coccidia de passeriformes da américa
TRANSCRIPT
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
e-mail: [email protected]
D. McIntosh
e-mail: [email protected]
W. L. Teixeira-Filho
e-mail: [email protected]
C. W. G. Lopes
e-mail: [email protected]
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.
Type-locality: Ecuador, Provincia de Sucumbios,
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.
Type-locality: Ecuador, Provincia de Morona-Santi-
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.
Type-locality: Ecuador, Provincia de Morona-Santi-
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.
Type-locality: Ecuador, Provincia de Esmeraldas,
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.
Type-locality: Ecuador, Provincia de Sucumbios,
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.
Type-locality: Ecuador, Provincia de Esmeraldas,
c.20 road km NNW of Alto Tambo.
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 &
Lopes, 2009 (Fig. 2b)
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
123
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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.
Type-locality: Brazil, State of Rio de Janeiro, Mar-
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
Sh
ape
Mea
sure
men
ts(l
m)
Sti
eda
bo
dy
Su
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)
McQ
uis
tio
net
al.
(19
99
)
sub
-sp
her
ical
too
vo
id
23
.49
21
.3(1
8–
28
91
7–
24
)
1.1
(1.0
–1
.2)
bi-
lay
ered
pre
sen
to
vo
id1
5.4
99
.9(1
4–
17
98
–1
1)
nip
ple
-li
ke
smal
lco
mp
act
I.sa
git
tula
eH
ylo
ph
yla
xn
aev
ioid
esn
aev
ioid
es(T
ham
no
ph
ilid
ae)
McQ
uis
tio
n& C
app
arel
la(1
99
2a)
ov
oid
toel
lip
soid
al2
7.5
92
1.8
(25
–3
09
21
–2
4)
1.3
(1.2
–1
.4)
bi-
lay
ered
pre
sen
t,1
to3
sub
-sp
her
ical
too
vo
id
14
.89
12
.4(1
3–
16
91
2–
13
)
den
setr
ian
gu
lar
dif
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.
Type-locality: Ecuador, Provincia de Esmeraldas,
c.20 road km NNW of Alto Tambo.
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.
Type-locality: Ecuador, Provincia de Esmeraldas,
c.20 road km NNW of Alto Tambo.
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 &
Lopes, 2008 (Fig. 3a)
Type-host: Saltator similis (Lafresnaye d’Orbigny),
green-winged saltator.
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).
Fig. 2 Line drawings of coccidia recorded from New World
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
ble
3C
om
par
ativ
em
orp
ho
log
yo
fIs
osp
ora
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cord
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ne
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-sp
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ical
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idal
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eric
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nt,
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idae
)
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(20
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lip
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al2
8.3
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(26
–3
19
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–2
3)
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.2–
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)b
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c.1
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rese
nt,
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idal
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ated
19
.79
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nd
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Ta
ble
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om
par
ativ
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orp
ho
log
yo
fIs
osp
ora
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cord
edfr
om
New
Wo
rld
pas
seri
ne
bir
ds
of
the
infr
aord
erP
asse
ri,
par
vo
rder
Co
rvid
a
Cocc
idia
Host
Ref
eren
ceO
ocy
sts
Sporo
cyst
s
Shap
eM
easu
rem
ents
(lm
)
Shap
e
index
Wal
l(l
m)
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r
gra
nule
Shap
eM
easu
rem
ents
(lm
)
Sti
eda
body
Subst
ieda
body
Res
iduum
I.bra
chyr
hyn
chi
Corv
us
bra
chyr
hyn
chos
(Corv
idae
)
Wobes
ter
&
Caw
thorn
(1985)
sub-
spher
ical
20.4
918.9
(15–25
9
14–23)
1.1 (1
.0–1.3
)
c.1.0
pre
sent
alongad
a16.2
910.6
(14–20
9
8–13)
pre
sent
–dif
fuse
I.cy
anoco
raci
sC
yanoco
rax
chry
sops
(Corv
idae
)
Upto
net
al.
