Coccidia de Passeriformes da América

Coccidia of New World passerine birds (Aves:Passeriformes): a review of Eimeria Schneider, 1875and Isospora Schneider, 1881 (Apicomplexa: Eimeriidae)

Bruno P. Berto • Walter Flausino •

Douglas McIntosh • Walter L. Teixeira-Filho •

Carlos W. G. Lopes

Received: 28 December 2010 / Accepted: 26 May 2011

� Springer Science+Business Media B.V. 2011

Abstract In the New World, the avian order Pass-

eriformes comprises 47 families and 2,453 species,

yet to date only 21 (45%) of the families and 58 (2%)

of the species have been examined for coccidia, and

from these only two species of Eimeria Schneider,

1875 and 81 species of Isospora Schneider, 1881

have been described. This review contributes to our

understanding of the morphology and systematics of

coccidian parasites of passeriforms, providing a

scientific basis for the identification of sporulated

oocysts recovered from the faeces of passerine birds

from North, Central and South America. To this end,

the coccidia were organised and grouped according to

the family of the host, following the widely recog-

nised concept of family-specificity and the updated

systematics of the class Aves. Details of 83 eimeriid

species are presented along with an illustration and

tabulated data.

Introduction

The order Passeriformes includes [5,000 species

worldwide and accounts for[50% of all avian species.

The New World passerine birds are mostly endemic

and occupy, in the case of South America, a large

number of ecological niches, which, in other conti-

nents, are inhabited by other groups of birds. At present

a total of 1,023 species are found in Brazil, of which

170 are endemic (CBRO, 2011). A small number of

families have numerical predominace, with the families

Tyrannidae, Formicariidae and Furnariidae (Sick, 1997;

IUCN, 2011) demonstrating the greatest levels of species

diversity. In common with other vertebrates, passerine

birds can be infected by coccidia, primarily by species of

Isospora Schneider, 1881 and, to a lesser extent,

Eimeria Schneider, 1875. These parasites generally

have intestinal life-cycles, although some species

present extra-intestinal life-history stages.

At present, our knowledge of the systematics and

morphology of coccidian parasites (i.e. species of

Isospora and Eimeria) of Passeriformes in the

Americas is widely distributed throughout an exten-

sive body of literature which spans three centuries.

The aims of the current review are firstly to assemble

the salient information into a single text, which will

hopefully serve to facilitate the study of the parasites

B. P. Berto (&) � W. Flausino � D. McIntosh �W. L. Teixeira-Filho � C. W. G. Lopes

Departamento de Parasitologia Animal, Instituto de

Veterinaria, Universidade Federal Rural do Rio de Janeiro

(UFRRJ), BR-465 km 7, 23890-000 Seropedica,

RJ, Brazil

e-mail: [email protected]

W. Flausino


D. McIntosh


W. L. Teixeira-Filho


C. W. G. Lopes


123

Syst Parasitol (2011) 80:159–204

DOI 10.1007/s11230-011-9317-8

in question, and secondly to provide an updated

scientific basis for the identification of sporulated

oocysts recovered from the faeces of passerine birds

in North, Central and South America.

Eimeria Schneider, 1875

Species of Eimeria parasitising Passeriformes in the

Americas were first described only recently, when

Berto et al. (2008c, 2009d) described two species

from two species of the Tyrannidae in southeastern

Brazil. Morphometric data for the sporulated oocysts

of these coccidia are presented in Table 1.

Eimeria divinolimai Berto, Flausino, Ferreira &

Lopes, 2008 (Fig. 1a)

Type-host: Casiornis rufus (Vieillot) (Tyrannidae),

rufous casiornis.

Type-locality: Brazil.

Remark: This was the first description of a species of

Eimeria from New World passerine birds (Berto

et al., 2008c).

Eimeria sicki Berto, Luz, Flausino, Ferreira &

Lopes, 2009 (Fig. 1b)

Type-host: Myiarchus ferox (Gmelin) (Tyrannidae),

short-crested flycatcher.

Type-locality: Brazil.

Remarks: Eimeria sicki oocysts are larger than those

of E. divinolimai. In addition, E. divinolimai contains

a polar granule which is not present in E. sicki (see

Berto et al., 2009d) (Table 1).

Isospora Schneider, 1881

Hundreds of species of Isospora have been described

from passerine birds; however, the majority of these

were recorded from Eurasia. To date, 21 families of

Passeriformes have been recognised as hosts for

Isospora spp. in the New World. These are: (1) the

Dendrocolaptidae, (2) Furnariidae and (3) Thamno-

philidae of the parvorder Furnariida, infraorder

Tyranni; (4) the Cotingidae and (5) Tyrannidae of

the parvorder Tyrannida, infraorder Tyranni; (6) the

Corvidae and (7) Meliphagidae of the parvorder

Corvida, infraorder Passeri; (8) the Cardinalidae, (9)

Coerebidae, (10) Emberizidae, (11) Estrildidae, (12) Ta

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160 Syst Parasitol (2011) 80:159–204

123

Fringillidae, (13) Hirundinidae, (14) Icteridae, (15)

Parulidae, (16) Passeridae, (17) Sturnidae, (18)

Thraupidae, (19) Timaliidae, (20) Turdidae and (21)

Zosteropidae of the parvorder Passerida, infraorder

Passeri.

The sections which follow provide descriptions

and illustrations of species of Isospora arranged

according to the family, parvorder and infraorder of

their passerine hosts, following the widely recognised

concept of family-specificity and the updated sys-

tematics (IUCN, 2011) of the class Aves. The

comparative morphometric data for the sporulated

oocysts of all Isospora species recorded from New

World passerine birds are provided in Tables 2–12.

Host: Infraorder Tyranni Wetmore & Miller

Host: Parvorder Furnariida Sibley, Ahlquist

& Monroe

Host: Family Dendrocolaptidae Gray

Isospora concentrica McQuistion & Capparella,

1995 (Fig. 1c)

Type-host: Dendrocolaptes certhia radiolatus (Sclater,

Salvin), Amazonian barred woodcreeper.

Other host: Dendrocolaptes sanctithomae colombi-

anus (Lafresnaye), northern barred woodcreeper.

Type-locality: Ecuador, Provincia de Sucumbios,

Imuya Cocha (0�340S, 75�170W).

Remark: This was the first description from New

World dendrocolaptid birds (McQuistion & Cappa-

rella, 1995) (Table 2).

Isospora magna McQuistion & Capparella, 1995

(Fig. 1d)

Type-host: Dendrocolaptes certhia radiolatus (Sclater,

Salvin), Amazonian barred woodcreeper.


Imuya Cocha (0�340S, 75�170W).

Remark: Isospora magna oocysts present similar

dimensions to those of I. concentrica; however, they

can be distinguished by differences in the Stieda and

substieda bodies (McQuistion & Capparella, 1995)

(Table 2).

Isospora ocellati McQuistion, Walden &

Capparella, 1997 (Fig. 1e)

Type-host: Xiphorhynchus ocellatus napensis (Spix),

ocellated woodcreeper.

Type-locality: Ecuador, Provincia de Morona-Santi-

ago, c.5 km southwest of Taisha (2�220S, 77�300W).

Remark: Isospora ocellati oocysts are smaller than

those of I. magna and I. concentrica (McQuistion

et al., 1997) (Table 2).

Isospora striata McQuistion, Walden & Capparel-

la, 1997 (Fig. 1f)

Type-host: Xiphorhynchus ocellatus napensis (Spix),

ocellated woodcreeper.


ago, c.5 km southwest of Taisha (2�220S, 77�300W).

Remarks: Isospora striata oocysts have similar

dimensions to those of I. ocellati; however, they

can be distinguished via differences in the Stieda

and substieda bodies (McQuistion et al., 1997)

(Table 2).

Isospora ubique McQuistion & Capparella, 1997

(Fig. 1g)

Type-host: Glyphorynchus spirurus (Vieillot),

wedge-billed woodcreeper.


ago, c.5 km SW of Taisha (2�220S, 77�300W).

Remarks: Isospora ubique oocysts are smaller than

those of both I. magna and I. concentrica, but larger

than those of I. ocellati and I. striata. In addition, I.

ubique lacks a substieda body (McQuistion &

Capparella, 1997) (Table 2).

Isospora dendrocinclae McQuistion, Galewsky,

Capparella & Rebling, 2010 (Fig. 1h)

Type-host: Dendrocincla merula merula (Lichten-

stein), white-chinned woodcreeper.

Other host: Dendrocincla merula barletti (Chubb),

white-chinned woodcreeper.

Type-locality: Guyana, Iwokrama Reserve, Kabocalli

Landing, West bank of Essequibo River, c.45 river

miles SE Kurupukari (4�170N, 58�310W).

Other locality (D. m. barletti): Peru, Loreto Departa-

mento, 79 km WNW of Contamana, c.400 m eleva-

tion (7�80S 75�410W).

Remark: The oocysts of I. dendrocinclae present

similar dimensions to those of I. ocellati and I.

striata; however, they can be distinguished by

examination of the Stieda and substieda bodies

(McQuistion et al., 2010) (Table 2).

Syst Parasitol (2011) 80:159–204 161

123

162 Syst Parasitol (2011) 80:159–204

123

Host: Family Furnariidae Gray

Isospora hyloctistum McQuistion & Capparella,

1994 (Fig. 1i)

Type-host: Hyloctistes subulatus assimilis (Ber-

lepsch, Taczanowski), striped woodhaunter.

Type-locality: Ecuador, Provincia de Esmeraldas,

c.20 road km NNW of Alto Tambo, 275 m elevation.

Remark: This represented the first description from

New World furnariid birds (McQuistion & Capparel-

la, 1994) (Table 2).

Isospora scleruri McQuistion & Capparella, 1994

(Fig. 1j)

Type-host: Sclerurus mexicanus obscurior (Hartert),

Tawny-throated leaftosser.

Other host: Sclerurus caudacutus brunneus (Sclater),

black-tailed leaftosser.


c.20 road km NNW of Alto Tambo.

Other locality (S. m. brunneus): Ecuador, Provincia

de Morona-Santiago, c.5 km SW of Taisha.

Remarks: Isospora scleruri presents oocysts which

are larger than those of I. hyloctistum. Moreover, they

can be distinguished based on differences in their

Stieda and substieda bodies (McQuistion & Cappa-

rella, 1994) (Table 2).

Isospora automoli McQuistion, Barber & Cappa-

rella, 1999 (Fig. 1k)

Type-host: Automolus ochrolaemus turdinus (Pelzeln),

buff-throated foliage-gleaner.

Other host: Automolus infuscatus infuscatus (Sclater),

olive-backed foliage-gleaner.


c.20 km NE of Lumbaqui.

Remark: Isospora automoli oocysts present similar

dimensions to those of I. scleruri; however, they can

be distinguished based on the morphology of the

substieda body (McQuistion et al., 1999) (Table 2).

Host: Family Thamnophilidae Swainson

Isospora sagittulae McQuistion & Capparella,

1992 (Fig. 1l)

Type-host: Hylophylax naevioides naevioides (Laf-

resnaye), spotted antbird.



Remark: This is the single Isospora species described

to date from New World thamnophilid birds

(McQuistion & Capparella, 1992a) (Table 2).

Host: Parvorder Tyrannida Wetmore &

Miller

Host: Family Cotingidae Bonaparte

Isospora araponga Dolezalova, Torres, Fernandez

& Modry, 2004 (Fig. 2a)

Type-host: Procnias nudicollis (Vieillot), bare-

throated bellbird.

Type-locality: Brazil. Exact locality not known.

Remarks: Dolezalova et al. (2004) recovered

oocysts of this species from the faeces of bare-

throated bellbirds in Spain. The birds had been

recently imported from Brazil by The Barcelona

City Zoo and were examined because they were in

quarantine. At present, this is the only Isospora

species described from New World cotingid birds

(Table 3).

Host: Family Tyrannidae Vigors

Isospora feroxis Berto, Luz, Flausino, Ferreira &


Type-host: Myiarchus ferox (Gmelin), short-crested

flycatcher.

Fig. 1 Line drawings of coccidia recorded from New World

passerine birds: a. Eimeria divinolimai [adapted from Berto et al.

(2008c)]; b. E. sicki [reproduced from Systematic Parasitology,

74, 75–80 with permission]; c. Isospora concentrica [reproduced

from Acta Protozoologica, 34, 299–302 with permission]; d.

I. magna [reproduced from Acta Protozoologica, 34, 299–302

with permission]; e. I. ocellati [adapted from McQuistion et al.

(1997)]; f. I. striata [adapted from McQuistion et al. (1997)]; g.

