ORIGINAL PAPER

New species of Eimeria (Apicomplexa: Eimeriidae)
from Thrichomys fosteri and Clyomys laticeps
(Rodentia: Echimyidae) of the Brazilian Pantanal

Wanessa Teixeira Gomes Barreto1 & Lúcio André Viana2 & Filipe Martins Santos1 &

Grasiela Edith de Oliveira Porfírio1 & Alessandra Cabral Perdomo3 &

Alanderson Rodrigues da Silva4 & Keyla Carstens Marques de Sousa5 &

Michel Angelo Constantino de Oliveira1 & Heitor Miraglia Herrera1 &

Gisele Braziliano de Andrade1

Received: 29 April 2017 /Accepted: 24 August 2017 /Published online: 5 September 2017
# Springer-Verlag GmbH Germany 2017

Abstract The echimyid rodents Thrichomys fosteri and
Clyomys laticeps are among the most commonly recorded
small mammals in the Pantanal wetland of Brazil. These spe-
cies play important ecological roles since they are the basis of
the food chain of some predators and are parasitized by some
pathogens. Knowledge of the eimerians that parasitize
echimyid rodents in Brazil is absent, and only one report is
available for South America. We therefore investigated parasit-
ism by coccidians in the echimyids T. fosteri and C. laticeps in
the Pantanal. Using morphological and morphometric features
and associated statistical analyses, we describe five new eimerian
species parasitizing T. fosteri (Eimeria nhecolandensis n. sp.,
Eimeria jansenae n. sp., and Eimeria fosteri n. sp.) and
C. laticeps (E. nhecolandensis n. sp., Eimeria corumbaensis n.

sp., and Eimeria laticeps n. sp.) in different types of infection
associations. We document the developmental forms in the tis-
sues, and describe lesions in the enteric tract of some infected
animals. We also discuss some approaches regarding epidemio-
logical and ecological data. Our results demonstrate that
echimyid rodents in the Brazilian Pantanal are important hosts
for the maintenance of enteric coccidia. Moreover, in some cir-
cumstances, this parasitism may threaten the health of the hosts.

Keywords Small mammals . Thrichomys fosteri .Clyomys
laticeps . Coccidia . Histopathology . Pantanal

Introduction

The superfamily Octodontoidea is the most diverse superfam-
ily of caviomorph rodents (Rodentia), comprising six families,
38 genera, and 193 living species (Upham and Patterson
2012). Its distribution extends from arid deserts to tropical
forests and alpine steppes (Mares and Ojeda 1982; Redford
and Eisenberg 1992). The octodontoidean family Echimyidae
comprises about 80 species. It is a diverse family and also the
one that presents the greatest diversity of ecomorphological
adaptations within the infraorder Hystricognathi (Emmons
and Feer 1997; Eisenberg and Redford 1999). Studies have
demonstrated that the echimyid rodents Thrichomys fosteri
Thomas, 1903, and Clyomys laticeps (Thomas, 1909) are
among the most commonly recorded small mammals in the
Pantanal wetland (Herrera et al. 2007; Andreazzi et al. 2011).

The genus Thrichomys comprises four recognized species:
Thrichomys apereoides (Lund, 1839), T. inermis (Pictet,
1843), T. fosteri (syn. pachyurus), and T. laurentius Thomas,

Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00436-017-5602-z) contains supplementary
material, which is available to authorized users.

* Heitor Miraglia Herrera
herrera@ucdb.br

1 Programa de Pós-Graduação em Ciências Ambientais e
Sustentabilidade Agropecuária, Universidade Católica Dom Bosco,
Campo Grande, MS, Brazil

2 Departamento de Ciências Biológicas e da Saúde, Universidade
Federal do Amapá, UNIFAP, Macapá, Amapá, Brazil

3 Curso de Medicina Veterinária, Universidade Católica Dom Bosco,
Campo Grande, MS, Brazil

4 Programa de Pós-Graduação em Biotecnologia, UCDB, Campo
Grande, MS, Brazil

5 Faculdade de Ciências Agrárias e Veterinárias, Universidade Federal
Paulista, UNESP, Jaboticabal, SP, Brazil

Parasitol Res (2017) 116:2941–2956
DOI 10.1007/s00436-017-5602-z

https://doi.org/10.1007/s00436-017-5602-z
mailto:herrera@ucdb.br
http://crossmark.crossref.org/dialog/?doi=10.1007/s00436-017-5602-z&domain=pdf


1904 (Pessôa et al. 2015). Thrichomys fosteri is a medium-
sized small mammal distributed across open tropical regions
in central and eastern South America, including the Chaco and
Pantanal ecoregions of Brazil, Bolivia, and Paraguay
(Bonvicino et al. 2008; D’Elía and Myers 2014; Lacher
2016). This species is nocturnal and primarily terrestrial, al-
though it may climb the lower strata of trees and shrubs, and
males occupy slightly larger home ranges than females
(Oliveira and Bonvicino 2011; Pessôa et al. 2015; Porfirio
et al. 2016). Its diet is composed mainly of fruits, shoots,
leaves, and arthropods (Camilo-Alves and Mourão 2009;
Oliveira and Bonvicino 2011; Antunes et al. 2016).