(1985)
sub-
spher
ical
28.7
926.8
(25–30
9
24–29)
1.1 (1
.0–1.1
)
bi-
layer
ed,
c.2.0
pre
sent,
1or
2
ovoid
19.3
911.4
(17–21
9
10–12)
pro
min
ent
hom
ogen
eous
com
pac
t
I.ca
loci
tta
Calo
citt
afo
rmosa
form
osa
(Corv
idae
)
Upto
net
al.
(1995a)
sub-
spher
ical
28.8
927.7
(26–31
9
25–29)
1.0 (1
.0–1.1
)
bi-
layer
ed,
c.2.0
pre
sent,
1to
3
ovoid
20.1
912.6
(19–22
9
11–14)
pre
sent
pre
sent
dif
fuse
I.sa
moaen
sis
Foule
haio
caru
ncu
latu
s(M
elip
hag
idae
)
Adam
czyk
etal
.
(2004)
ovoid
28.9
926.1
(25–32
9
23–30)
1.1 (1
.0–1.3
)
bi-
layer
edpre
sent,
1or
2
ovoid
17.1
910.9
(16–18
9
10–11)
larg
ere
tangula
rco
mpac
t
168 Syst Parasitol (2011) 80:159–204
123
Ta
ble
5C
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
t1
)
Co
ccid
iaH
ost
(s)
Ref
eren
ce(s
)sO
ocy
sts
Sp
oro
cyst
s
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ape
Mea
sure
men
ts
(lm
)
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ape
ind
ex
Wal
l(l
m)
Po
lar
gra
nu
le
Sh
ape
Mea
sure
men
ts
(lm
)
Sti
eda
bo
dy
Su
bst
ied
a
bo
dy
Res
idu
um
I.va
nrip
eror
umC
ard
ina
lis
card
ina
lis
(Car
din
alid
ae);
Sa
lta
tor
sim
ilis
(Car
din
alid
ae)
Lev
ine
etal
.
(19
80);
Lo
pes
etal
.
(20
07)
sub
-sp
her
ical
24
92
3
(22
–2
69
20
–2
5)
–o
ne- lay
ered
,
c.0
.8
pre
sen
to
vo
id1
69
10
(15
–1
79
10
)
kn
ob
-lik
ein
dis
tin
ctco
mp
act
I.p
ityl
iS
.g
ross
us
satu
ratu
s(C
ard
inal
idae
)
McQ
uis
tio
n
& Cap
par
ella
(19
92
)
sub
-sp
her
ical
20
.19
18
.8
(20
–2
19
17
–2
0)
1.1 (1
.0–
1.2
)
bi-
lay
ered
,
c.1
.5
abse
nt
ov
oid
14
.79
9.4
(12
–1
79
8–
11
)
nip
ple
-
lik
e
abse
nt
com
pac
t
I.fo
rma
rum
S.
g.
gro
ssu
s(C
ard
inal
idae
);
S.
g.
satu
ratu
s(C
ard
inal
idae
)
McQ
uis
tio
n
& Cap
par
ella
(19
92
)
sub
-sp
her
ical
24
.69
23
.5
(21
–2
79
20
–2
5)
1.0 (1
.0–
1.1
)
bi-
lay
ered
,
c.1
.5
abse
nt
ov
oid
15
.79
11
.3
(14
–1
79
10
–1
3)
smal
l,
nip
ple
-
lik
e
larg
e,
tria
ng
ula
r
or
con
ical
com
pac
t
I.sa
lta
tori
S.
sim
ilis
(Car
din
alid
ae)
Ber
toet
al.