I. ubique [reproduced from Acta Protozoologica, 36, 75–78 with

permission]; h. I. dendrocinclae [reproduced from Acta Proto-zoologica, 49, 121–124 with permission]; i. I. hyloctistum[reproduced from Transactions of the American MicroscopicalSociety, 113, 90–95 with permission]; j. I. scleruri [reproduced

from Transactions of the American Microscopical Society, 113,

90–95 with permission]; k. I. automoli [reproduced fromSystematic Parasitology, 44, 71–73 with permission]; l.

I. sagittulae [reproduced from Transactions of the AmericanMicroscopical Society, 111, 365–368 with permission]. Accord-

ing to McQuistion & Capparella (1992a), McQuistion &

Capparella (1994), McQuistion & Capparella (1995; 1997),

McQuistion et al. (1997; 1999; 2010), Berto et al. (2008c,

2009d). Scale-bar: 10 lm

b

Syst Parasitol (2011) 80:159–204 163

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164 Syst Parasitol (2011) 80:159–204

123

Type-locality: Brazil, State of Rio de Janeiro, Mar-

ambaia Island (23�040S, 43�530W).

Remark: This was the first description of an Isospora

species from New World tyrannids (Berto et al.,

2009d) (Table 3).

Isospora mionectesi Berto, Flausino, Luz, Ferreira

& Lopes, 2009 (Fig. 2c)

Type-host: Mionectes rufiventris (Cabanis), grey-

hooded flycatcher.


ambaia Island (23�040S, 43�530W).

Remarks: Isospora mionectesi can be easily distin-

guished from I. feroxis based on the shape of the

oocysts and sporocysts. Specifically, I. feroxis oocysts

are smaller than those of I. mionectesi and present a

sub-spherical shape (Berto et al., 2009e) (Table 3).

Host: Infraorder Passeri L.

Host: Parvorder Corvida Wagler

Host: Family Corvidae Leach

Isospora brachyrhynchi Wobester & Cawthorn,

1985 (Fig. 2d)

Type-host: Corvus brachyrhynchos (Brehm), Amer-

ican crow.

Type-locality: Canada, Province of Saskatchewan.

Remark: This was the first species described from

New World corvids (Wobester & Cawthorn, 1985)

(Table 4).

Isospora cyanocoracis Upton, Current & Clubb,

1985 (Fig. 2e)

Type-host: Cyanocorax chrysops (Vieillot), plush-

crested jay.

Type-locality: Argentina. Exact locality not known.

Remarks: Upton et al. (1985) described this species

from birds in Florida imported from Argentina. The

oocysts of I. cyanocoracis are larger than those of

I. brachyrhynchi (see Upton et al., 1985) (Table 4).

Isospora calocitta Upton, Wright & Langen, 1995

(Fig. 2f)

Type-host: Calocitta formosa formosa (Swainson),

white-throated magpie-jay.

Type-locality: Costa Rica, Guanacaste Conservation

Area, Santa Rosa National Park, (10�450N, 85�350W).

Remark: Isospora calocitta oocysts present similar

dimensions to those of I. cyanocoracis; however, theTa

ble

2co

nti

nu

ed

Co

ccid

iaH

ost

(s)

Ref

eren

ceO

ocy

sts

Sp

oro

cyst

s

Sh

ape

Mea

sure

men

ts(l

m)

Sh

ape

ind

exW

all

(lm

)P

ola

rg

ran

ule

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ape

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sure

men

ts(l

m)

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eda

bo

dy

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bst

ied

ab

od

yR

esid

uu

m

I.a

uto

mo

liA

uto

mo

lus

och

rola

emu

stu

rdin

us

(Fu

rnar

iid

ae);

A.

infu

sca

tus

infu

sca

tus

(Fu

rnar

iid

ae)

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uis

tio

net

al.

(19

99

)

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-sp

her

ical

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vo

id

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lar

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fuse

Syst Parasitol (2011) 80:159–204 165

123

166 Syst Parasitol (2011) 80:159–204

123

sporocysts are larger and the sporozoites possess

elongated refractile bodies rather than the spherical

form observed in I. cyanocoracis (Upton et al.,

1995a) (Table 4).

Host: Family Meliphagidae Vigors

Isospora samoaensis Adamczyk, McQuistion &

LaPointe, 2004 (Fig. 2g)

Type-host: Foulehaio carunculatus (Gmelin), wattled

honeyeater.

Type-locality: American Samoa, Tau village on Tau

Island (14�1400100S, 169�3005200W).

Remark: This is the single Isospora species described

to date from New World meliphagid birds (Adam-

czyk et al., 2004) (Table 4).

Host: Parvorder Passerida L.

Host: Family Cardinalidae Ridgway

Isospora vanriperorum Levine, 1982 (Fig. 2h)

Syn. Isospora cardinalis Levine, Van Riper & Van

Riper, 1980 nec Gottschalk, 1972

Type-host: Cardinalis cardinalis (L.), northern

cardinal.

Other host: Saltator similis (Lafresnaye d’Orbigny),

green-winged saltator.

Type-locality: USA, Hawaii.

Other locality: Brazil, State of the Rio de Janeiro,

Rio de Janeiro City.

Remarks: This species was the first coccidium

described from the family Cardinalidae and was

initially named I. cardinalis by Levine et al. (1980).

However, it was subsequently renamed I. vanripero-

rum by Levine (1982b), since the name I. cardinalis

had previously been ascribed to the coccidium

parasite of an extinct passerine, Lophospingus pusil-

lus, described in East Germany by Gottschalk (1972).

Lopes et al. (2007) recovered oocysts, which they

considered identical to those of I. vanriperorum, from

the green-winged saltator Saltator similis in Brazil

(Table 5). According to Carvalho (2009), it is

possible that cross-transmission to a second genus

in the family took place following the introduction of

northern cardinals into South America for captive

breeding purposes.

Isospora pityli McQuistion & Capparella, 1992

(Fig. 2i)

Type-host: Saltator grossus saturatus (Todd), slate-

coloured grosbeak.



Remarks: The I. pityli oocysts are smaller than those

of I. vanriperorum. In addition, it does not present a

polar granule (McQuistion & Capparella, 1992b)

(Table 5).

Isospora formarum McQuistion & Capparella,

1992 (Fig. 2j–k)

Type-host: Saltator grossus grossus (L.), slate-col-

oured grosbeak.

Other host: Saltator grossus saturatus (Todd), slate-

coloured grosbeak.



Remark: Isospora formarum oocysts share similar

dimensions with those of I. vanriperorum; however,

it can be clearly distinguished by the presence of a

characteristic large, triangular or conical substieda

body (McQuistion & Capparella, 1992b) (Table 5).

Isospora saltatori Berto, Balthazar, Flausino &


Type-host: Saltator similis (Lafresnaye d’Orbigny),


Type-locality: Brazil, State of the Rio de Janeiro,

Teresopolis City (22�250S, 42�590W).

Remark: The oocyst dimensions of I. pityli are

similar to those of I. saltatori; however, the former

species does not present a substieda body (Berto

et al., 2008d) (Table 5).


passerine birds: a. Isopora araponga [adapted from Dolezalova

et al. (2004)]; b. I. feroxis [reproduced from SystematicParasitology, 74, 75–80 with permission]; c. I. mionectesi[adapted from Berto et al. (2009e)]; d. I. brachyrhynchi [adapted

from Wobester & Cawthorn (1985)]; e. I. cyanocoracis[reproduced from Systematic Parasitology, 7, 227–229 with per-

mission]; f. I. calocitta [reproduced from Systematic Parasitol-ogy, 31, 195–199 with permission]; g. I. samoaensis [adapted

from Adamczyk et al. (2004)]; h. I. vanriperorum [reproduced

from Journal of Protozoology, 27, 258–259 with permission]; i.

I. pityli [reproduced from Journal of Parasitology, 78, 805–807

with permission]; j–k. I. formarum [reproduced from Journal ofParasitology, 78, 805–807 with permission]. According to

Levine et al. (1980), Wobester & Cawthorn (1985), Upton et al.

(1985), McQuistion & Capparella (1992), Upton et al. (1995a),

Adamczyk et al. (2004), Dolezalova et al. (2004), Berto et al.

(2009d, e). Scale-bar: 10 lm

b

Syst Parasitol (2011) 80:159–204 167

123

Ta

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iduum

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chos

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ter

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ical

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.0–1.3

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ical

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(17–21

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rmosa

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net

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(1995a)

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spher

ical

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927.7

(26–31

9

25–29)

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)

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layer

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pre

sent,

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czyk

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.

(2004)

ovoid

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9

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larg

ere

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mpac

t

168 Syst Parasitol (2011) 80:159–204

123

Ta

ble

5C

om

par

ativ

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orp

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(19

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ard

inal

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ella

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her

ical

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n

& Cap

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(20

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her

ical

26

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(24

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)

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her

ical

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(18

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la(C

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-sp

her

ical

24

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23

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(23

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21

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rou

nd

edsm

all

dif

fuse

Syst Parasitol (2011) 80:159–204 169

123

170 Syst Parasitol (2011) 80:159–204

123

Isospora trincaferri Berto, Balthazar, Flausino &


Type-host: Saltator similis (Lafresnaye d’Orbigny),




Remark: Isospora trincaferri oocysts are larger than

those of I. pityli and I. saltatori, and they present a

large polar granule and prominent substieda body,

which are not found in I. formarum and I. vanrip-

erorum, respectively (Berto et al., 2008d) (Table 5).

Host: Family Coerebidae Lafresnaye &

d’Orbigny

Isospora cagasebi Berto, Flausino, Luz, Ferreira &

Lopes, 2008 (Fig. 3c)

Type-host: Coereba flaveola (L.), bananaquit.


Marambaia Island (23�040S, 43�530W).


World coerebids (Berto et al., 2008b) (Table 5).

Isospora coerebae Berto, Flausino, Luz, Ferreira

& Lopes, 2010 (Fig. 3d)

Type-host: Coereba flaveola (L.), bananaquit.



Remark: This species is very similar to I. cagasebi;

however, the two species can be readily distinguished

by examining the details of the Stieda and substieda

bodies (Berto et al., 2011a) (Table 5).

Host: Family Emberizidae Vigors

Isospora paroariae Upton, Current & Clubb, 1985

(Fig. 3e)

Type-host: Paroaria coronata (Miller), red-crested

cardinal.

Type-locality: Argentina. Exact locality not known.

Remarks: Upton et al. (1985) described this species

from birds in Florida imported from Argentina. This

was the first description from New World emberizids

(Table 6).

Isospora rotunda McQuistion & Wilson, 1988

(Fig. 3f)

Type-host: Camarhynchus parvulus (Gould), small

tree-finch.

Type-locality: Galapagos archipelago, Isabela Island,

near Sierra Negra.

Remarks: Isospora rotunda oocysts present a polar

granule, which is absent in I. paroariae. Furthermore,

the geographical isolation of the Galapagos archipel-

ago from continental South America is considered to

represent a segregational factor for species of Isos-

pora (see McQuistion & Wilson, 1988; Ball &

Daszak, 1997; Carvalho-Filho et al., 2005; Silva

et al., 2006; Berto et al., 2009a; Balthazar et al., 2009;

Pereira et al., 2011) (Table 6).

Isospora fragmenta McQuistion & Wilson, 1988

(Fig. 3g)


tree-finch.


near Sierra Negra.

Remark: Isospora fragmenta presents oocysts which

are larger than those of I. paroariae and I. rotunda

and can be easily distinguished by the presence of

10–20 polar granules (McQuistion & Wilson, 1988)

(Table 6).

Isospora exigua McQuistion & Wilson, 1988

(Fig. 3h)


tree-finch.


near Sierra Negra.

Remarks: Isospora exigua oocysts do not present the

polar granules encountered in I. fragmenta and

I. rotunda. In addition, it can be distinguished from


passerine birds: a. Isospora saltatori [reproduced from ActaProtozoologica, 47, 263–267 with permission]; b. I. trincaferri[reproduced from Acta Protozoologica, 47, 263–267 with

permission]; c. I. cagasebi [adapted from Berto et al. (2011a)];

d. I. coerebae [adapted from Berto et al. (2011a)]; e. I. paroariae[reproduced from Systematic Parasitology, 7, 227–229 with

permission]; f. I. rotunda [reproduced from Journal of Parasi-tology, 35, 98–99 with permission]; g. I. fragmenta [reproduced

from Journal of Parasitology, 35, 98–99 with permission]; h.

I. exigua [reproduced from Journal of Parasitology, 35, 98–99

with permission]; i. I. temeraria [reproduced from Journal ofParasitology, 35, 98–99 with permission]; j. I. geospizae[reproduced from Systematic Parasitology, 14, 141–144, 1989

with permission]; k. I. daphnensis [reproduced from Journal ofParasitology, 76, 30–32 with permission]; l. I. tiaris [reproduced

from Journal of Parasitology, 83, 465–466 with permission].

