric

Present

28,9 (32-27,2)

27,2 (30-25)

1,1

Ellipsoidal

17,8 (19,2-16,8)

12,8 (13,6-12)

1,39

Small, mammiliform

Diffuse

Isospora icterus

Icterus jamacaii

Marques et al. 2011

Sub-spheric

Present

30,1 (32,5-27,5)

28,5 (30-26,25)

1,1

Ellipsoidal1.3

17,6 (20-15)

12,9 (15-12,5)

1,4

Small, mammiliform

Diffuse

Isospora graceannae

Icterus graceannae

Upton & Whitaker (2000)

Sub-spheric

Present

23,9 (26,4-20)

22,3 (25-18,6)

1,1

Ellipsoidal

15,5 (16,2-14,2)

10,7 (11,4-10)

1,44

Robust

Diffuse

Isospora gnorimopsar

Gnorimopsar chopi

Present study

Sub-spheric to ovoid

Present 1 or 2

27 (32-22)

23 (28-20)

1,18 (1,33 -1)

Ellipsoidal

16 (19-14)

11 (12 - 9)

1,52 (1,72 - 1,33)

Flat 1 x 2

Absent

Isospora chopi

Gnorimopsar chopi

Present study

Sub-spheric to ovoid

Absent

24,5 (30-21)

22 (25-20)

1,08 (1,19 - 1)

Ellipsoidal

15 (16-13)

9,7 (10-8)

1,57 (1,66-1,3

Prominent 2 x 1

Present

Isospora beagai n. sp.

Description of the sporulated oocyst: Ovoidal oocysts, 25 x 28µm (16 -29 x 17-32µm) (n = 53), with morphometric index (MI, length/width) 1.1 (1..0 - 1.5), smooth bilayer wall approximately 1 µm in thickness. Absence of micropyle and the presence of polar granule (Table II).

Description of the sporocyst: The sporocysts are ovoidal of 11 x 18 µm (9-15 x 12 - 23 µm), SI 1.5 (1.2 - 2.2), prominent club-shaped Stieda body, of 2 µm in height by 3 µm in width and compact sporocysts residuum (Table II).

Figures 3, 4
Oocysts of Isospora beagai recovered from Saltator similis. (3) Note the ovoidal oocyst, the presence of polar granule (arrowhead) and prominent Stieda body (arrow). (4) Note the ovoidal oocyst, the presence of prominent Stieda body (arrowhead) and diffused sporocyst residuum (arrow).

Taxonomy summary

Host: Saltator similis (Aves: Passeriformes: Thraupidae).

Geographical location and date: Samples obtained at the Wild Animal Triage Center of Belo Horizonte (CETAS/BH), Brazil, from August 21^st to September 21^st, 2012.

Site of infection: Undetermined. Samples were taken from feces.

Sporulation: Exogenous.

Frequency of detection: In 36/54 (68%).

Collection material Id. Beagai: Refrigerated (4-8 ºC) for analysis and subsequently frozen feces; oocycts photomicrographs; stored at the Avian Diseases Laboratory, Veterinary College, UFMG.

Etymology: The name given to this species was based on the acronym of the geographical location in which it was found (BH, Belo Horizonte) (Brazil).

Remarks

Comparing the oocysts possessing a polar granule with previously described species (Table II), it was shown that, among the 23 known species, including the 4 described in this manuscript, only 8 Isospora species have been characterized by the presence of a polar granule. The species described here (Table III) (Isospora beagai) had a bubble-shaped polar granule similar to Isospora vanriperorum, Isospora trincaferrri, Isospora iridornisi, Isospora sepetibensis and Isospora similis. Considering the sporocyst residuum, a compact residuum similar to I. vanriperorum and I. sepetibensis was observed. In order to compare the species described here to the previously described I. vanriperorum, data in Table II along with descriptive images previously published, were employed (Lopes et al., 2007; Berto et al., 2011a; 2011b). Dissimilarities were found when compared to I. vanriperorum, such as a bilayered wall and a large and conspicuous substieda body. The sporocyst, although both ovoidal, also showed differences. Such characteristics are considered sufficient in determining this to be a different species (Duszynski & Wilber, 1997).

When considering I. sepetibensis, comparisons using dichotomic keys, descriptive drawings (Berto et al., 2010; 2011a; 2011b), and data in Table II, show that sporocysts were described as ellipsoidal, in contrast to the ovoidal sporocysts found in the new I. beagai species found in this paper. The sporocyst residuum has been reported as compact, in contrast to the slightly larger and diffused sporocyst described here. Comparing the morphometric data of I. beagai with that of I. sepetibensis, a slight difference of oocyst and sporocyst measurements were revealed, being greater for the former.