The broad-headed spiny rat C. laticeps is another medium-
sized rodent that inhabits the tropical savannas and grasslands
of central Brazil and the open vegetation areas of the
Paraguayan Chaco and the Brazilian Pantanal (Bishop 1974;
Avila-Pires and Wutke 1981; Lacher and Alho 1989; Vieira
1997). This species is the only representative of its genus, as
recently revised by Bezerra et al. (2016). Clyomys laticeps
exhibits fossorial to semi-fossorial habits and lives in excavat-
ed burrows (Lacher and Alho 1989; Bezerra and De Oliveira
2010). Studies carried out in São Paulo state and in the
Pantanal of Mato Grosso do Sul state revealed a positive as-
sociation between C. laticeps populations and the presence of
palm trees (Attalea geraensis, A. phalerata, and Syagrus
petraea) (Almeida and Galetti 2007; Antunes et al. 2016),
areas of cultivation of corn and manioc (Alho et al. 1987),
areas of Pinus monoculture (Carvalho and Bueno 1975), and
areas with monocot plants (Vieira 2003). The diet of the spe-
cies is composed of the seeds of palms and monocot plants
(Vieira 2003; Almeida and Galetti 2007).

Although T. fosteri and C. laticeps overlap in geographic
distribution, competition is avoided since one is scansorial
while the other is fossorial (Lacher and Alho 1989).
Moreover, due to their abundance, these species play impor-
tant ecological roles as seed dispersers and are the basis of the
food chains of some predators (Lessa and Costa 2009; Bianchi
et al. 2014; Bezerra et al. 2016). These two rodents have been
found to be parasitized in the Pantanal region by some species
of protozoans, helminths, bacteria, and ticks (Herrera et al.
2007; Simões et al. 2010; Vieira et al. 2013; Wolf et al.
2016). To our knowledge, however, no previous information
regarding enteric coccidian infections has been reported in
these two species.

The genus Eimeria Schneider, 1875, comprises more than
1200 species and is considered the largest genus in the family
Eimeriidae (Tenter et al. 2002). Traditionally, enteric
coccidians are identified based on the morphometry and mor-
phology of the oocysts, as well as the identity of the host
species (Tenter et al. 2002; Berto et al. 2014). Duszynski
and Wilber (1997) prepared a guideline for description and
species differentiation in order to better evaluate and propose
new species of Eimeriidae. These authors recommended that

new coccidian species should be compared in detail with sim-
ilar coccidian species found in the same host genus and, in
particular, that comparisons should be made between the can-
didate new species and all described species found in the host
family in order to avoid naming new species based only on the
host. Moreover, sporulated oocysts in the Eimeriidae may
exhibit polymorphism, and this should be an important ele-
ment to be considered in the identification of new eimerian
species (Gardner and Duszynski 1990; Berto et al. 2011).

Knowledge of eimerians parasitizing echimyid rodents in
Brazil is lacking, and only one report is available for South
America (Arcay-de-Peraza 1964). Our objective was therefore
to investigate parasitism by coccidians in the echimyid rodents
T. fosteri and C. laticeps sampled in the Brazilian Pantanal.
We also collected epidemiological and ecological data from
these species.

Material and methods

Study area and sampling procedures

Our study was carried out at the research station of the
Brazilian Agricultural Research Corporation (Embrapa), lo-
cated in the Nhecolândia sub-region of the Pantanal wetland,
Corumbá municipality, Mato Grosso do Sul state, Brazil (19°
08′ 28″ S, 56° 49′ 23″ W). The climate is tropical sub-humid
(Aw), with a characteristic dry season from May to October
and a rainy season from November to April. The annual pre-
cipitation is ~ 1180 mm, the minimum average temperature is
19 °C, while the maximum can reach 38 °C (Cadavid 1984;
Soriano and Alves 2005). The main economic activity in the
area is cattle ranching (Zucco and Mourão 2009), which in-
creases the likelihood of contact between domestic and wild
species. The study area is characterized by sandy soil with a
mosaic vegetation of semi-deciduous forest, dispersed shrub
vegetation, and seasonally flooded fields. Permanent and tem-
porary freshwater ponds and alkaline ponds occur throughout
the area. The understory is dominated by patches of caraguatá
bromeliad (Bromelia balansae), and stands of acuri palm
(Attalea phalerata) and bamboo (Guadua paniculata)
(Abdon et al. 1998; Antunes et al. 2016).