According to Upton et al. (1985), McQuistion & Wilson (1988;

1989), McQuistion (1990), Ball & Daszak (1997), Berto et al.

(2008d, 2011a). Scale-bar: 10 lm

b

Syst Parasitol (2011) 80:159–204 171

123

I. paroariae via differences in the small Stieda and

substieda bodies (McQuistion & Wilson, 1988)

(Table 6).

Isospora temeraria McQuistion & Wilson, 1988

(Fig. 3i)


tree-finch.


near Sierra Negra.

Remark: Isospora temeraria is different from I.

temeraria, I. exigua, I. fragmenta, I. rotunda and I.

paroariae because it presents ellipsoidal and large

oocysts and 1–4 polar granules (McQuistion &

Wilson, 1988) (Table 6).

Isospora geospizae McQuistion & Wilson, 1989

(Fig. 3j)

Type-host: Geospiza fuliginosa (Gould), small

ground-finch.

Other host: Geospiza fortis (Gould), medium ground-

finch.

Type-locality: Galapagos archipelago, Santa Cruz

Island, Puerto Ayora and Los Tuneles region.

Remark: The oocysts of I. geospizae are the smallest

recorded to date among the Isospora species associ-

ated with emberizids (McQuistion & Wilson, 1989)

(Table 6).

Isospora daphnensis McQuistion, 1990 (Fig. 3k)

Type-host: Geospiza fortis (Gould), medium ground-

finch.

Type-locality: Galapagos archipelago, Daphne Major

Island.

Remarks: Isospora temeraria is the closest in terms

of morphological characteristics to I. daphnensis;

however, it can be distinguished by details in the

Stieda body, which is more rounded in I. daphnensis.

Moreover, I. daphnensis presents a rough outer

oocyst wall that causes the oocysts to cluster into

small groups or adhere to faecal debris (McQuistion,

1990) (Table 6).

Isospora tiaris Ball & Daszak, 1997 (Fig. 3l)

Type-host: Tiaris fuliginosus (Wied), sooty grassquit.

Type-locality: Venezuela. Exact locality of origin is

unknown.

Remarks: Ball & Daszak (1997), based in the United

Kingdom, described this species from sooty

grassquits imported from Venezuela. Isospora par-

oariae, I. rotunda, I. exigua and I. geospizae oocysts

are all smaller than those of I. tiaris. In contrast, I.

fragmenta oocysts contain larger sporocysts and

present 10–20 polar granules; I. temeraria presents

a knob-like Stieda body; and I. daphnensis has a

rough outer oocyst wall (Table 6).

Isospora sporophilae Carvalho-Filho, Meireles,

Ribeiro & Lopes, 2005 (Fig. 4a)

Type-host: Sporophila caerulescens (Vieillot), dou-

ble-collared seedeater.


Seropedica City (22�43023.7900S, 43�42036.9400W).

Remarks: The hosts were held at the Centro de

Triagem de Animais Silvestres (Centre for Triage of

Wild Animals - CETAS/IBAMA) for rehabilitation

and reintroduction into the wild. Isospora sporophi-

lae can be distinguished from the majority of the

other Isospora species described from New World

emberizids by the absence of the substieda body

(Carvalho-Filho et al., 2005) (Table 6).

Isospora flausinoi Carvalho-Filho, Meireles, Ribe-

iro & Lopes, 2005 (Fig. 4b)





Remark: In common with I. sporophilae, the substieda

body is absent in I. flausinoi; however, I. flausinoi

oocysts are smaller and present a single large polar gran-

ule body (Carvalho-Filho et al., 2005) (Tables 6, 7).

Isospora teixeirafilhoi Carvalho-Filho, Meireles,

Ribeiro & Lopes, 2005 (Fig. 4c)





Remarks: This represented the third species described

by Carvalho-Filho et al. (2005) from double-collared

seedeaters held in captivity at CETAS/IBAMA. It

also lacks a substieda body. However, Isospora

teixeirafilhoi oocysts are smaller than those of I.

sporophilae, and it can be distinguished from I.

flausinoi based on the sporocyst shape, which is

pyriform in I. flausinoi and ovoid in I. teixeirafilhoi

(Tables 6, 7).

172 Syst Parasitol (2011) 80:159–204

123

Ta

ble

6C

om

par

ativ

em

orp

ho

log

yo

fIs

osp

ora

spp

.re

cord

edfr

om

New

Wo

rld

pas

seri

ne

bir

ds

of

the

infr

aord

erP

asse

ri,

par

vo

rder

Pas

seri

da

(Par

t2

)

Cocc

idia

Host

(s)

Ref

eren

ceO

ocy

sts

Sporo

cyst

s

Shap

eM

easu

rem

ents

(lm

)

Shap

e

index

Wal

l(l

m)

Pola

r

gra

nule

Shap

eM

easu

rem

ents

(lm

)

Sti

eda

body

Subst

ieda

body

Res

iduum

I.paro

ari

ae

Paro

ari

aco

ronate

(Em

ber

izid

ae)

Upto

net

al.

(1985

)

sub-s

pher

ical

22.3

921.4

(19–26

9

18–24)

1.1 (1

.0–1.1

)

bi-

layer

ed,

c.1.8

abse

nt

ovoid

15.2

910.0

(14–17

9

8–12)

pre

sent

pro

min

ent

com

pac

t

I.ro

tunda

Cam

arh

ynch

us

parv

ulu

s(E

mber

izid

ae)

McQ

uis

tion

&W

ilso

n

(1988

)

sub-s

pher

ical

21.8

920.9

(20–24

9

19–23)

1.0

one-

layer

ed,

c.1.0

pre

sent

ovoid

15

99.7

(13–16

9

9–10)

knob-l

ike

pro

min

ent

com

pac

t

I.fr

agm

enta

C.

parv

ulu

s(E

mber

izid

ae)

McQ

uis

tion

&W

ilso

n

(1988

)

sub-s

pher

ical

25.3

924.2

(24–27

9

23–25)

1.1

one-

layer

ed,

c.1.0

pre

sent,

10

to20

pyri

form

15.4

911.5

(14–17

9

11–12)

knob-l

ike

pro

min

ent

com

pac

t

I.ex

igua

C.

parv

ulu

s(E

mber

izid

ae)

McQ

uis

tion

&W

ilso

n

(1988

)

sub-s

pher

ical

20.4

920.1

(20–23

9

18–23)

1.0

one-

layer

ed,

c.1.0

abse

nt

ovoid

14

99.5

(13–15

9

8–10)

smal

lsm

all

com

pac

t

I.te

mer

ari

aC

.parv

ulu

s(E

mber

izid

ae)

McQ

uis

tion

&W

ilso

n

(1988

)

elli

pso

idal

25.4

921.1

(21–30

9

17–23)

1.2

one-

layer

ed,

c.1.0

pre

sent,

1

to4

pyri

form

15

910

(14–15

9

9–11)

knob-l

ike

pro

min

ent

com

pac

t

I.geo

spiz

ae

Geo

spiz

afu

ligin

osa

(Em

ber

izid

ae);

G.

fort

is(E

mber

izid

ae)

McQ

uis

tion

&W

ilso

n

(1989

)

sub-s

pher

ical

15.5

914.5

(13–17

9

12–17)

1.1 (1

.0–1.1

)

one-

layer

ed,

c.1.0

pre

sent

ovoid

10

97.5

(10–12

9

6–9)

rounded

smal

lco

mpac

t

I.daphnen

sis

G.

fort

is(E

mber

izid

ae)

McQ

uis

tion

(1990

)

elli

pso

idal

27.3

923.6

(22–30

9

20–27)

1.2 (1

.0–1.3

)

bi-

layer

ed,

c.1.5

pre

sent

ovoid

15.2

910.2

(15–16

9

9–11)

nip

ple

-

like,

rounded

smal

lco

mpac

t

I.ti

ari

sT

iari

sfu

ligin

osu

s(E

mber

izid

ae)

Bal

l&

Das

zak

(1997

)

sub-s

pher

ical

27.1

923.8

(25–30

9

21–27)

1.1

bi-

layer

ed,

c.1.0

pre

sent

ovoid

14.7

910.8

(12–17

9

9–12)

pro

min

ent

pro

min

ent

dif

fuse

I.sp

oro

phil

ae

Sporo

phil

aca

erule

scen

s(E

mber

izid

ae)

Car

val

ho-

Fil

ho

etal

.

(2005

)

sub-s

pher

ical

21.6

920.1

(19–23

9

18–23)

1.0 (1

.0–1.1

)

bi-

layer

ed,

c.1.3

pre

sent,

man

y

spli

nte

r-

like

or

com

ma-

like

gra

nule

s

ovoid

15.1

910.7

(13–17

9

8–13)

knob-l

ike

abse

nt

com

pac

t

Syst Parasitol (2011) 80:159–204 173

123

174 Syst Parasitol (2011) 80:159–204

123

Isopora curio Silva, Literak & Koudela, 2006

(Fig. 4d)

Type-host: Oryzoborus angolensis (L.), lesser seed-

finch.

Type-locality: Brazil, State of the Mato Grosso do

Sul.

Remarks: The oocysts reported in this description

were isolated from the faeces of captive birds.

Isopora curio has no substieda body, and, within this

group, its oocysts are most similar to those of I.

sporophilae. Yet, unlike I. curio, the oocysts of I.

sporophilae present numerous polar granules (Silva

et al., 2006) (Tables 6, 7).

Isospora braziliensis Silva, Literak & Koudela,

2006 (Fig. 4e)


finch.


Sul.

Remarks: This was the second species described from

O. angolensis by Silva et al. (2006). The oocysts used

for its description were isolated from the faeces of

captive birds. Isospora braziliensis has no substieda

body and its oocysts are similar to those of I. flausinoi

and I. teixeirafilhoi; however, in I. braziliensis the

oocysts lack a polar granule and the sporocysts are

slightly more elongated than those of both I. flausinoi

and I. teixeirafilhoi (Tables 6, 7).

Isospora paranaensis Silva, Literak & Koudela,

2006 (Fig. 4f)


finch.


Sul.

Remarks: This represented the third species described

by Silva et al. (2006). Isospora geospizae oocysts are

smaller than those of I. paranaensis, whereas those of

I. tiaris are larger. Both I. paroariae and I. exigua have

no polar granule, and I. fragmenta and I. temeraria

have more than one; I. rotunda presents a knob-like

Stieda body; I. daphnensis has a rough outer oocyst

wall; and I. sporophilae, I. flausinoi, I. teixeirafilhoi,

I. curio and I. braziliensis have no substieda body.

All these features are absent in I. paranaensis

(Tables 6, 7).

Isospora frontalis Berto, Balthazar, Flausino &

Lopes, 2009 (Fig. 4g)

Type-host: Sporophila frontalis (Verreaux), buffy-

fronted seedeater.



Remarks: The oocysts used for the description of this

species were isolated from the faeces of captive birds.

Sporophila frontalis is categorised as ‘Vulnerable’ by

the International Union for Conservation of Nature

and Natural Resources (IUCN, 2011). Only I. tiaris,

I. daphnensis and I. temeraria share similar dimen-

sions with I. frontalis; however, I. frontalis can be

easily distinguished by its elongate sporocyst and by

the presence of splinter-like or comma-shaped polar

granules (Berto et al., 2009a) (Tables 6, 7).

Isospora teresopoliensis Berto, Balthazar, Flausino

& Lopes, 2009 (Fig. 4h)


fronted seedeater.



Remarks: This is the second species described from S.

frontalis by Berto et al. (2009a). The oocysts for its

description were isolated from the faeces of captive

birds. Isospora paranaensis, I. curio, I. tiaris, I.

daphnensis, I. temeraria, I. fragmenta and I. paroariae

all present similar oocyst dimensions to those of I.

teresopoliensis; however, only I. curio and I. paroariae

share with I. teresopoliensis the feature of the absence

of a polar granule. However, I. curio has no substieda

body, and I. teresopoliensis has sporocysts which are

larger than those of I. paroariae (Tables 6, 7).

Fig. 4 Line drawings of coccidia recorded from New

World passerine birds: a. Isospora sporophilae [adapted from

Carvalho-Filho et al. (2005)]; b. I. flausinoi [adapted

from Carvalho-Filho et al. (2005)]; c. I. teixeirafilhoi [adapted

from Carvalho-Filho et al. (2005)]; d. I. curio [adapted from

Silva et al. (2006)]; e. I. braziliensis [adapted from Silva et al.

(2006)]; f. I. paranaensis [adapted from Silva et al. (2006)]; g.