The dichotomic key (Berto et al., 2010) suggests this species be compared to I. iridornisi, which presents larger oocysts and sporocysts than Isospora beagai (p = 0.0001), a compact but not diffused sporocyst residuum in I. beagai, a larger substieda body, and not collar-shaped as seen in I. beagai. These individual features were considered sufficient in order to describe a new species (Duszynski & Wilber, 1997). In addition, the described host (Irisidornis analis) for Isospora iridornisi occcurs only in Colombia, Ecuador and Peru (northern South America), while Saltator similis occurs in southcentral South America, including Argentina, Bolivia, Brazil, Paraguay and Uruguay.

The morphologic and morphometric data and images were compared with descriptions in literature (Table II). The differences described for I. beagai, in comparison to I. iridornisi, include a diffused and ovoidal sporocyst for I. beagai, in contrast with a compact and ellipsoidal sporocyst for I. iridornisi.

Considering the morphometrical data of oocysts in Saltator similis (Tables II and III), two different set of data were obtained, and oocyst dimensions, the presence of polar granule, and compact sporocyst residuum, were considered sufficient reasons to describe a new species Isospora beagai (Duszynski & Wilber, 1997).

Isospora ferri n.sp.

Figures 5, 6
Oocysts of Isospora ferri recovered from Saltator similis. (5) Note the spheric to subspheric oocyst, absence of polar granule, flat delicate Stieda body (arrowhead), large and conspicuous substieda (arrow), and round oocyst. (6) Note the absence of polar granule, flat and delicate Stieda body (arrowhead), and diffused sporocyst residuum (arrows).

Description of the sporulated oocyst: Spherical to subspherical oocysts, 18 x 20 µm (15-22 x 16-22) (n=59), MI 1.0 (1.0 x 1.2), presenting a smooth double layered wall of approximately 1 µm, and the absence of micropyle, polar granule and diffused sporocyst residuum (Table II).

Description of the sporocyst: Sporocysts are ellipsoidal, 8 x 14 µm (7 - 11 x 12 - 20) SI, 1,6 (1.3 - 2.5), with flat Stieda body 1 µm in height and 2 µm in width, prominent substieda body of approximately 2 µm in height and 3 µm in width (Table II).

Taxonomy summary

Host: Saltator similis (Aves: Passeriformes: Thraupi-dae).

Geographical location and date: samples obtained at the Wild Animal Triage Center of Belo Horizonte (CETAS/BH), Brazil, from August 21^st to September 21^st, 2012.

Site of infection: Undetermined. Samples were taken from feces.

Sporulation: Exogenous.

Frequency of detection: In 36/54 (68%).

Collection material Id. Ferri: Refrigerated (4-8 ºC) for analysis and subsequently frozen feces; oocysts photomicrographs; stored at the Avian Diseases Laboratory, Veterinary College, UFMG.

Etymology: The name I. ferri was given based on the host’s popular Portuguese name: trinca-ferro.

Remarks

In comparison to the coccidia previously found in feces of S. similis (Table II), the oocysts in this study were larger, thus reinforcing the need to introduce a separate species (Duszynski & Wilber, 1997).

Oocysts of Isospora, which do not present polar granule of previously described species in S. similis, were compared to those of this new species, I. ferri (Table II). Out of the 20 known species, in addition to 4 described in this family (Thraupidae), 16 do not present a polar granule oocyst. The dichotomic key (Berto et al., 2010) suggests this species be compared to Isospora tiesangui of the Brazilian tanager Ramphocelus bresilius. However, comparing the oocyst and sporocyst of these coccidians, I. ferri had a smaller dimension (Table II). The oocyst format was ovoidal for I. ferri but ellipsoidal for I. tiesangui; the Stieda body measured 0.5 x 3 µm in I. tiesangui in comparison to 1 x 2 µm in I. ferri; and the substieda body measured 2.5 x 4 µm in I. tiesangui, but 2 x 3 µm for I. ferri. Such differences are considered sufficient in determining this to be a different species of Isospora in Saltator similis (Duszynski & Wilber, 1997).

The differences to Isospora navarroi were visible at the Stieda and substieda bodies (Berto et al., 2011a, 2011b). The new species presented a larger flat Stieda and larger conspicuous substieda body. The sporocyst residuum was diffused and spread within the sporocyst, and not ring-shaped as in I. navarroi.