(20
08
d)
sub
-sp
her
ical
18
.39
17
.9
(17
–2
09
16
–2
0)
1.0 (1
.0–
1.1
)
bi-
lay
ered
,
c.1
.1
abse
nt
ov
oid
13
.49
8.9
(12
–1
59
8–
10
)
smal
l,
flat
ten
ed
smal
lco
mp
act
I.tr
inca
ferr
iS
.si
mil
is(C
ard
inal
idae
)
Ber
toet
al.
(20
08
d)
sub
-sp
her
ical
26
.29
23
.6
(24
–2
99
22
–2
5)
1.1 (1
.0–
1.2
)
bi-
lay
ered
,
c.1
.2
pre
sen
to
vo
id1
7.5
91
1.5
(17
–1
89
10
–1
3)
bu
bb
le-
shap
ed
pro
min
ent
dif
fuse
I.ca
ga
seb
iC
oer
eba
fla
veo
la(C
oer
ebid
ae)
Ber
toet
al.
(20
08
b,
20
11
a)
sub
-sp
her
ical
24
.99
24
.5
(23
–2
69
23
–2
5)
1.0
bi-
lay
ered
,
c.1
.4
abse
nt
ov
oid
18
.79
11
.5
(18
–1
99
10
–1
2)
kn
ob
-lik
ep
rom
inen
td
iffu
se
I.co
ereb
ae
C.
fla
veo
la(C
oer
ebid
ae)
Ber
toet
al.
(20
11
a)
sub
-sp
her
ical
24
.89
23
.3
(23
–2
79
21
–2
6)
1.1 (1
.0–
1.1
)
bi-
lay
ered
,
c.1
.2
abse
nt
ov
oid
17
.99
10
.9
(17
–1
99
10
–1
2)
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 &
Lopes, 2008 (Fig. 3b)
Type-host: Saltator similis (Lafresnaye d’Orbigny),
green-winged saltator.
Type-locality: Brazil, State of the Rio de Janeiro,
Teresopolis City (22�250S, 42�590W).
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.
Type-locality: Brazil, State of the Rio de Janeiro,
Marambaia Island (23�040S, 43�530W).
Remark: This was the first description from New
World coerebids (Berto et al., 2008b) (Table 5).
Isospora coerebae Berto, Flausino, Luz, Ferreira
& Lopes, 2010 (Fig. 3d)
Type-host: Coereba flaveola (L.), bananaquit.
Type-locality: Brazil, State of the Rio de Janeiro,
Marambaia Island (23�040S, 43�530W).
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)
Type-host: Camarhynchus parvulus (Gould), small
tree-finch.
Type-locality: Galapagos archipelago, Isabela Island,
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)
Type-host: Camarhynchus parvulus (Gould), small
tree-finch.
Type-locality: Galapagos archipelago, Isabela Island,
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
Fig. 3 Line drawings of coccidia recorded from New World
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)
Type-host: Camarhynchus parvulus (Gould), small
tree-finch.
Type-locality: Galapagos archipelago, Isabela Island,
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.
Type-locality: Brazil, State of the Rio de Janeiro,
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)
Type-host: Sporophila caerulescens (Vieillot), dou-
ble-collared seedeater.
Type-locality: Brazil, State of the Rio de Janeiro,
Seropedica City (22�43023.7900S, 43�42036.9400W).
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)
Type-host: Sporophila caerulescens (Vieillot), dou-
ble-collared seedeater.
Type-locality: Brazil, State of the Rio de Janeiro,
Seropedica City (22�43023.7900S, 43�42036.9400W).
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)
Type-host: Oryzoborus angolensis (L.), lesser seed-
finch.
Type-locality: Brazil, State of the Mato Grosso do
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)
Type-host: Oryzoborus angolensis (L.), lesser seed-
finch.
Type-locality: Brazil, State of the Mato Grosso do
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.
Type-locality: Brazil, State of the Rio de Janeiro,
Teresopolis City (22�250S, 42�590W).
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)
Type-host: Sporophila frontalis (Verreaux), buffy-
fronted seedeater.