I. frontalis [reproduced from Systematic Parasitology, 73,

65–69 with permission]; h. I. teresopoliensis [reproduced from

Systematic Parasitology, 73, 65–69 with permission]; i. I.chanchaoi [reproduced from Systematic Parasitology, 73,

65–69 with permission]; j. I. ticoticoi [reproduced from ActaProtozoologica, 48, 345–349 with permission]; k. I. boca-montensis [reproduced from Systematic Parasitology, 78,

73–80 with permission]. According to Carvalho-Filho et al.

(2005), Silva et al. (2006), Berto et al. (2009a), Balthazar et al.

(2009b), Pereira et al. (2011). Scale-bar: 10 lm

b

Syst Parasitol (2011) 80:159–204 175

123

Ta

ble

7C

om

par

ativ

em

orp

ho

log

yo

fIs

osp

ora

spp

.re

cord

edfr

om

New

Wo

rld

pas

seri

ne

bir

ds

of

the

infr

aord

erP

asse

ri,

par

vo

rder

Pas

seri

da

(Par

t3

)

Cocc

idia

Host

(s)

Ref

eren

ce(s

)O

ocy

sts

Sporo

cyst

s

Shap

eM

easu

rem

ents

(lm

)

Shap

e

index

Wal

l(l

m)

Pola

r

gra

nule

Shap

eM

easu

rem

ents

(lm

)

Sti

eda

body

Subst

ieda

body

Res

iduum

I.flausi

noi

Sporo

phil

a

caer

ule

scen

s

(Em

ber

izid

ae)

Car

val

ho-

Fil

ho

etal

.

(2005)

sub-

spher

ical

17.3

916.5

(14–20

9

14–20)

1.1 (1

.0–1.2

)

bi-

layer

ed,

c.1.0

pre

sent

pyri

form

14.9

910.7

(12–18

9

8–12)

rounded

abse

nt

com

pac

t

I.te

ixei

rafilh

oi

S.

caer

ule

scen

s

(Em

ber

izid

ae)

Car

val

ho-

Fil

ho

etal

.

(2005)

sub-

spher

ical

17.4

916.8

(16––19

9

14–19)

1.0 (1

.0–1.2

)

bi-

layer

ed,

c.1.2

pre

sent

ovoid

11.7

98.1

(9–14

9

6–9)

knob-

like

abse

nt

com

pac

t

I.cu

rio

Ory

zoboru

s

angole

nsi

s

(Em

ber

izid

ae)

Sil

va

etal

.

(2006)

sub-

spher

ical

24.6

923.6

(22–26

9

22–25)

1.0 (1

.0–1.2

)

bi-

layer

ed,

c.1.5

abse

nt

ovoid

13.2

910.9

(15–17

9

10–13)

pre

sent

abse

nt

dif

fuse

I.bra

zili

ensi

sO

.angole

nsi

s

(Em

ber

izid

ae)

Sil

va

etal

.

(2006)

sub-

spher

ical

17.8

916.9

(16–19

9

16–18)

1.1 (1

.0–1.1

)

one- la

yer

ed,

c.1.0

abse

nt

elli

pso

idal

13.2

910.8

(12–14

9

9–12)

flat

tened

abse

nt

dif

fuse

I.para

nae

nsi

sO

.angole

nsi

s

(Em

ber

izid

ae)

Sil

va

etal

.

(2006)

sub-

spher

ical

to elli

pso

idal

24.3

919.8

(22–26

9

18–22)

1.2 (1

.1–1.4

)

one- la

yer

ed,

c.1.5

pre

sent

ovoid

15.7

910.1

(14–18

9

8–12)

pre

sent

pre

sent

com

pac

t

I.fr

onta

lis

Sporo

phil

a

fronta

lis

(Em

ber

izid

ae)

Ber

toet

al.

(2009a)

sub-

spher

ical

27.9

926.9

(27–29

9

25–28)

1.0 (1

.0–1.1

)

bi-

layer

ed,

c.1.4

pre

sent,

man

y

spli

nte

r-li

ke

or

com

ma-

like

gra

nule

s

elongat

e

elli

pso

idal

19.6

911.1

(19–21

9

10–12)

knob-

like

del

icat

edif

fuse

I.te

reso

poli

ensi

sS.

fronta

lis

(Em

ber

izid

ae)

Ber

toet

al.

(2009a)

sub-

spher

ical

25.7

924.3

(24–27

9

23–25)

1.1 (1

.0–1.1

)

bi-

layer

ed,

c.1.3

abse

nt

ovoid

18.8

911.2

(18–20

9

10–12)

nip

ple

-

like

larg

edif

fuse

I.ch

anc

haoi

S.

fronta

lis

(Em

ber

izid

ae);

S.

schis

tace

a

(Em

ber

izid

ae)

Ber

toet

al.

(2009a)

;

Bal

thaz

ar

etal

.

(2009a)

sub-

spher

ical

or

ovoid

24.2

922.0

(23–26

9

21–23)

1.1 (1

.0–1.1

)

bi-

layer

ed,

c.1.2

pre

sent,

1or

2el

lipso

idal

16.1

910.3

(15–17

9

10–11)

nip

ple

-

like

smal

lco

mpac

t

I.ti

coti

coi

Zonot

rich

ia

capen

sis

(Em

ber

izid

ae)

Bal

thaz

ar

etal

.

(2009b

)

sub-

spher

ical

23.3

922.4

(20–25

9

20–24)

1.1 (1

.0–1.1

)

bi-

layer

ed,

c.1.2

usu

alm

ente

abse

nt

elli

pso

idal

17.0

910.8

(15–18

9

10–11)

nip

ple

-

like

wit

h com

par

tmen

t

dif

fuse

I.boca

monte

nsi

sG

uber

nat

rix

cris

tata

(Em

ber

izid

ae)

Per

eira

etal

.

(2011)

sub-

spher

ical

32.1

928.9

(27–34

9

26–32)

1.0 (1

.0–1.2

)

bi-

layer

ed,

c.1.5

usu

ally

abse

nt

elli

pso

idal

17.3

912.2

(16–19

9

11–13)

hal

f- moon-

shap

ed

pro

min

ent

com

pac

t

176 Syst Parasitol (2011) 80:159–204

123

Isospora chanchaoi Berto, Balthazar, Flausino &

Lopes, 2009 (Fig. 4i)


fronted seedeater.

Other host: Sporophila schistacea (Lawrence), slate-

coloured seedeater.



Remarks: This is the third species described by Berto

et al. (2009a). Subsequently, Balthazar et al. (2009a)

reported S. schistacea as a new host in the same local-

ity. Isospora teresopoliensis, I. paranaensis, I. curio,

I. daphnensis, I. temeraria, I. fragmenta, I. rotunda

and I. paroariae all present similar oocyst dimensions

to I. chanchaoi; however, I. teresopoliensis, I. curio

and I. paroariae have no polar granule, whereas

I. fragmenta has many, I. daphnensis has a rough

outer oocyst wall, and I. paranaensis, I. rotunda and

I. temeraria have ovoid, ovoid and pyriform spo-

rocysts, respectively. All these features are absent in

I. paranaensis (see Berto et al., 2009a) (Tables 6, 7).

Isospora ticoticoi Balthazar, Berto, Flausino &

Lopes, 2009 (Fig. 4j)

Type-host: Zonotrichia capensis (Muller), rufous-

collared sparrow.



Remarks: This species was also reported by Berto

et al. (2009a) in the same locality and also from

captive birds. It has a substieda body with a

compartment, which is an isolated and unique feature

among the Isospora species from emberizids (Bal-

thazar et al., 2009b) (Tables 6, 7).

Isospora bocamontensis Pereira, Berto, Flausino,

Lovato & Lopes, 2011 (Fig. 4k)

Type-host: Gubernatrix cristata (Vieillot), yellow

cardinal.

Type-locality: Brazil, State of the Rio Grande do Sul,

Santa Maria City, Boca do Monte district

(29�38032.2500S, 53�55044.6200W).

Remarks: The oocysts of this species were isolated

from the faeces of captive birds. Gubernatrix cristata

is categorised as ‘Endangered’ by the International

Union for Conservation of Nature and Natural

Resources (IUCN, 2011). Only three species, I.

daphnensis, I. tiaris and I. frontalis have similar

dimensions to I. bocamontensis. In each of these the

substieda body is smaller than in I. bocamontensis.

Furthermore, the ellipsoidal sporocysts of I. boca-

montensis are readily distinguishable (Pereira et al.,

2011) (Tables 6, 7).

Host: Family Estrildidae Bonaparte

Isospora ivensae Levine, Van Riper & Van Riper,

1980 (Fig. 5a)

Type-host: Lonchura punctulata (L.), scaly-breasted

Munia.


Remark: This was the first species of Isospora

described from New World estrildid birds (Levine

et al., 1980) (Table 8).

Isospora lyonensis Upton, Marchiondo & Wil-

liams, 1988 (Fig. 5b)

Type-host: Lonchura punctulata (L.), scaly-breasted

Munia.

Type-locality: USA, Hawaii, Oahu, Manoa Valley,

Lyon Arboretum.

Remark: Isospora lyonensis can easily be distin-

guished from I. ivensae by the presence of a substieda

body, which is absent in I. ivensae (see Upton et al.,

1988) (Table 8).

Host: Family Fringillidae Leach

Isospora canaria Box, 1975 (Fig. 5c)

Type-host: Serinus canaria (L.), island canary.

Type-locality: USA. Exact locality not known.

Remarks: The oocysts upon which this description

was based were isolated from the faeces of captive

birds. This was the first description from New World

fringillids (Box, 1975) (Table 8).

Isospora serini (Aragao, 1933) Box, 1975 (Fig. 5d)

Syns Haemogregarina serini Aragao, 1933; Lanke-

sterella serini (Aragao, 1933) Lainson, 1959;

Atoxoplasma serini (Aragao, 1933) Levine, 1982

Type-host: Serinus canaria (L.), island canary.

Type-locality: USA. Exact locality not known.

Remarks: Isospora serini was the second species

described by Box (1975). It can be distinguished from

I. canaria by differences in the Stieda and substieda

bodies. In additional to morphological differences,

subsequent studies by Box (1977; 1981) demonstrated

that I. serini has an extra-intestinal cycle (Table 8).

Syst Parasitol (2011) 80:159–204 177

123

178 Syst Parasitol (2011) 80:159–204

123

Isospora lacazei (Labbe, 1893) Levine, 1982

(Fig. 5e)

Type-host: Carduelis carduelis (L.), European

goldfinch.

Other hosts: Carduelis chloris (L.), European green-

finch; Fringilla coelebs (L.), Eurasian chaffinch.

Type-locality: Spain, Province of Cordoba.

Other locality: England, Berkshire, Ascot, College

Field Station.

Remarks: The overwhelming majority of reports of

coccidia in passerines refer to I. lacazei. Moreover,

the introduction of C. carduelis and C. chloris into

the Americas (United States, Brazil, Uruguay and

Argentina) (IUCN, 2011), coupled with reports of

Isospora sp. from fringilids in the USA by Boughton

et al. (1938), supports the likely presence of this

coccidian species in the New World. Levine (1982a)

classified this coccidium as a parasite of C. carduelis,

in view of the description of Hernandez-Rodriguez

et al. (1976a,b). This description is similar to that of

oocysts recorded from C. chloris and F. coelebs by

Anwar (1966b). The oocysts of I. lacazei can be

distinguished from those of I. canaria and I. serini by

its pyriform sporocysts (Table 8).

Isospora loxopis Levine, Van Riper & Van Riper,

1980 (Fig. 5f)

Type-host: Hemignathus virens (Cabanis), common

amakihi.


Remark: Isospora loxopis is different from the other

species because its oocysts have no polar granule or

substieda body (Levine et al., 1980) (Table 8).

Isospora atrata Rossi, Macchione & Perrucci, 1996

(Fig. 5g)

Type-host: Carduelis atrata (Lafresnaye d’Orbigny),

black siskin.

Type-locality: Bolivia and Peru. Exact locality not

known.

Remarks: Rossi et al. (1996) recovered oocysts of

this species from the faeces of black siskins imported

from South America into Spain. Oocysts of I. atrata

are smaller than those of I. loxopis. In addition, it can

be distinguished from I. canaria, I. serini and I.

lacazei by the shape of its substieda body, which is

trapezoidal with a linear base (Table 8).

Isospora gryphoni Olson, Gissing, Barta & Mid-

dleton, 1998 (Fig. 5h)

Type-host: Carduelis tristis (L.), American goldfinch.

Type-locality: Canada, Province of Ontario, Guelph,

University of Guelph arboretum.

Other locality: Canada, Province of Ontario, Eden

Mills.