Considering the morphometrical data of oocysts in Saltator similis (Tables II and III), two different sets of data were obtained, and oocyst dimensions, the absence of polar granule, and diffuse sporocyst residuum, considered sufficient reasons enough to indicate Isospora ferri as a new species.

Isospora ruficapillus

Figures 7, 8
Oocysts of Isospora ruficapillus recovered from Schistochlamys ruficapillus. (7) Note the mammilliform Stieda body (arrowhead) and the sporocyst diffused residuum (arrow). (8) Note the complex formed by the mammilliform Stieda body (arrowhead) and the prominent substieda (arrow).

Description of the sporulated oocyst: Spherical to subspherical oocysts, 24 x 25 µm (21-25 x 23-26) (n = 20), MI, 1.0 (1.0 - 1.1), presenting a double smooth wall, approximately 1 µm in thickness, the absence of micropyle and polar granule (Table II).

Description of the sporocyst: The ellipsoidal sporocysts, 11 x 17 µm (10 -11 x 16 x 18), with mammilliform Stieda body 1 µm in height per 2 µm in width, prominent substieda 2.5 x 3 µm (2.5 µm in height by 3µm in width), and the presence of a diffused sporocyst residuum (Table II).

Taxonomic summary

Host: Schistoclamys ruficapillus (Aves: Passeriformes: Thraupidae).

Geographical location and date: Samples obtained at the Wild Animal Triage Center of Belo Horizonte (CETAS/BH), Brazil, from August 21st to September 21st, 2012.

Site of infection: Undetermined. Samples were taken from feces.

Sporulation: Exogenous.

Frequency of detection: 1/2 (50%).

Collection material Id. Ruficapillus: Refrigerated (4-8 ºC) for analysis and subsequently frozen feces; oocycsts photomicrographs stored at the Avian Diseases Laboratory, Veterinary College, UFMG.

Etymology: The name I. Ruficapillus was given based on the species’ host Schistoclamys ruficapillus.

Remarks

The morphometric and morphologic data obtained after sporulation were compared to data from the literature (Table II) and using a previously described dichotomic key (Berto et al., 2010) which enabled the description of a new species: Isospora ruficapillus.

The closest species to Isospora ruficapillus was Isospora sanhaci, based on the dichotomic key (Berto et al., 2010). I. sanhaci was described as having a roundish delicate substieda body, which differed from I. ruficapillus as observed in the present study, even though it presented similarities in other structures. The sporocyst shape of both species differed, being ellipsoidal for I. ruficapillus and ovoid for I. sanhaci. Considering the sporocyst residuum, the new described species presented a diffused structure.

Taking into account the absence of polar granule, the shape of the Stieda body and sporocyst residuum; the species found in Schistochlamys ruficapillus suggests this species be compared to Isospora navarroi and Isospora marambaiensis previously described in Ramphocelus bresilius dorsalis (Berto et al., 2008a; 2009b; 2010). I. marambaiensis presented larger oocysts and sporocyts, but the Stieda and substieda bodies were smaller and more delicate than in I. ruficapillus (Berto et al. 2011a, 2011b), and such differences were considered sufficient for describing a new coccidian species (Duszynski & Wilber, 1997).

Isospora chopi

Figures 9, 10
Oocysts of Isospora chopi recovered from Gnorimopsar chopi. (9) Note the spheric to subspheric oocyst of Isospora chopi without polar granule, with prominent Stieda body (arrow) and diffused sporocyst residuum (arrowhead). (10) Note the spheric to subspheric Isospora chopi oocyst with sporocyst residuum (arrow), prominent Stieda body (arrowhead) and absence of polar granule.

Description of the sporulated oocyst: Spheric to subspheric oocysts (n = 48) of 22 x 24.5µm (20-25 x 20-30µm), MI of 1.2 (1.0 -1.2), with smooth double layered wall of approximately 1 µm in thickness, without micropyle or polar granule (Table IV).

Table IV
Morphometric comparisons of Isospora found in feces* of Gnorimopsar chopi (Aves, Passeriformes: Icteridae) in triage in the Wild Animals Triage Center (CETAS) of Belo Horizonte, Minas Gerais, Brazil.