Type-locality: Brazil, State of the Rio de Janeiro,
Teresopolis City (22�250S, 42�590W).
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)
Type-host: Sporophila frontalis (Verreaux), buffy-
fronted seedeater.
Other host: Sporophila schistacea (Lawrence), slate-
coloured seedeater.
Type-locality: Brazil, State of the Rio de Janeiro,
Teresopolis City (22�250S, 42�590W).
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.
Type-locality: Brazil, State of the Rio de Janeiro,
Teresopolis City (22�250S, 42�590W).
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.
Type-locality: USA, Hawaii.
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.
Type-locality: USA, Hawaii.
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.
Remark: This was the first description from New
World icterid birds (Pellerdy, 1967) (Table 9).
Isospora cacici Lainson, 1994 (Fig. 6a)
Type-host: Cacicus cela cela (L.), yellow-rumped
cacique.
Fig. 5 Line drawings of coccidia recorded from New World
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
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
t4
)
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.iv
ensa
eL
onch
ura
punct
ula
ta(E
stri
ldid
ae)
Lev
ine
etal
.
(1980)
sub-
spher
ical
26
925
–one-
layer
ed,
c.0.6
pre
sent
ovoid
18
912
(18
9
11–12)
pre
sent
abse
nt
dif
fuse
I.ly
onen
sis
L.
punct
ula
ta(E
stri
ldid
ae)
Upto
net
al.
(1988)
sub-
spher
ical
24
923
(21–27
9
21–27)
1.0 (1
.0–1.1
)
bi-
layer
ed,
c.1.5
pre
sent
ovoid
17.5
911.5
(16–21
9
10–12)
pre
sent
larg
e,
hom
ogen
eous
dif
fuse
I.ca
nari
aSer
inus
canari
a(F
ringil
lidae
)
Box
(1975
)su
b-
spher
ical
to elli
pso
idal
24.6
921.8
(17–30
9
17–30)
1.1 (1
.0–1.2
)
one-
layer
ed,
c.1.0
pre
sent
lem
on-
shap
ed
18.1
911.5
(17–22
9
10–13)
nip
ple
-
like
pre
sent
com
pac
t
I.se
rini
S.
canari
a(F
ringil
lidae
)
Box
(1975
)su
b-
spher
ical
20.1
919.2
(13–23
9
13–23)
1.0 (1
.0–1.1
)
one-
layer
ed,
c.1.0
pre
sent
elli
pso
idal
15.2
99.4
(13–16
9
8–11)
pro
min
ent
bar
ely
dis
cern
ible
dif
fuse
or
com
pac
t
I.la
caze
iC
ard
uel
isca
rduel
is(F
ringil
lidae
);C
.ch
lori
s(F
ringil
lidae
);F
ringil
laco
eleb
s(F
ringil
lidae
)
Anw
ar
(1966b);
Her
nan
dez
-
Rodri
guez
etal
.
(1976a,
b)
sub-
spher
ical
26.8
924.5
(20–34
9
18–30)
1.1 (1
.0–1.5
)
bi-
layer
ed,
c.1.0
pre
sent,
1or
2
pyri
form
(15–199
9–12)
pre
sent
pre
sent
dif
fuse
or
com
pac
t
I.lo
xopis
Hem
ignath
us
vire
ns
(Fri
ngil
lidae
)
Lev
ine
etal
.
(1980)
sub-
spher
ical
26
923
(25–26
9
22–25)
–bi-
layer
ed,
c.0.8
abse
nt
ovoid
16
913
(16–17
9
12–13)
knob-l
ike
abse
nt
dif
fuse
I.atr
ata
C.
atr
ata
(Fri
ngil
lidae
)
Ross
iet
al.