Remark: Only I. lacazei presents similar dimensions

to I. gryphoni; however, they can be distinguished by

the charactistic ovoid sporocyst of I. gryphoni (see

Olson et al., 1998) (Table 8).

Host: Family Hirundinidae Rafinesque

Isospora petrochelidon Stabler & Kitzmiller, 1972

(Fig. 5i)

Type-host: Petrochelidon pyrrhonota (Vieillot), cliff

swallow.

Type-locality: USA, Colorado, Douglas County.

Remarks: At present this is the only Isospora species

described from New World hirundinids (Stabler &

Kitzmiller, 1972) (Table 9).

Host: Family Icteridae Vigors

Isospora divitis Pellerdy, 1967 (Fig. 5j)

Type-host: Dives atroviolaceus (Lafresnaye d’Orbi-

gny), cuban blackbird.

Type-locality: Cuba, Havana Zoo.


World icterid birds (Pellerdy, 1967) (Table 9).

Isospora cacici Lainson, 1994 (Fig. 6a)

Type-host: Cacicus cela cela (L.), yellow-rumped

cacique.


passerine birds: a. Isospora ivensae [reproduced from Journal ofProtozoology, 27, 258–259 with permission]; b. I. lyonensis[reproduced from Systematic Parasitology, 12, 81–85 with

permission]; c. I. canaria [reproduced from Journal ofProtozoology, 22, 165–169 with permission]; d. I. serini[reproduced from Journal of Protozoology, 22, 165–169 with

permission]; e. I. lacazei [reproduced from Journal of Proto-zoology, 13, 84–90 with permission]; f. I. loxopis [reproduced

from Journal of Protozoology, 27, 258–259 with permission]; g.

I. atrata [reproduced from Journal of Eukaryotic Microbiology,

43, 489–491 with permission]; h. I. gryphoni [reproduced from

Journal of Parasitology, 84, 153–156 with permission];

i. I. petrochelidon [adapted from Stabler & Kitzmiller (1972)];

j. I. divitis [adapted from Pellerdy (1967)]. According to Anwar

(1966b), Pellerdy (1967), Stabler & Kitzmiller (1972), Box

(1975), Levine et al. (1980), Upton et al. (1988), Rossi et al.

(1996), Olson et al. (1998). Scale-bar: 10 lm

b

Syst Parasitol (2011) 80:159–204 179

123

Ta

ble

8C

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par

ativ

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sent

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eous

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sent

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pac

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b-

spher

ical

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9

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cern

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ar

(1966b);

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nan

dez

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Rodri

guez

etal

.

(1976a,

b)

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ical

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9

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layer

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sent,

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sent

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sent

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pac

t

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Hem

ignath

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vire

ns

(Fri

ngil

lidae

)

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ine

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.

(1980)

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spher

ical

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(25–26

9

22–25)

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layer

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nt

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9

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ngil

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iet

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.0–1.1

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layer

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sent,

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lin

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tinct

com

pac

t

180 Syst Parasitol (2011) 80:159–204

123

Type-locality: Brazil, State of the Para, Serra dos

Carajas (Amazonian Brazil).

Remark: Isospora loxopis is different from I. divitis

because its oocysts contain one or two polar granules

and a prominent substieda body (Lainson, 1994)

(Table 9).

Isospora bellicosa Upton, Stamper & Whitaker,

1995 (Fig. 6b)

Type-host: Sturnella bellicosa (Filippi), Peruvian

meadowlark.

Type-locality: Peru, at an unknown location west of

the Andes mountains.

Remarks: Upton et al. (1995b) described this coccid-

ium from Peruvian meadowlarks housed at the

National Aquarium in Baltimore, Maryland, USA.

These passerines had been wild-caught as adults in

Peru. This species can be distinguished from other

Isospora species from this host-family owing to its

elongate sporocysts and Stieda and substieda bodies

(Table 9).

Isospora icterus Upton & Whitaker, 2000 (Fig. 6c)

Type-host: Icterus icterus (L.), Venezuelan troupial.

Type-locality: USA, Maryland, Baltimore, National

Aquarium.

Remarks: Upton & Whitaker (2000) described this

species from the same locality as Upton et al.

(1995b); however, in their report, the origin of the

hosts was given as unknown. Oocysts of I. icterus are

morphologically similar to I. cacici and I. bellicosa;

however, it can be distinguished because it presents

an oocyst residuum and a large substieda body

(Upton & Whitaker, 2000) (Table 9).

Isospora graceannae Upton & Whitaker, 2000

(Fig. 6d)

Type-host: Icterus graceannae (Cassin), white-edged

oriole.

Type-locality: USA, Maryland, Baltimore, National

Aquarium.

Remarks: This was the second species described by

Upton & Whitaker (2000). It is the only species,

from the host-family Icteridae, which has a substi-

eda body with a compartment; a feature which

makes it readily distinguishable (Upton & Whitaker,

2000) (Table 9).

Host: Family Parulidae Wetmore et al.

Isospora piacobrai Berto, Flausino, Luz, Ferreira

& Lopes, 2009 (Fig. 6e)

Type-host: Geothlypis aequinoctialis (Gmelin),

masked yellowthroat.


ambaia Island (23�040S. 43�530W).

Remark: To date, this is the only Isospora species

described from New World parulids (Berto et al.,

2009f) (Table 9).

Host: Family Passeridae Rafinesque

Isospora passeris Levine, 1982 (Fig. 6f)

Type-host: Passer domesticus (L.), house sparrow.

Type-locality: USA. Exact locality of origin is

unknown.

Remarks: Levine (1982a) proposed this name for an

intestinal species of Isospora described from house

sparrows, using the oocysts features reported previ-

ously by Levine & Mohan (1960). This is the only

Isospora species so far described from New World

passerids (Table 10).

Host: Family Sturnidae Rafinesque

Isospora graculai Bhatia, Chauhan, Arora &

Agrawal, 1973 (Fig. 6g)

Type-host: Gracula religiosa (L.), hill myna.

Type-locality: India, Delhi Zoo.

Other locality: USA (imported for commercial sale

as household pets).

Remarks: Isospora graculai was originally described

by Bhatia et al. (1973). Upton et al. (1984) subse-

quently re-described this species, providing more

features, when they recovered morphologically sim-

ilar oocysts in the faeces of hill mynas imported from

Southeast Asia into the USA. This represented the

first description from New World sturnids (Table 10).

Isospora rothschildi Upton, Wilson, Norton &

Greiner, 2001 (Fig. 6h)

Type-host: Leucopsar rothschildi (Stresemann), Bali

starling.

Type-locality: Indonesia, Bali.

Other locality: USA, Kansas, Topeka, Topeka Zoo-

logical Park.

Syst Parasitol (2011) 80:159–204 181

123

182 Syst Parasitol (2011) 80:159–204

123

Remarks: Isospora rothschildi was described from

starlings hatched at the Topeka Zoological Park, but

derived from parents originally captured live in Bali.

This coccidium is easily distinguished from I. gracu-

lai owing to it having a substieda body with a

compartment (Upton et al., 2001) (Table 10).

Host: Family Thraupidae Cabanis

Isospora thraupis Lainson, 1994 (Fig. 6i)

Type-host: Thraupis palmarum melanoptera (Sclat-

er), palm tanager.

Type-locality: Brazil, State of the Para, Serra dos

Carajas (Amazonian Brazil).

Remarks: This was the first species of Isospora

reported from New World thraupids (Lainson, 1994;

Berto et al., 2010c) (Table 10).

Isospora andesensis Templar, McQuistion &

Capparella, 2004 (Fig. 7a)

Type-host: Chlorospingus ophthalmicus (Du Bus

Gisignies), common bush-tanager.

Type-locality: Peru, San Martin Departamento,

c.24 km ENE of Florida (village) (5 4302300S,

77�4500100W).

Remarks: Isospora andesensis oocysts have a polar

granule and are slightly larger than those of I.

thraupis. Futhermore, I. thraupis has an inconspicu-

ous Stieda body and a small substieda body, wheras I.

andesensis presents a prominent, triangular Stieda

body and lacks a substieda body (Templar et al.,

2004; Berto et al., 2010c) (Table 10).

Isospora iridosornisi Metzelaars, Spaargaren,

McQuistion & Capparella, 2005 (Fig. 7b)

Type-host: Iridosornis analis (Tschudi), yellow-

throated tanager.

Type-locality: Peru, San Martin Departamento, ca.

24 km ENE of Florida (village) (5�4100900S, 77�450

1600W).

Remark: Isospora iridosornisi oocysts have a polar

granule and similar dimensions to those of I. andes-

ensis; however, they can be easily distinguished by

comparing their Stieda and substieda bodies (Metz-

elaars et al., 2005; Berto et al., 2010c) (Table 10).

Isospora tiesangui Berto, Flausino, Luz, Ferreira

& Lopes, 2008 (Fig. 7c)

Type-host: Ramphocelus bresilius dorsalis (Sclater),

Brazilian tanager.

Other hosts: Thraupis palmarum (Wied), palm tan-

ager; Dacnis cayana (L.), blue dacnis.



Remarks: In the original description, this coccidium

was reported to parasitise only R. b. dorsalis;

however, Berto et al. (2010a) subsequently recorded

T. palmarum and D. cayana as new hosts on

Marambaia Island. Oocysts of I. tiesangui lacks the

polar granule found in I. andesensis and I. iridos-

ornisi, and this species can be differentiated from

I. thraupis owing to its large, prominent substieda

body (Berto et al., 2008a, 2010a,c, 2011b)

(Table 10).

Isospora marambaiensis Berto, Flausino, Luz,

Ferreira & Lopes, 2008 (Fig. 7d)


Brazilian tanager.



Remarks: This was the second species described from

R. b. dorsalis on Marambaia Island. Oocysts of

I. marambaiensis are larger than those of I. tiesangui,

I. andesensis, I. iridosornisi and I. thraupis (Berto

et al., 2008a, 2010c, 2011b) (Table 10).

Isospora sepetibensis Berto, Flausino, Luz, Ferreira

& Lopes, 2008 (Fig. 7e)


Brazilian tanager.

Other host: Dacnis cayana (L.), blue dacnis.



Remarks: This was the third species described from

R. b. dorsalis on Marambaia Island. Thereafter, Berto


passerine birds: a. Isospora cacici [adapted from Lainson

(1994)]; b. I. bellicosa [adapted from Upton et al. (1995b)];

c. I. icterus [adapted from Upton & Whitaker (2000)]; d.

I. graceannae [adapted from Upton & Whitaker (2000)]; e.

I. piacobrai [reproduced from Systematic Parasitology, 75,

225–230 with permission]; f. I. passeris [reproduced from

Journal of Parasitology, 46, 733–741 with permission]; g. I.graculai [reproduced from Systematic Parasitology, 6, 237–240

with permission]; h. I. rothschildi [reproduced from SystematicParasitology, 48, 47–53 with permission]; i. I. thraupis[adapted from Lainson (1994)]. According to Levine (1982a),

Upton et al. (1984), Lainson (1994), Upton et al. (1995b), Upton

& Whitaker (2000), Upton et al. (2001), Berto et al. (2009f).

Scale-bar: 10 lm

b

Syst Parasitol (2011) 80:159–204 183

123

Ta

ble

9C

om

par

ativ

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Div

es

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ola

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nt

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Caci

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n

(1994

)

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)

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9

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Upto

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Upto

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23.9

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(20–26

9

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184 Syst Parasitol (2011) 80:159–204

123

Ta

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Syst Parasitol (2011) 80:159–204 185

123

et al. (2011b) reported D. cayana as a new host in the

same locality. Oocysts of I. sepetibensis have similar

dimensions to those of I. iridosornisi; however,

I. sepetibensis is slightly larger, usually presents two

polar granules and its sporocysts are large and

ellipsoidal (Berto et al., 2008a, 2010c, 2011b)

(Table 10).

Isospora cadimi Berto, Flausino, Luz, Ferreira &

Lopes, 2009 (Fig. 7f)


Brazilian tanager.



Remarks: This was the fourth species described from

R. b. dorsalis on Marambaia Island. It is the only

Isospora species from the host-family Thraupidae

containing a substieda body with a compartment

(Berto et al., 2009b, 2010c, 2011b) (Tables 10, 11).

Isospora navarroi Berto, Flausino, Luz, Ferreira &

Lopes, 2009 (Fig. 7g)


Brazilian tanager.

Other host: Thraupis palmarum (Wied), palm tanager



Remarks: This was the fifth species described from

R. b. dorsalis on Marambaia Island. Berto et al.

(2011b) subsequently reported T. palmarum as a new

host in the same locality. Oocysts of Isospora

navarroi have no polar granule and present a small

substieda body. Only I. thraupis shares these features;

however, these species can be distinguished because

I. navarroi has ellipsoidal sporocysts and a single

robust refractile body in the sporozoite (Berto et al.,

2009b, 2010c, 2011b) (Tables 10, 11).