Species	Mean	Standard deviation	Median	Maximum	Mínimum	Prob. (P=)
Oocyst length
1	24,23	1,94	24,5	30,00	20,00	0,0001
2	26,95	2,32	27,00	32,00	22,00
Oocyst width
1	22,52	1,57	22,00	25,00	20,00	0,5635
2	22,81	1,84	23,00	28,00	20,00
Oocyst morphometric index
1	1,08	0,06	1,08	1,20	1,00	0,0001
2	1,19	0,11	1,18	1,52	1,00
Sporocyst length
1	15,05	0,95	15,00	16,00	13,00	0,0001
2	16,33	1,03	16,00	19,00	14,00
Sporocyst width
1	9,70	0,57	10,00	10,00	8,00	0,0001
2	10,69	0,64	11,00	12,00	9,00
Sporocyst morphometric índex
1	1,55	0,08	1,58	1,67	1,30	0,2028
2	1,53	0,10	1,52	1,73	1,33

• *Fecal samples were colected from August 21 to September 21, 2012.
• Species 1: proposed name Isospora chopi; species 2: proposed name Isospora gnorimopsar.

Description of sporocyst: Ellipsoidal sporocysts of 10 x 15 µm (8-10 x 13-16 µm) with 2 µm in height and 1 µm in width prominent Stieda body and diffused sporocyst residuums (Table IV)

Host: Gnorimopsar chopi (Aves: Passeriformes: Icteridae).

Geographical location and date: Samples obtained at the Wild Animal Triage Center of Belo Horizonte (CETAS/BH), Brazil, from August 21st to September 21st, 2012.

Site of infection: Unknown. Samples were taken from feces.

Sporulation: Exogenous. Frequency of detection: In 5/ 9 (55%).

Collection material Id. Chopi: Refrigerated (4-8 ºC) for analysis and subsequently frozen feces; oocysts photomicrographs stored at the Avian Diseases Laboratory, Veterinary College, UFMG.

Etymology: The name given to this species was based on its host name: Gnorimopsar chopi.

Remarks

The morphometric and morphologic data (Table IV) obtained after sporulation were compared to data from the literature (Table V) for Isospora of Icteridae and using a previously described dichotomic key (Berto et al., 2010) which enabled the description of a new species, Isospora chopi.

Table V
Morphometric comparisons of Isospora species described in passerines of family Icteridae (Aves: Passeriformes, Icteridae).

Species

Host

Reference

Oocyst

Sporocyst

Shape

Polar granule

Diameter (µm)

Morpho-metric Index

Shape

Diameter (µm)

Morphometric index

Stieda body

Residuum

Length (L)

Width (W)

Length (L)

Width (W)

Shape height x width (µm)

Isospora divitis

Dives atroviolaceus

Pellérdy (1967)

Sub-spheric

Absent

(30-22)

(28-20)

1.1

17

13

1.3

Conspicuous

Diffuse

Isospora cacici

Cacicus cela cela

Lainson (1994)

Sub-spheric

Present 1 or 2

26,5 (27,5-22,5)

23,7 (26,2-20)

1,1

Elongated

17,7 (18,75-17,5)

12,5 (13,75-11,25)

1,4

Prominent, cork shaped

Compact

Isospora belicosa

Sturnella belicosa

Upton et al.(1995)

Episoidal or ovoid

Present 1 or 2

29,4 (26,4-23,5)

23,5 (26,4-21)

1,2

Ellipsoidal

17,8 (18,6-16,8)

10,7 (11,2-10,2)

1,67

Large

Diffuse

Isospora icterus

Icterus icterus

Upton & Whitaker (2000)

Sub-spheric

Present

28,9 (32-27,2)

27,2 (30-25)

1,1

Ellipsoidal

17,8 (19,2-16,8)

12,8 (13,6-12)

1,39

Small, mammiliform

Diffuse

Isospora icterus

Icterus jamacaii

Marques et al. 2011

Sub-spheric

Present

30,1 (32,5-27,5)

28,5 (30-26,25)

1,1

Ellipsoidal1.3

17,6 (20-15)

12,9 (15-12,5)

1,4

Small, mammiliform

Diffuse

Isospora graceannae

Icterus graceannae

Upton & Whitaker (2000)

Sub-spheric

Present

23,9 (26,4-20)

22,3 (25-18,6)

1,1

Ellipsoidal

15,5 (16,2-14,2)

10,7 (11,4-10)

1,44

Robust

Diffuse

Isospora gnorimopsar

Gnorimopsar chopi

Present study

Sub-spheric to ovoid

Present 1 or 2

27 (32-22)