(1996)
sub-
spher
ical
21
920.3
(19–24
9
18–22)
1.0 (1
.0–1.1
)
bi-
layer
ed,
c.1.2
pre
sent,
1or
2
elli
pso
idal
18.8
910.3
(17–19
9
9–11)
del
icat
etr
apez
oid
al
wit
hli
nea
r
bas
is
dif
fuse
or
com
pac
t
I.gry
phoni
C.
tris
tis
(Fri
ngil
lidae
)
Ols
on
etal
.
(1998)
sub-
spher
ical
30.7
929.2
(28–34
9
25–33)
1.0 (1
.0–1.1
)
bi-
layer
edpre
sent,
2to
4
ovoid
22.2
913.4
(15–25
9
12–15)
smal
lin
dis
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.
Type-locality: Brazil, State of Rio de Janeiro, Mar-
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.
Type-locality: Brazil, State of the Rio de Janeiro,
Marambaia Island (23�040S, 43�530W).
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)
Type-host: Ramphocelus bresilius dorsalis (Sclater),
Brazilian tanager.
Type-locality: Brazil, State of the Rio de Janeiro,
Marambaia Island (23�040S, 43�530W).
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)
Type-host: Ramphocelus bresilius dorsalis (Sclater),
Brazilian tanager.
Other host: Dacnis cayana (L.), blue dacnis.
Type-locality: Brazil, State of the Rio de Janeiro,
Marambaia Island (23�040S, 43�530W).
Remarks: This was the third species described from
R. b. dorsalis on Marambaia Island. Thereafter, Berto
Fig. 6 Line drawings of coccidia recorded from New World
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
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
t5
)
Cocc
idia
Host
Ref
eren
ceO
ocy
sts
Sporo
cyst
s
Shap
eM
easu
rem
ents
(lm
)
Shap
ein
dex
Wal
l(l
m)
Pola
rgra
nule
Shap
eM
easu
rem
ents
(lm
)
Sti
eda
body
Subst
ieda
body
Res
iduum
I.pet
roch
elid
on
Pet
roch
elid
on
pyr
rhonota
(Hir
undin
idae
)
Sta
ble
r&
Kit
zmil
ler
(1972
)
elli
pso
idal
toovoid
25.2
922.2
(23–30
9
19–25)
–one- la
yer
ed,
c.1.0
pre
sent
lem
on-
shap
ed
18.4
910.8
(16–22
9
10–12)
pro
min
ent
elli
pso
idal
com
pac
t
I.div
itis
Div
es
atr
ovi
ola
ceus
(Ict
erid
ae)
Pel
lerd
y
(1967
)
sub-
spher
ical
(22–30
9
20–28)
––
abse
nt
elongat
ed17
913
consp
icuous
–dif
fuse
I.ca
cici
Caci
cus
cela
cela
(Ict
erid
ae)
Lai
nso
n
(1994
)
sub-
spher
ical
26.5
923.7
(22–28
9
20–26)
1.1 (1
.0–1.2
)
one- la
yer
ed,
c.1.5
pre
sent,
1or
2
elli
pso
idal
17.7
912.5
(17–19
9
11–14)
pro
min
ent,
stopper
-
shap
ed
pro
min
ent
com
pac
t
I.bel
lico
saStu
rnel
la
bel
lico
sa
(Ict
erid
ae)
Upto
net
al.