Isospora ramphoceli Berto, Flausino, Luz, Ferreira

& Lopes, 2010 (Fig. 7h)


Brazilian tanager.



Remarks: This was the sixth species described from

R. b. dorsalis on Marambaia Island. It lacks both a

polar granule and a large substieda body. Only

I. tiesangui also has these features; however, they can

be distinguished because in I. ramphoceli the StiedaTa

ble

10

con

tin

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tera

l

186 Syst Parasitol (2011) 80:159–204

123

body is knob-like and the sporocysts are less elongate

(Berto et al., 2010b,c, 2011b) (Tables 10, 11).

Isospora sanhaci Berto, Balthazar, Flausino &

Lopes, 2009 (Fig. 7i)

Type-host: Thraupis sayaca (L.), sayaca tanager.



Remarks: The oocysts of this species were isolated

from the faeces of captive birds. In common with

I. tiesangui and I. ramphoceli, I. sanhaci also lacks a

polar granule and a large substieda body; however,

I. tiesangui has a flattened Stieda body and I.

ramphoceli has an ellipsoidal or slightly ovoid

sporocyst. In contrast, I. sanhaci has an elongate

sporocyst and nipple-like Stieda body (Berto et al.,

2009c, 2010c) (Tables 10, 11).

Isospora sayacae Berto, Balthazar, Flausino &

Lopes, 2009 (Fig. 7j)





Berto et al. (2009c) from T. sayaca. Only I.

marambaiensis has similar dimensions to I. sayacae;

however, I. sayacae has bottle-shaped sporocysts, a

prominent Stieda body and a large substieda body

(Berto et al., 2009c, 2010c) (Tables 10, 11).

Isospora silvasouzai Berto, Balthazar, Flausino &





Remarks: This was the third species described by

Berto et al. (2009c) from T. sayaca. Oocytes of

I. silvasouzai have a polar granule, a delicate Stieda

body and a small substieda body. These features are

not shared with any other species of this host-family

(Berto et al., 2009c, 2010c) (Tables 10, 11).

Host: Family Timaliidae Horsfield & Vigors

Isospora leiothrixi McQuistion, McAllister &

Buice, 1996 (Fig. 8b)

Type-host: Leiothrix lutea (Scopoli), Pekin robin.


Other locality: USA, Texas, Dallas, Dallas Count,

Dallas Zoo.

Remarks: Isospora leiothrixi was described from

birds housed at the Dallas Zoo, but is believed to have

originated from the Hawaiian Islands. To date, this is

the only Isospora species described from New World

timaliids (McQuistion et al., 1996) (Table 11).

Host: Family Turdidae Rafinesque

Isospora phaeornis Levine, Van Riper & Van

Riper, 1980 (Fig. 8c)

Type-host: Myadestes obscurus (Gmelin), omao.



described from New World turdids (Levine et al.,

1980) (Table 12).

Isospora robini McQuistion & Holmes, 1988

(Fig. 8d)

Type-host: Turdus migratorius (L.), American robin.

Type-locality: USA, Wildlife Rehabilitation Center

of Illinois.

Remarks: This coccidium was described from Amer-

ican robins captured in central Illinois. Despite the

similarity between I. robini and I. phaeornis, they can

be distinguished by the shape of the sporocyst and

Stieda and substieda bodies (McQuistion & Holmes,

1988) (Table 12).

Isospora tucuruiensis Lainson & Shaw, 1989

(Fig. 8e)

Type-host: Turdus albicollis (Vieillot), white-necked

thrush.

Type-locality: Brazil, State of the Para, Island of

Tocantins.

Remark: The oocysts of I. tucuruiensis are the

smallest among the Isospora species of the host-

family Turdidae in the New World (Lainson & Shaw,

1989) (Table 12).

Isospora albicollis Lainson & Shaw, 1989 (Fig. 8f)

Type-host: Turdus albicollis (Vieillot), white-necked

thrush.

Type-locality: Brazil, State of the Para, Island of

Tocantins.


Lainson & Shaw (1989) from T. albicollis. The

ooccysts of I. albicollis have a micropyle. This

Syst Parasitol (2011) 80:159–204 187

123

188 Syst Parasitol (2011) 80:159–204

123

feature is unique among the Isospora species from

turdids (Table 12).

Host: Family Zosteropidae Bonaparte

Isospora brayi Levine, Van Riper & Van Riper,

1980 (Fig. 8g)

Type-host: Zosterops japonicus (Temminck, Schle-

gel), Japanese white-eye.



described from New World zosteropids (Levine

et al., 1980; Upton et al., 1988) (Table 12).

Isospora manoaensis Upton, Marchiondo & Wil-

liams, 1988 (Fig. 8h)




Lyon Arboretum.

Remark: Isospora manoaensis differs from I. brayi

by virtue of its rounded sporocyst and the presence of

numerous splinter-like polar granules (Upton et al.,

1988) (Table 12).

Isospora mejiro Upton, Marchiondo & Williams,

1988 (Fig. 8i)




Lyon Arboretum.

Remarks: Isospora mejiro has a single (rarely two)

large polar granule, which is not present in the other

two coccidians recorded from this host-family (Upton

et al., 1988) (Table 12).

Discussion

Coccidia were among the first microorganisms

observed, as spherical forms in the bile of a rabbit,

by Antonie van Leeuwenhoek using a rudimentary

microscope in 1674. Nowadays, it is generally

accepted that those forms were in fact oocysts of

Eimeria stiedae (Lindemann, 1865) Kisskalt & Hart-

mann, 1907 (Wenyon, 1926; Duszynski et al., 1999).

Hake (1839) must have been the first scientist to

have viewed oocysts in greater detail; however, this

author regarded them as globules of pus. Kloss (1846)

observed coccidian parasites of a snail which were

subsequently named Klossia helicina Schneider,

1875. Almost 20 years later, Lindemann (1865),

studying oocysts in the bile of a rabbit, described

the species Monocystis stiedae Lindemann, 1865,

considering it to be a gregarine.

The first description of a coccidian in birds is

accredited to Rivolta (1869), who recovered coccidia

from fowls and other birds. Although this author had

noted the division of the contents of some oocysts

into two masses, these were neither distinguished nor

characterised, being described simply as Psorosper-

mium avium Rivolta, 1869. Indeed, Rivolta (1873)

and Rivolta & Silvestrini (1873) also referred to this

coccidium, considering all coccidia from birds as

belonging to this single taxon.

The asexual stage of the life-cycle of coccidia was

originally described by Eimer (1870) for a coccidium

found in mice. Five years later, Schneider (1875)

observed this same coccidium and proposed the

genus Eimeria, after Theodor Eimer, and named the

type-species E. falciformis Schneider, 1875.

In addition to his studies with birds, Rivolta

described coccidian parasites of frogs, calves and

dogs (Rivolta, 1878), establishing the genus Cyto-

spermium Rivolta, 1878; however, it is now recog-

nised that these parasites should have been included

within Eimeria.

Leuckart (1879), without prior knowledge of the

studies of Lindemann (1865), Eimer (1870) and

Schneider (1875), described coccidia encountered in

the bile of rabbits as Coccidium oviforme Leuckart,

1879. This species was subsequently considered a

synonym of E. stiedae.

Isospora was proposed by Schneider (1881) for

oocysts recovered from a slug. The species was


passerine birds: a. Isospora andesensis [adapted from Templar

et al. (2004)]; b. I. iridosornisi [adapted from Metzelaars et al.

(2005)]; c. I. tiesangui [adapted from Berto et al. (2008a)]; d. I.marambaiensis [adapted from Berto et al. (2008a)]; e. I.sepetibensis [adapted from Berto et al. (2008a)]; f. I. cadimi[adapted from Berto et al. (2009b)]; g. I. navarroi [adapted

from Berto et al. (2009b)]; h. I. ramphoceli [reproduced from

Zootaxa, 2650, 57–62 with permission]; i. I. sanhaci [adapted

from Berto et al. (2009c)]; j. I. sayacae [adapted from Berto

et al. (2009c)]. According to Templar et al. (2004), Metzelaars

et al. (2005), Berto et al. (2008a, 2009b,c, 2010b). Scale-bar:

10 lm

b

Syst Parasitol (2011) 80:159–204 189

123

Ta

ble

11

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body

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dim

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sili

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9

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(15–18

9

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(2009b,

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(19–24

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layer

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16.1

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(14–19

9

9–12)

flat

tened

smal

ldif

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mphoce

liR

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dors

ali

s(T

hra

upid

ae)

Ber

toet

al.

(2010b,c

)

sub-

spher

ical

23

.79

22.8

(22–26

9

21–24)

1.0 (1

.0–1

.1)

bi-

layer

ed,

c.1.1

abse

nt

elli

pso

idal

or

ovoid

16.0

911.4

(14–18

9

10–13)

knob-l

ike

larg

e,

hom

ogen

eous

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fuse

I.sa

nhaci

Thra

upis

saya

ca(T

hra

upid

ae)

Ber

toet

al.

(2009c,

2010c)

sub-

spher

ical

22

.19

21.0

(19–24

9

17–23)

1.1 (1

.0–1

.1)

bi-

layer

ed,

c.1.0

abse

nt

ovoid

17.0

99. 9

(15–19

9

9–11)

nip

ple

-

like

larg

e,

pro

min

ent

dif

fuse

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yaca

eT

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yaca

(Thra

upid

ae)

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toet

al.

(2009c,

2010c)

sub-

spher

ical

28

.99

27.4

(28–30

9

24–29)

1.1 (1

.0–1

.1)

bi-

layer

ed,

c.1.3

abse

nt

bott

le-

shap

ed

23.4

911.8

(23–25

9

11–12)

pro

min

ent

larg

edif

fuse

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lvaso

uza

iT

.sa

yaca

(Thra

upid

ae)

Ber

toet

al.

(2009c,

2010c)

sub-

spher

ical

25.5

922.6

(22–28

9

19–25)

1.1 (1

.0–1

.2)

bi-

layer

ed,

c.1.0

pre

sent

pyri

form

17.6

910.5

(17–18

9

10–11)

del

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esm

all

com

pac

t

I.le

ioth

rixi

Lei

oth

rix

lute

a(T

imal

iidae

)

McQ

uis

tion

etal

.

(1996)

elli

pso

idal

28

.09

16.6

(24–32

9

15–18)

1.5 (1

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layer

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910.3

(12–20

9

7–12)

nip

ple

-

like

pro

min

ent

com

pac

t

190 Syst Parasitol (2011) 80:159–204

123

Syst Parasitol (2011) 80:159–204 191

123

named as I. rara Schneider, 1881. The line drawings

and photomicrographs of the oocysts of this descrip-

tion were of low resolution; however, they demon-

strated the presence of only two sporocysts in each

oocyst, justifying the description of a new genus.

Rivolta & Delprato (1881) were the first to

mention specimens of Isospora from passerine birds.

These authors recovered oocysts from the faeces of

Sylvia atricapilla (L.), Erithacus rubecula (L.) and

Passer domesticus (L.). However, no species was

described or named.

Labbe (1893), without knowledge of the publica-

tion of Schneider (1881), erected Diplospora Labbe,

1893 for coccidian parasites of various birds. The

species were named D. lacazei Labbe, 1893 and

D. rivoltae Labbe, 1893. Subsequently, these species

were transferred to Isospora. Hosoda (1928) rede-

scribed I. lacazei from tree sparrows Passer mont-

anus (L.) in Japan. This identification was later

confirmed by Becker (1934). Boughton (1930),

Henry (1932), Boughton et al. (1938), Rysavy

(1954), Scholtyseck (1954), Levine & Mohan

(1960), Mandal (1965), Anwar (1966a,b), Mandal &

Bhattacharya (1969) and Hernandez-Rodriguez et al.

(1976a,b) all reported I. lacazei from different species

of fringillids and passerids. However, during this

same period, Schwalbach (1959), basing his analysis

on the morphology of the oocysts, described new

species of Isospora from wild birds in Germany.

With regard to the life-history, Anwar (1966b)

described meronts and gametes of I. lacazei from the

small intestine of Carduelis chloris (L.) in England.

Shortly thereafter, Box (1975) described the extrain-

testinal stages of I. serini when she isolated meronts

from mononuclear phagocytes derived from the blood

of Serinus canaria. Later, this species and more than

18 others, all with extra-intestinal life-cycles, were

redescribed and allocated to Atoxoplasma Garnham,

1950 by Levine (1982c). However, the validity of this

genus was questioned by Boulard et al. (1987) and,

more recently, by Carreno & Barta (1999), Schrenzel

et al. (2005), Barta et al. (2005) and Gill & Paperna

(2008).