23 (28-20)

1,18 (1,33 -1)

Ellipsoidal

16 (19-14)

11 (12 - 9)

1,52 (1,72 - 1,33)

Flat 1 x 2

Absent

Isospora chopi

Gnorimopsar chopi

Present study

Sub-spheric to ovoid

Absent

24,5 (30-21)

22 (25-20)

1,08 (1,19 - 1)

Ellipsoidal

15 (16-13)

9,7 (10-8)

1,57 (1,66-1,3

Prominent 2 x 1

Present

Analyzing the previously known Isospora of Icteridae, only Isospora divitis (Pellérdy, 1967) (Table V) shares common features to the new species (I. chopi), including the presence of sporocyst residuum, even though the morphometric measurements of the sporocyst differed. I. divitis was described in Dives atroviolaceus as an endemic icterid in Cuba. D. atroviolaceus and G. chopi never share the same environment; G. chopi occurs up to the southern borders of the Amazon forest in Brazil and D. atroviolaceus occurs only in Cuba.

Isospora gnorimopsar

Description of the sporulated oocyst: Subspheric to ovoid oocysts of 23 - 27 µm (20-28 x 22-32µm) (n = 59), with morphometric index (MI) 1.2 (1.0-1.4), with a smooth double layered wall of approximately 1 µm in thickness, absent micropyle and with 1 or 2 polar granules (Table IV).

Description of the sporocyst: Ellipsoidal sporocysts, 11-16 µm (9-12 x 14-19 µm), with SI 1.5 (1.3 x 1.), flat Stieda body (1 µm in thickness and 2 µm in width) and diffused sporocyst residuum (Table IV).

Figures 11, 12
Oocysts of Isospora gnorimopsar recovered from Gnorimopsar chopi. (11) Note the ovoid to subspheric oocyst of Isospora gnorimopsar with two polar granules (arrow). (12) Note the ovoidal to subspheric oocyst of Isospora gnorimopsar with one polar granule (arrowhead) and sporocyst residuum (arrows).

Taxonomic summary

Host: Gnorimopsar chopi (Aves: Passeriformes: Icteridae).

Geographical location and date: Samples obtained at the Wild Animal Triage Center of Belo Horizonte (CETAS/BH), Brazil, from August 21st to September 21st, 2012.

Site of infection: Unknown. Samples were taken from feces.

Sporulation: Exogenous.

Frequency of detection: In 5/9 (55%).

Collection material Id. Gnorimopsar: Refrigerated (4-8 ºC) for analysis and subsequently frozen feces; oocysts photomicrographs stored at the Avian Diseases Laboratory, Veterinary College, UFMG.

Etymology: The name given to this species was based on the genus of the host, Gnorimopsar chopi.

Remarks

The morphometric and morphologic data obtained after sporulation were compared to data from literature (Table II) and using a previously described dichotomic key (Berto et al., 2010) which enabled the description of a new species, Isospora gnorimopsar.

The presence of the polar granule in I. gnorimopsar, were compared to those of I. cacici (Lainson, 1994), I. belicosa (Upton et al., 1995), I. icterus (Upton and Whitaker, 2000) and I. graceannae (Upton and Whitaker, 2000). However, the flattened shape of the Stieda body was distinct in I. gnorimopsar. Although I. icterus was described with a small Stieda body, the oocyst and sporocyst average dimensions were significantly different. In addition, no sporocyst residuum was found in I. gnorimopsar, in contrast to a diffused residuum in I. icterus. The analyses were performed based on descriptions by Berto et al. (2011a). Such differences are considered sufficient in determining this to be a new coccidian species (Duszynski & Wilber, 1997).

DISCUSSION

Out of the 216 fecal samples evaluated, 61 were positive for oocysts, which corresponded to 28% of this total, all being of the genus Isospora. Considering this occurrence, similar results had been previously found in birds by McQuistion (2000), Marietto-Gonçalves et al. (2009), Vilela et al. (2009) and Schoener et al. (2013). Considering passerines (Passeriformes), results are in agreement with previous reports by Pereira et al., (2011) and Coelho et al. (2013), studying Gubernatrix cristata and Saltator similis, respectively, and found only Isospora.