(1995b
)
elli
pso
idal
,
ovoid
or
oblo
ng
29.4
923.5
(26–32
9
21–26)
1.2 (1
.1–1.4
)
bi-
layer
ed,
c.1.1
pre
sent,
1or
2
elli
pso
idal
17.8
910.7
(17–19
9
10–11)
larg
ehom
ogen
eous,
elli
pso
idal
dif
fuse
I.ic
teru
sIc
teru
sic
teru
s
(Ict
erid
ae)
Upto
n&
Whit
aker
(2000
)
sub-
spher
ical
28.9
927.2
(27–32
9
25–30)
1.1 (1
.0–1.1
)
bi-
layer
ed,
c.1.8
pre
sent
(res
iduum
consi
stin
g
of
asm
all
pie
ceof
deb
ris)
elli
pso
idal
17.8
912.8
(17–19
9
12–14)
smal
l,
nip
ple
-
like
larg
e,
hom
ogen
eous
dif
fuse
I.gra
ceannae
Icte
rus
gra
ceannae
(Ict
erid
ae)
Upto
n&
Whit
aker
(2000
)
sub-
spher
ical
23.9
922.3
(20–26
9
19–25)
1.1 (1
.0–1.2
)
bi-
layer
ed,
c.2.1
pre
sent
elli
pso
idal
15.5
910.7
(14–16
9
10–11)
robust
wit
h com
par
tmen
t
dif
fuse
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cobra
iG
eoth
lypis
aeq
uin
oct
iali
s
(Par
uli
dae
)
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toet
al.
(2009f)
sub-
spher
ical
or
ovoid
23.5
921.6
(21–26
9
20–24)
1.1 (1
.1–1.1
)
bi-
layer
ed,
c.1.2
pre
sent
ovoid
15.8
910.5
(15–17
9
9–12)
knob-l
ike
larg
e,
trap
ezoid
al
dif
fuse
184 Syst Parasitol (2011) 80:159–204
123
Ta
ble
10
Co
mp
arat
ive
mo
rph
olo
gy
of
Iso
spo
rasp
p.
reco
rded
fro
mN
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asse
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fth
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rder
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seri
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rid
a(P
art
6)
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ccid
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Ref
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sts
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oro
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ape
Mea
sure
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ts
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Sh
ape
ind
ex
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l(l
m)
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lar
gra
nu
le
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ape
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sure
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ts
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eda
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dy
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bst
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sser
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mes
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asse
rid
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ine
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Mo
han
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60
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ine
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82
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-
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eric
al
or
elli
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idal
24
92
2
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99
17
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7)
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ne- la
yer
ed,
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pre
sen
t,
1o
r
mo
re
ov
oid
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lem
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-
shap
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16
91
0
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sen
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lai
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gio
sa(S
turn
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atia
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73
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ton
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84
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-
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al
24
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22
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89
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sen
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-
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–2
49
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.1–
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sen
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9)
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zela
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to
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oid
22
.19
18
.9
(20
–2
59
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–2
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.1–
1.3
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up
idae
);
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pa
lma
rum
(Th
rau
pid
ae);
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cnis
caya
na
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rau
pid
ae)
Ber
toet
al.
(20
08
a,
20
10
a,c)
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-
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eric
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24
.29
23
.4
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–2
69
21
–2
6)
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1.1
)
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lay
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,
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.3
abse
nt
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oid
17
.79
11
.5
(17
–1
99
11
–1
3)
flat
ten
edla
rge,
pro
min
ent
dif
fuse
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)
Type-host: Ramphocelus bresilius dorsalis (Sclater),
Brazilian tanager.
Type-locality: Brazil, State of the Rio de Janeiro,
Marambaia Island (23�040S, 43�530W).
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)
Type-host: Ramphocelus bresilius dorsalis (Sclater),
Brazilian tanager.
Other host: Thraupis palmarum (Wied), palm tanager
Type-locality: Brazil, State of the Rio de Janeiro,
Marambaia Island (23�040S, 43�530W).
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)
Type-host: Ramphocelus bresilius dorsalis (Sclater),
Brazilian tanager.
Type-locality: Brazil, State of the Rio de Janeiro,
Marambaia Island (23�040S, 43�530W).
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
ued
Co
ccid
iaH
ost
(s)
Ref
eren
ce(s
)O
ocy
sts
Sp
oro
cyst
s
Sh
ape
Mea
sure
men
ts
(lm
)
Sh
ape
ind
ex
Wal
l(l
m)
Po
lar
gra
nu
le
Sh
ape
Mea
sure
men
ts
(lm
)
Sti
eda
bo
dy
Su
bst
ied
a
bo
dy
Res
idu
um
I.m
ara
mb
aie
nsi
sR
.b
.d
ors
ali
s(T
hra
up
idae
)
Ber
toet
al.