In 1982, while searching for new combinations to

assist in the identification of coccidia from passerines,

Levine (1982a) suggested the names I. passeris for

parasites of Passer domesticus, and I. lacazei for

parasites of Carduelis carduelis (L.). Moreover, he

presented a list of 60 species of Isospora, each with

their respective hosts. In contrast, Grulet et al. (1982),

via a detailed study on the morphology of the

sporocysts, described 12 new species from P. domes-

ticus in France.

At present, descriptions of new species of coccidia

parasitising passerine birds are frequent. In an

attempt to organise this growing body of information,

Duszynski et al. (1999) assembled hundreds of

species into a database named ‘The Coccidia of the

World’.

Life-cycle

The pioneering studies by Tyzzer (1929) and Tyzzer

et al. (1932) on coccidiosis in poultry established the

conceptual basis of the biology of coccidia. In these

studies, the coccidia were considered homoxenous

parasites of the epithelial cells of the intestinal

mucosa. The described life-cycles were confirmed

in the reviews of Levine (1985) and Ball et al. (1989).

Traditionally, studies on Eimeria spp. in passerines

were limited to descriptions of oocysts. Therefore,

there is a dearth of information in relation to the life-

cycles of Eimeria spp. in passerines (Yakimoff &

Gousseff, 1938; Chakravarty & Kar, 1944; Cerna,

1976; Varghese, 1977; Haldar et al., 1982; Dzerz-

hinskii & Kairullaev, 1989; Berto et al., 2008c,

2009d). Considering other avian orders, it is recog-

nised that the majority of species of Eimeria have

intestinal cycles (Levine, 1985; Ball et al., 1989).

However, there are some exceptions, including those

observed in: E. reichenowi Yakimoff & Matschoulsky,

1935, parasites of the cranes Grus canadensis (L.)

and G. americana (L.); and E. truncata (Railliet &


passerine birds: a. Isospora silvasouzai [adapted from Berto

et al. (2009c)]; b. I. leiothrixi [reproduced from ActaProtozoologica, 35, 73–75 with permission]; c. I. phaeornis[reproduced from Journal of Protozoology, 27, 258–259 with

permission]; d. I. robini [reproduced from Proceedings of theHelminthological Society of Washington, 55, 324–325 with

permission]; e. I. tucuruiensis [adapted from Lainson & Shaw

(1989)]; f. I. albicollis [adapted from Lainson & Shaw (1989)];

g. I. brayi [reproduced from Journal of Protozoology, 27, 258–

259 with permission]; h. I. manoaensis [reproduced from

Systematic Parasitology, 12, 81–85 with permission]; i.

I. mejiro [reproduced from Systematic Parasitology, 12,

81–85 with permission]. According to Levine et al. (1980),

McQuistion & Holmes (1988), Upton et al. (1988), Lainson &

Shaw (1989), McQuistion et al. (1996), Berto et al. (2009c).

Scale-bar: 10 lm

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192 Syst Parasitol (2011) 80:159–204

123

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Syst Parasitol (2011) 80:159–204 193

123

Lucet, 1891) Waiselewski, 1904 which parasitises

geese of the genera Anser (Brisson) and Branta

(Scopoli). The former species can cause systemic

disease after crossing the intestinal mucosa by

invading the underlying tissues and muscular layer,

then developing asexually and sexually within organs

such as the liver, spleen, heart and lungs. The oocysts

are later shed from the lungs and ascend into the

pharynx, where they are swallowed and then voided

with the faeces (Novilla et al., 1981; Augustine et al.,

2001). In the life-cycle of E. truncata, the sporozoites

migrate to the kidneys and develop into meronts and

gametocytes in the epithelial cells of the renal tubules

(Entzeroth et al., 1981).

In contrast to Eimeria, the life-cycles of various

Isospora species in passerines have been reported in

detail during in the last four decades. Prior to 1966,

only the intestinal cycle had been recognised; however,

after the pioneering studies of Box (1966, 1967, 1970,

1975, 1977, 1981) and those of Levine (1982c), the

existence of an extra-intestinal cycle was confirmed.

The possibility of an extra-intestinal cycle was

strongly inferred based on the proposed association

between intestinal coccidiosis and forms similar to

sporozoites which had been observed in the spleen of

sparrows Passer domesticus and in the liver of

canaries Serinus canaria (see Box, 1966, 1967).

Subsequent experimental observations suggested that

the species of Atoxoplasma, described by Garnham

(1950) parasitising macrophages of canaries, more

likely represent extra-intestinal stages of Isospora

(see Box, 1970). Previously, in unrelated studies,

Lainson (1958, 1959, 1960) had reported the presence

of the parasite, allocated to Lankesterella Labbe,

1899, from gametocytes obtained from the viscera of

sparrows, noting that transmission occurred via the

mite Dermanyssus gallinae De Geer. Box (1975,

1977, 1981) subsequently confirmed that species

referred to as Atoxoplasma and Lankesterella, from

canaries and sparrows, could not be transmitted either

via blood transfusion or mites, but only by the

ingestion of Isospora oocysts. Thus, Dr Edith D. Box

is credited with having associated extra-intestinal

merogony with Isospora infection.

It should be noted that the parasite which demon-

strated the capacity to cross the intestinal barrier and

infect other tissues was recognised as I. serini, and

that this should be distinguished from I. canaria

which maintains a strictly intestinal life-cycle (Box,

1975, 1977, 1981). This species develops in the

intestinal epithelium and has prepatent and patent

periods of four to five days and two to three weeks,

respectively. In comparison, the sporozoites of I. se-

rini penetrate into macrophages within the lamina

propria of the small intestine and are transported to

various organs, including the liver, spleen and lungs,

where five merogonies into phagocytes take place.

Following this process, I. serini returns to the intestine

in one of two ways, i.e. merozoites can penetrate

directly into intestinal mucosa, or, alternatively,

following the accumulation of merozoites in the

lungs, they can migrate into the digestive tract via the

pharynx and trachea. Within the intestine, new

merogonies, gametogonies and the shedding of the

oocysts take place (Box, 1977, 1981). The patent

period of the extra-intestinal cycle contrasts with the

self-limiting nature of the intestinal cycle, because the

low release of the parasite from macrophages pro-

motes a chronic infection (Box, 1981). Furthermore,

Milde (1979) suggested that the extra-intestinal forms

most likely act as reservoirs, allowing the return of

coccidia to the intestine after the intial infection.

Following a re-evaluation of Atoxoplasma, Levine

(1982c) listed 19 species, including a new combina-

tion for I. serini as A. serini (Aragao, 1933) Levine,

1982. However Box (1966, 1967, 1970, 1975, 1977,

1981) had previously provided compelling evidence

that the forms observed in leukocytes in the viscera of

passerines were in fact developmental phases of

Isospora. Thus, as such forms do not belong to a

distinct species, the recognition of Atoxoplasma and

Lankesterella could not be justified. This assertion

was supported by the work of Boulard et al. (1987),

Upton et al. (2001) and Gill & Paperna (2008).

Finally, Carreno & Barta (1999), Schrenzel et al.

(2005) and Barta et al. (2005), using a combination of

morphological and molecular studies, confirmed that

species of Isospora and Atoxoplasma are closely

related and that these genera are synonyms.

Dynamics of shedding of the oocysts of Isospora

in passerines

Grulet et al. (1982) described 12 species of Isospora

based upon a detailed examination of the morphology

of the oocysts and some aspects of the life-cycles.

Additional observations on the biology of these

species indicated that their development followed a

194 Syst Parasitol (2011) 80:159–204

123

circadian rhythm, which, during the summer, resulted

in abundant shedding of the oocysts during the last

hours of the afternoon (Grulet et al., 1986a,b,c). As a

result of these studies, three life-cycle patterns were

proposed.

The first pattern has a prepatent period of four to

five days and a patent period of 12 days. This life-

cycle is limited to the villi of the intestinal epithelium

and was considered similar to that described for

I. canaria. The second pattern results in a chronic

infection and is also limited to the intestine. In this

life-cycle, the gametogony occurs each night, in the

intestinal villi, via merozoites which developed in the

crypts of Lieberkuhn. Finally, the third pattern also

tends to result in a chronic infection due to intense

merogony and gametogony within the intestine

throughout the entire 24 hour period, with merozoites

developing from monocytic-phagocytic complexes.

This third life-cycle is similar to that previously

described by Box (1981) for I. serini (see Grulet

et al., 1986a,b,c).

In the last decade, Brawner & Hill (1999), Dolnik

(1999), Hudman et al. (2000), McQuistion (2000) and

Brown et al. (2001) have confirmed the presence of a

circadian rhythm, which had previously been sug-

gested by Grulet et al. (1986a,b,c). Misof (2004) also

noted a daily fluctuation in the shedding of oocysts in

blackbirds Turdus merula (L.), where both juveniles

and adults shed oocysts predominantly in the late

afternoon. Lopez et al. (2007) affirmed that any study

of the prevalence of coccidia in passerines should be

delineated by taking into consideration the circadian

rhythm of these parasites.

Dolnik (1999), McQuistion (2000), Misof (2004)

and Martinaud et al. (2009) proposed two hypotheses

to explain the dynamics of the shedding of Isospora

oocysts in passeriforms. Firstly, the period of shed-

ding of the oocysts could correspond to a peak in the

feeding activity of the host. As many individuals

share the same feeding patch, it is assumed that

oocysts released in the feeding area will have a higher

probability of transmission after sporulation. How-

ever, it should be considered that, in the humidity of

the tropics, it is possible that the oocysts may be

washed away before sporulation can occur. An

additional weakness in this hypothesis is that, for

many passerine birds, two peaks of feeding activity

are recognised, one in the morning and the other in

the afternoon.

The second hypothesis is based on the resistance

of oocysts to environmental factors, such as temper-

ature and humidity. It is well recognised that

desiccation can reduce the infectivity of oocysts.

Thus, the shedding of the oocysts in the late

afternoon, when temperatures are lower and humidity

levels are higher, could represent an adaptation to

prevent desiccation under natural conditions (Dolnik,

1999; McQuistion, 2000; Misof, 2004; Martinaud

et al., 2009). This hypothesis has recently been tested

using oocysts of I. turdi Schwalbach, 1959, a parasite

of Turdus merula L. (Martinaud et al., 2009). It was

observed that the exposure of the faeces to natural

sunlight reduced the infectivity of the oocysts. These

findings strongly indicated that the shedding of the

oocysts in the late afternoon is indeed an adaptative

trait to protect against the effects of desiccation and

ultraviolet radiation and which results in the reduced

mortality of oocysts in the environment (Martinaud

et al., 2009).

Host-specificity

Prior to 1982, more than 100 species of passerines

had been reported as hosts of I. lacazei. Yet, based on

available descriptions and on the improbability that a

single species could parasitise so many hosts, Levine

(1982a) proposed that each species of bird would

more likely be parasitised by a different species of

Isospora, but that, in some cases, a single species

could possibly parasitise birds of the same genus. In

this sense, the concept of host-specificity in passe-

rines would be genus-specific.

In the case of Eimeira, according to Marquardt

(1981), there is a high degree of host-specificity.

According to this author, closely related species

could host a single species of coccidian; however,

there would also be a remote possibility of cross-

transmission between different genera and families of

birds.

During the past two decades, the descriptions of

coccidia have generally been made in accordance with

the guidelines proposed by Duszynski & Wilber

(1997). These authors put forward the concept of

intra-familial specificity when they suggested that a

new coccidian species should be compared in detail

with the coccidian species that is most structurally

similar to it within the same host family. However,

Tung et al. (2007) considered that this concept should

Syst Parasitol (2011) 80:159–204 195

123

be genus-specific based on data from studies of

experimental infection. In these experiments, oocysts

of I. michaelbakeri Grulet, Landau & Baccam, 1982, a

parasite of the sparrow Passer rutilans (Temminck),

were used to inoculate their natural host and the

following birds: the estrildids passerines Lonchura

punctulata (L.) and Padda oryzivora (L.); the fringil-

lid passerine Serinus canaria; the galliform Gallus

gallus (L.); and the anseriform Anas platyrhynchos

(L.). In support of the genus-specific concept, only the

sparrow P. rutilans developed an infection (Tung

et al., 2007).

In contrast, Berto et al. (2010a, 2011b) provided

support for the family-specific concept when they

reported the description of two new hosts for

I. tiesangui, I. sepetibensis and I. navarroi, which

had been recognised as parasites of Ramphocelus

bresilius dorsalis. The new hosts were the palm

tanager Thraupis palmarum (I. tiesangui and

I. navarroi) and the blue dacnis Dacnis cayana

(I. tiesangui and I. sepetibensis), which inhabit the

same biotope as R. b. dorsalis on Marambaia Island.