Although the impact of coccidiosis in free-living passerines is unknown, the disease is highly significant in captive birds (Swayne et al., 1991; Cork and Alley, 1999; Twentyman, 2001; Gill and Paperna, 2008; Marques et al., 2011; Vasconcelos et al., 2012). Results indicate that the triage birds evaluated, despite being temporarily in captivity, have undergone challenge, which could eventually have become clinically significant for susceptible birds, with the increasing concentration of oocysts in the housing environment. The adequate cleaning and disinfection of the premises should be intensified using more efficient principles such as ammonium hydroxide (Kahrs, 1995). Considering the risk of coccidiosis for birds in triage, in agreement with monitoring recommendations, the authors suggest routine evaluations of feces to be performed weekly (Friend and Franson, 1999).

In this study, not all oocysts found were characterized. A few samples, although adequate for determining the genus, were not adequate for the description of species due to the lack of development, presentation or preservation of discernible features. New host species presenting Isospora in this study include Cyanoloxia brisonii, Gnorimopsar chopi, Paroaria dominicana, Schistochlamys ruficapillus, Sicalis flaveola, Sporophila caerulescens and Sporophila nigricolis. The coccidians found in the host species Cyanoloxia brisonii, Sicalis flaveola, Sporophila caerulescens and Sporophila nigricolis belong to the genus Isospora, and a detailed morphology of the oocysts was not evaluated.

The morphological comparisons were performed for characterizing Isospora species in the host family taxon. The careful analysis of oocysts included the determination of oocyst and sporocyst metrics (length and width), oocyst wall, including layers, projections, texture and thickness, and the presence and characteristics of structures (micropyle, polar granule, oocyst residuum, Stieda and substieda bodies, refractile bodies, nucleus, residuum, adherent membranes, sporodium and sutures) (Duszynski & Wilber, 1997). When comparing features, Isospora gnorimopsar differed from Isospora cacici (Lainson 1994), Isospora belicosa (Upton et al., 1995), Isospora icterus and Isospora graceannae (Upton and Whitaker 2000). Isospora chopi was compared to Isospora divitis (Pellérdy 1967) and differed from this species.

Isospora dominicana, I. beagai, I. ferri and I. ruficapillus, which were found in the Thraupidae feces, were compared to and differed from I. vanriperorum (Levine et al., 1980; Lopes et al., 2007), I. paroariae (Upton et al., 1985), I. pityli and I. formarum (McQuistion and Capparella, 1992), I. saltatori (Berto et al. 2008b), I. trincaferri, (Berto et al., 2008b), I. thraupis (Lainson, 1994; Berto, 2010), I. andesensis (Templar et al., 2004; Berto, 2010), I. irisidornisi (Metzelaars et al., 2005; Berto, 2010), I. tiesangui (Berto et al., 2008a; Berto, 2010), I. marambaiensis (Berto et al. 2008a; 2010), I. sepetibensis (Berto et al., 2008a; 2010), I. cadimi (Berto et al., 2009a; 2010), I. navarroi (Berto et al., 2009b; 2010), I. ramphoceli (Berto et al, 2010), I. sanhaci (Berto et al., 2009c; 2010), I. silvasouzai (Berto et al., 2009c; 2010), I. sayacae (Berto et al., 2009c; 2010) and I. similisi (Coelho et al., 2013).

The morphometric and morphologic comparisons enabled the identification of new Isospora species in previously known and unknown passerine host species. However, more reliable and conclusive studies should be developed, including phylogenetic studies, in order to evaluate, compare and group genotypes, using molecular techniques.

In addition to previous studies, we have demonstrated the occurrence of new host species and new coccicidian species in native avian host passerine species. The higher risk for the host species of Thraupidae became clear, as compared to Cardinalidae, Emberizidae, Fringillidae and Turdidae. Within Thraupidae, Saltator similis is the most frequently described host species. Isospora was unpublished in Paroaria dominicana, Schistochlamys ruficapillus and Gnorimopsar chopi. The new species of Isospora described were Isospora dominicana, Isospora ferri, Isospora ruficapillus, Isospora chopi and Isospora gnorimopsar. The new coccidian species and new passerine hosts add to the complexity of Isospora in passerines and indicates for frequent monitoring during rehabilitation.

ACKNOWLEDGMENTS

The authors are indebted to IBAMA (Instituto Brasileiro de Meio Ambiente e Recursos Naturais Renováveis), for the sampled birds. This project is part of the National Institute for Science and Technology (INCT) - Brazilian Livestock Genetic and Health Information (IGSPB) and was partially supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG).

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Publication Dates

• Publication in this collection
  05 June 2020
• Date of issue
  2020

History

• Received
  11 Apr 2019
• Accepted
  23 Nov 2019