(20
08
a,
20
10
c)
sub
-
sph
eric
al
29
.49
27
.9
(27
–3
19
26
–2
9)
1.0 (1
.0–
1.1
)
bi-
lay
ered
,
c.1
.5
abse
nt
elli
pso
idal
22
.69
13
.0
(21
–2
49
12
–1
4)
flat
ten
edsm
all
dif
fuse
I.se
pet
iben
sis
R.
b.
do
rsa
lis
(Th
rau
pid
ae)
Ber
toet
al.
(20
08
a,
20
10
c)
sub
-
sph
eric
al
to elli
pso
idal
25
.59
23
.8
(24
–2
99
22
–2
6)
1.1 (1
.0–
1.2
)
bi-
lay
ered
,
c.1
.4
pre
sen
t,
1o
r2
elli
pso
idal
16
.99
11
.0
(16
–1
89
10
–1
2)
kn
ob
-lik
ep
rom
inen
tla
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.
Type-locality: Brazil, State of the Rio de Janeiro,
Teresopolis City (22�250S, 42�590W).
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)
Type-host: Thraupis sayaca (L.), sayaca tanager.
Type-locality: Brazil, State of the Rio de Janeiro,
Teresopolis City (22�250S, 42�590W).
Remarks: This was the second species described by
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 &
Lopes, 2009 (Fig. 8a)
Type-host: Thraupis sayaca (L.), sayaca tanager.
Type-locality: Brazil, State of the Rio de Janeiro,
Teresopolis City (22�250S, 42�590W).
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.
Type-locality: USA, Hawaii.
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.
Type-locality: USA, Hawaii.
Remark: This was the first species of Isospora
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.
Remarks: This was the second species described by
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.
Type-locality: USA, Hawaii.
Remark: This was the first species of Isospora
described from New World zosteropids (Levine
et al., 1980; Upton et al., 1988) (Table 12).
Isospora manoaensis Upton, Marchiondo & Wil-
liams, 1988 (Fig. 8h)
Type-host: Zosterops japonicus (Temminck, Schle-
gel), Japanese white-eye.
Type-locality: USA, Hawaii, Oahu, Manoa Valley,
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)
Type-host: Zosterops japonicus (Temminck, Schle-
gel), Japanese white-eye.
Type-locality: USA, Hawaii, Oahu, Manoa Valley,
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
Fig. 7 Line drawings of coccidia recorded from New World
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
Co
mp
arat
ive
mo
rph
olo
gy
of
Iso
spo
rasp
p.
reco
rded
fro
mN
ewW
orl
dp
asse
rin
eb
ird
so
fth
ein
frao
rder
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seri
,p
arv
ord
erP
asse
rid
a(P
art
7)
Cocc
idia
Host
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.ca
dim
iR
am
phoce
lus
bre
sili
us
dors
ali
s(T
hra
upid
ae)
Ber
toet
al.
(2009b,
2010c)
sub-
spher
ical
24
.29
22.9
(22–26
9
21–24)
1.1 (1
.0–1
.1)
bi-
layer
ed,
c.1.1
abse
nt
ovoid
16.9
911.6
(15–18
9
10–13)
nip
ple
-
like
wit
h
com
par
tmen
t
dif
fuse
I.nava
rroi
R.
b.
dors
ali
s(T
hra
upid
ae)
Ber
toet
al.
(2009b,
2010c)
sub-
spher
ical
21
.49
20.6
(19–24
9
18–23)
1.1 (1
.0–1
.1)
bi-
layer
ed,
c.1.1
abse
nt
elli
pso
idal
16.1
910.2
(14–19
9
9–12)
flat
tened
smal
ldif
fuse
I.ra
mphoce
liR
.b.