Consequently, three passerines of the same family,

but distinct genera, were shown to be hosts of the

same coccidian species.

It is worth mentioning that not all studies follow the

guidelines proposed by Duszynski & Wilber (1997). In

this context, two new species of Isospora were recently

described without comparative studies of coccidian

parasites of birds of the same family. Thus, Dolnik &

Loonen (2007) described I. plectrophenaxia Dolnik &

Loonen, 2007, parasitising Plectrophenax nivalis (L.),

by comparing it only with the descriptions of other

coccidia found in this same host genus. Using a similar

experimental approach, the species I. hypoleucae

Dolnik, Ronn & Bensch, 2009 was described from

Ficedula hypoleuca (Pallas) (Dolnik et al., 2009b).

Morphology and diagnosis

The features of the oocyst are commonly used for the

differentiation and identification of Eimeria spp.,

because many species present oocyst walls which are

readily distinguishable, with rough surfaces, spines,

micropyle, micropyle cap, residuum and polar gran-

ules (Casas et al., 1995; Arslan et al., 2002). In

contrast, the Isospora spp. commonly have uniform

oocyst walls, and consequently it is necessary to

observe additional features in order to achieve a

confident identification (Grulet et al., 1982; Berto

et al., 2008a, 2009a,b,c, 2010c, 2011a,b).

The numerous species of Isospora which can

parasitise sparrows, as described by Grulet et al.

(1982), clearly demonstrate the importance of the

structures and features of the sporocysts, particularly

the Stieda and substieda bodies, in identification.

Currently, the sporocysts of new species are

described in minute detail in order to achieve a

definitive identification (Balthazar et al., 2009b;

Berto et al., 2009b,c,d,e,f, 2010b, 2011a,b; Pereira

et al., 2011).

In addition to simple microscopical examination,

histological methods that reveal details of the biology

of coccidia (Abd-Al-Aal et al., 2000) and molecular

methods are highly relevant to both the systematics

and the diagnosis of coccidian parasites, including

those of the Passeriformes (Dolnik et al., 2009a,b;

McQuistion et al., 2010; Schrenzel et al., 2005),

because they may serve to complement data generated

from the morphological examination of sporulated

oocysts. In this context, cases of recent divergence,

such as among species and strains of coccidia, may

not be supported by any morphological variation

whatsoever, but can often be readily detected using

molecular characters (Tenter et al., 2002).

Future studies on coccidia of New World

passerine birds

A number of coccidia have been described in

passerines which inhabit geographically remote areas

and have thus remained isolated. However, the

majority of the passerine hosts demonstrate a wide

geographical distribution. As such, for the study of

the coccidian parasites of New World passerine birds,

the species of coccidia described from birds that

inhabit North, Central and South America are highly

relevant, given that transmission of parasites can

occur between sympatric birds of the same family.

On the other hand, transmission between non-sym-

patric species that inhabit distant continents is

unlikely (Levine et al., 1980; Duszynski & Wilber,

1997; Duszynski et al., 1999; Carvalho-Filho et al.,

2005; Berto et al., 2010c).

Studies aimed at providing descriptions of new

species should be conducted through the detailed

characterisation of the oocysts. Statistical evaluations

can be performed targeting the morphometrics of the

196 Syst Parasitol (2011) 80:159–204

123

oocysts of a taxon in comparison with those of other

species. Three statistical methods are commonly

performed: (1) histograms plot the values of length,

width and the shape-index of the oocysts, along with

their frequencies; this method demonstrates tenden-

cies and regularities in the distribution of the

dimensions (Berto et al., 2008e,f,g, 2011b); (2)

analysis of variance (ANOVA), Student’s t-test or

other parametric tests should be used to compare

measurements of length, width and shape-index of

the oocysts and sporocysts in two situations: firstly,

comparing species recovered from the host-family

and, secondly, comparing the same species recovered

from different host-species (Gomez et al., 1982;

Berto et al., 2008e,f,g, 2011b); and (3) linear

regression analyses plot measurements of width on

length of oocysts; when different host-species shed

oocysts, regressions can be performed for each host

individual and later plots from several hosts can be

superimposed for a better visualisation (Norton &

Joyner, 1981; Berto et al., 2008e,f,g, 2011b). The

application of these types of morphometric

approaches to the coccidia recorded in tanagers from

Marambaia Island revealed trends, patterns, regular-

ities and, more importantly, which species can or

cannot be reliably identified by morphometry and

how (Berto et al., 2011b).

In addition, when possible, studies should examine

all of the developmental phases of species of

Isospora, including merogony, gametogony and spo-

rogony, for the purposes of establishing the sites of

infection and the determination of life-cycles. The

determination of the number of oocysts per gram of

faeces should reveal the intensity of infection, the

duration of the patent period, fluctuations in the

shedding of the oocysts, the number of merogonies

and, therefore, life-cycle patterns (Box, 1977, 1981;

Cardozo et al., 2010). Those species with an extra-

intestinal cycle should be attributed to Isospora,

because Atoxoplasma is considered invalid (Carreno

& Barta, 1999; Barta et al., 2005; Schrenzel et al.,

2005). Invariably, these studies must be conducted

following the death of the passerine host, followed by

necropsy and histological methods. Yet the killing of

wild birds, even for scientific studies, is prohibited in

some countries, including Brazil, where the native

birds are protected by law. As such, molecular

methods that require only small quantities of parasi-

tised cells or tissues, and which may possibly be

collected non-lethally, will most likely play an

increasingly important role in future studies on the

distribution and identification of coccidia in passerine

birds.

It is becoming increasingly clear that molecular

phylogenetic studies need to be conducted on cocci-

dia from passerines, with the principal objectives of

clarifying the position of Isospora and Eimeira

among other parasite groups, revealing inter- and

intra-specific differences, and to resolve taxonomic

discrepencies. DNA sequencing provides another

marker for the investigation of phylogenetic relation-

ships for taxa that cannot unequivocally be classified

based on phenotypic markers, and may provide

solutions to problems of species identity and host-

specificity which cannot be resolved using traditional

approaches. Molecular data have been increasingly

used over the past three decades to infer phylogenetic

relationships between various protozoa, including

eimeriid coccidians (Barta 2001, Schrenzel et al.,

2005, Dolnik et al., 2010), although the number of

studies focused on the coccidia of passerines has been

very limited (Dolnik et al., 2009b; McQuistion et al.,

2010). In an evolutionary sense, molecular characters

can be reasonably assumed to be homologous and

should also provide sufficient variability to generate

character states for analysis. Early molecular studies

of the eimeriid coccidian, for the purpose of inferring

relationships between a variety of taxa, relied almost

exclusively on ribosomal RNA gene sequences and

generated findings which largely supported the major

groupings of taxa recognised using morphological

and life-cycle traits (Barta, 2001). Yet, comparative

analysis of a single molecular sequence, such as that

of the 18S rRNA gene, represents only the phylogeny

of that one gene, which may or may not represent the

phylogeny of the coccidia. Hence, in order to

unequivocally resolve relationships between closely

related species, it is now considered both necessary

and desirable to use multiple sequences from differ-

ent genes, with the choice of genes preferentially

including sequences from both nuclear and non-

nuclear (e.g. mitochondrial) genomes (Barta, 2001).

Moreover, it is recognised that, in order to be

of value, there needs to be concordance between

the phylogenies derived from different molecular

sequences.

The study of Schrenzel et al. (2005), applying

a multi-gene strategy to the characterisation of

Syst Parasitol (2011) 80:159–204 197

123

isosporian pathogens of passerine birds clearly dem-

onstrated the potential of molecular methods for

resolving taxonomic inconsistencies and assessing

host-specificity, and also serve as an example of how

future studies on coccidians of New World passerines

could be developed. Sequences obtained by polymer-

ase chain reaction (PCR) based amplification of

regions of the large and small subunit ribosomal RNA

genes of isosporian coccidians, present in the faeces or

tissues, were collected from a total of 59 birds

representing 23 species. Additional sequences derived

from the heat shock protein 70 (hsp70) gene, apicop-

last rRNA and chromosomal 5.8 s were derived from

a subset of the samples. The molecular date revealed

that the isosporian coccidia were monophyletic and

related to Eimeria (Eimeriidae). In addition, they

demonstrated a significant parasite diversity within

individual birds and within groups of birds of the

same species. Interestingly, they also provided evi-

dence suggesting that some of the passerine isospo-

rian coccidians might have low levels of host-fidelity.

The purpose of that study was not to compare

molecular methods with the traditional morphology-

based approach and, as such, no detailed analysis of

morphological characteristics was performed. Clearly,

the lack of such morphological data could be viewed

as a shortcoming and highlights the necessity for a

multi-disciplinary approach to the systematics of

these parasites. We consider it unlikely that morpho-

logical or molecular criteria, when used in isolation,

will result in the establishment of a stable nomen-

clature which will aid communication and avoid

confusion among protozoologists and non-protozool-

ogists. In this context, there appear to have been only

a few attempts to combine molecular and phenotypic

characters for phylogenetic analyses of apicomplexan

protozoa. More intensive and systematic sampling of

the biological diversity found within both the cocci-

dian parasites of passerine birds and the phylum

Apicomplexa as a whole is required at both pheno-

typic and molecular levels (Tenter et al., 2002).

A futher issue for consideration in relation to

genetic studies of the passerine-associated protozoa is

the need to be able to work with a source of genetic

material derived from a single cell. Ideally, the same

individual cell would have been identified using

morphological criteria prior to the extraction of

nucleic acid for molecular analysis. This can be

particularly difficult to achieve when working with

faeces, and for this reason the majority of studies have

traditionally performed their analysis on pooled

nucleic acids, possibly derived from different parasite

species, recovered from faecal samples. However, a

recently reported method (Dolnik et al., 2009) for the

isolation of individual oocysts of Isospora from avian

faeces, followed by sequence analysis of amplicons

generated by the PCR amplification of fragments of

the mitochondrial genome, has great potential as a

means of improving our knowledge of the systematics,

host-specificity, population structure and identifica-

tion of coccidian parasites of passerine birds.

As a final point of interest, the identification of

passerine coccidia can potentially form part of a

classification system for the allocation of bird species

to their correct families, or provide evidence in

support of existing classifications. As an example, the

Coerebidae comprises a single species, Coereba

flaveola; however this family is closely related to

both the Thraupidae and the Emberizidae (Burns

et al., 2003; IUCN, 2011). A recent study examining

birds on Marambaia Island reported the presence of

Isospora cagasebi and I. coerebae in specimens of

C. flaveola, but not in thraupids or emberezids,

despite the fact that these families inhabited the same

biotope. The limited distribution of these coccidian

species provides support for the current classification

of C. flaveola in its own family, since coccidia from

coerebids have not yet been reported in thraupids or

emberezids (Berto et al., 2011a,b). In this sense, in a

first description from a host-family, it appears relevant

that the new coccidium be compared with those

coccidia in other host-families of the same parvorder,

or with those that are morphologically and phyloge-

netically similar (Berto et al., 2008b, 2009d,e,f). The

finding of the same coccidium in two closely related

host-families may suggest the need for a reclassifica-

tion of those two families as one.

It is our hope that this review of the coccidia of New

World passerine birds will serve as a useful tool for

differential diagnosis as well as for the identification of

individual species. Avian systematics has recently

undergone a reorganisation (Cicero & Johnson, 2001;

Birdsley, 2002; Burns et al., 2003; IUCN, 2011) and,

in view of this, the present review was aimed at

clearly elucidating the host-family relationship of

each coccidian and reorganising the species according

to the guidelines proposed by Duszynski & Wilber

(1997). At the same time, we vigorously encourage

198 Syst Parasitol (2011) 80:159–204

123

parasitologists to consult the original papers, com-

piled herein for the first time, that describe each of the

species in order to study the photosyntypes, symbio-

types, deposited material and other detailed informa-

tion which was beyond the scope of the current

review.

Acknowledgements We thank the late Dr Steve J. Upton,

Division of Biology, Kansas State University, USA for his help

through the generous provision of access to scientific

publications unavailable in Brazil. In addition, we thank the

following editors and journals for allowing us to reproduce the

drawing of the oocysts: Dr David I. Gibson (Systematic Parasi-tology); Dr Krzysztof Wiackowski (Acta Protozoologica); Dr

Gerald W. Esch (Journal of Parasitology); Dr Portia Holt

(Journal of Eukaryotic Microbiology); Dr Sherman S. Hendrix

(Proceedings of the Helminthological Society of Washington);

Dr Richard S. Jones (Invertebrate Biology); and Dr Zhi-Qiang

Zhang (Zootaxa).

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Coccidia de Passeriformes da América