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
dif
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
I.sa
yaca
eT
.sa
yaca
(Thra
upid
ae)
Ber
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
I.si
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
icat
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
.3–1
.8)
bi-
layer
ed,
c.1.0
pre
sent,
1or
2
ovoid
15.5
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 &
Fig. 8 Line drawings of coccidia recorded from New World
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
b
192 Syst Parasitol (2011) 80:159–204
123
Ta
ble
12
Co
mp
arat
ive
mo
rph
olo
gy
of
Iso
spo
rasp
p.
reco
rded
fro
mN
ewW
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dp
asse
rin
eb
ird
so
fth
ein
frao
rder
Pas
seri
,p
arv
ord
erP
asse
rid
a(P
art
8)
Cocc
idia
Host
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.phaeo
rnis
Mya
des
tes
obsc
uru
s(T
urd
idae
)
Lev
ine
etal
.
(1980
)
elli
pso
idal
27
919
(25–28
9
18–20)
–one-
layer
ed,
c.0
.8pre
sent
ovoid
16
911
(15–18
9
10–11)
pre
sent
pre
sent
com
pac
t
I.ro
bin
iT
urd
us
mig
rato
rius
(Turd
idae
)
McQ
uis
tion
&H
olm
es
(1988
)
elli
pso
idal
or
ovoid
23
920
(20–28
9
16–22)
1.1
one-
layer
ed,
c.1
.0pre
sent
ovoid
13
.89
9.0
(10–17
9
7–12)
nip
ple
-lik
epro
min
ent
com
pac
t
I.tu
curu
iensi
sT
.alb
icoll
is(T
urd
idae
)
Lai
nso
n&
Shaw
(1989
)
sub-
spher
ical
17
.39
17
.1(1
5–19
9
14–19)
–one-
layer
ed,
c.0
.8pre
sent
elli
pso
idal
11
.89
8.4
(10–13
9
7–10)
nip
ple
-lik
epre
sent
dif
fuse
or
com
pac
t
I.alb
icoll
isT
.alb
icoll
is(T
urd
idae
)
Lai
nso
n&
Shaw
(1989
)
ovoid
24
.59
20
.3(2
2–27
9
19–24)
–one-
layer
ed,
c.0
.8,
wit
h
mic
ropyle
pre
sent
elli
pso
idal
16
.09
11
.2(1
2–15
9
8–10)
nip
ple
-lik
e,
pro
min
ent
pre
sent
dif
fuse
or
com
pac
t
I.bra
yiZ
ost
erops
japonic
us
(Zost
eropid
ae)
Lev
ine
etal
.
(1980
);
Upto
net
al.
(1988
)
sub-
spher
ical
27
926
(26–28
9
25–27)
–one-
layer
ed,
c.0
.5ab
sent
ovoid
or
pyri
form
19
912
(18–21
9
11–13)
pre
sent
pre
sent
com
pac
t
I.m
anoaen
sis
Z.
japonic
us
(Zost
eropid
ae)
Upto
net
al.
(1988
)
sub-
spher
ical
28
926
.5(2
5–31
9
22–29)
1.1 (1
.0–1
.2)
bi-
layer
ed,
c.1
.5pre
sent,
man
y
spli
nte
r-
like
gra
nule
s
ovoid
18
.59
12
(16–20
9
10–14)
pre
sent,
flat
tened
pre
sent
com
pac
t
I.m
ejir
oZ
.ja
ponic
us
(Zost
eropid
ae)
Upto
net
al.
(1988
)
sub-
spher
ical
28.5
927
(25–32
9
25–30)
1.1 (1
.0–1
.1)
bi-
layer
ed,
c.1.5
pre
sent
ovoid
17
911
(16–19
9
10–12)
pre
sent,
dom
e-li
ke
pre
sent
com
pac
t
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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