Study animals were captured with Tomahawk
(45 × 17.5 × 15 cm) and Sherman (31 × 0.8 × 0.9 cm) live traps
baited with a mix of banana, peanut candy, sardine, and rolled
oats in March 2015. The traps were placed on the ground at 10-
m intervals along five linear transects in forested areas, with 15
Tomahawk and 15 Sherman traps alternating in each transect.
Traps were rebaited daily and remained open for seven consec-
utive nights, for a total sampling effort of 2100 trap-nights,
equally distributed among the linear transects. Captured ani-
mals were sedated by intramuscular injection of ketamine and
acepromazine (5–10 mg/kg) and were euthanized by

2942 Parasitol Res (2017) 116:2941–2956



intracardiac injection of 0.2–2 mL/individual of T61®
(Intervet; Unterschleissheim, Germany) (mebezonium iodide
5 g + embutramide 20 g + tetracaine hydrochloride 0.5 g).

Small mammals were trapped and collected by authoriza-
tion of the Sistema de Autorização e Informação em
Biodiversidade (SISBIO) under licenses 38145 and 38787-1,
and according to the Ethical Guidelines for Animal Research
established by the Brazilian Society of Laboratory Animal
Science (SBCAL); the work was approved by the university’s
Animal Research Ethics Committee (protocol number UCDB
013/2016). Photosyntypes of the parasites have been deposit-
ed in the Parasitology Collection of the Laboratório de
Biologia de Coccídios at Universidade Federal Rural do Rio
de Janeiro (UFRRJ), located in Seropedica, Rio de Janeiro,
Brazil.

Coprological analysis

Conventional methods for concentration, preservation, and
description of oocysts followed Duszynski and Wilber
(1997). At necropsy, fecal material was removed from the
lower bowel of each animal, preserved in Falcon™ 50-mL
tubes containing 2.5% aqueous (w/v) potassium dichromate
(K2Cr2O7) solution, and maintained at room temperature.
Sporulated oocysts were concentrated by flotation in
Sheather’s sugar solution and examined from 329 to 522 days
after the specimens were collected using a Zeiss Axio
Scope.A1 microscope equipped with a camera. The oocysts
were measured and photographed with the software Zen lite
Blue edition 2011 using 100× objective lenses. All measure-
ments were recorded in micrometers (μm). The ratio of length
by width (shape-index, L × W) was used to demonstrate the
shape of the oocysts and sporocysts. The morphology of the
Stieda body was described according the recommendations of
Berto et al. (2014). Morphometrical and morphological fea-
tures were primarily compared with those Eimeria species
previously reported from members of the Echimyidae family.
Moreover, due to the scarcity of studies in echimyid rodents
and to their phylogenetic proximity, we used in our compari-
sons rodent species belonging to the Ctenomyidae family,
within the superfamily Octodontoidea (Blanga-Kanfi et al.
2009; Upham and Patterson 2015).

Histological analysis

For histopathological examination, tissue samples of the
intestine of each rodent were prepared by the Swiss roll
technique (Moolenbeek and Ruitenberg 1981) to in-
crease the surface area for analysis, and by conventional
transverse cuts. The samples were fixed in neutral-
buffered 10% formaldehyde for preparation of histolog-
ical slides, and stained with hematoxylin-eosin (HE).
Inflammatory infiltrates were characterized as described

by Solano-Gallego et al. (2004): (a) discrete and focal,
with small isolated foci of inflammatory cells; (b) mod-
erate and multifocal, with coalescent foci; and (c) severe
and diffuse, with large diffuse areas. To quantify para-
site load, endogenous stages (meronts, immature game-
tocytes, macrogamonts, microgametocytes, and oocysts)
were counted on slides stained by HE under a light
microscope. Ten microscopic fields of 145.649 μm2

(20× objective) were selected from among those show-
ing endogenous stages of coccidian parasites, for a final
total evaluation area of 1456.49 μm2, following Verçosa
et al. (2012) with adaptations, such as the number of
fields that were counted and the magnification used.

Data analysis

Statistical analyses were performed on morphotypes of
coccidian oocysts identified in each host species sampled
(T. fosteri and C. laticeps). We tested for differences in
morphometrical measurements of oocysts, in addition to con-
sidering host species identity, in order to distinguish eimerian
species, following the recommendations of Duszynski and
Wilber (1997). Measurements of six characters of each oocyst
(oocyst length, oocyst width, oocyst index, sporocyst length,
sporocyst width, and sporocyst index) were used in the anal-
ysis. Data were log10 transformed before analysis due to
slight deviations from normality.

To test for possible differences in morphotypes with
respect to the six measurements taken, we performed a
MANOVA (multiple analysis of variance). Wilk’s lambda
was selected as the MANOVA test criterion. If the
MANOVA was significant (p ≤ 0.05), a Hotelling test
was performed for each morphotype in order to determine
the pairwise significance. Canonical variable analysis
(CVA) yielded a scatter plot of morphotypes on the first
two canonical axes through discriminant analysis. The
axes are linear combinations of the original variables,
and the eigenvalues show the amount of variation that
was explained in the axes. Levels of statistical signifi-
cance were set a priori at p ≤ 0.05. This approach was
carried out initially with oocyst measurements taken from
one host species, and then the analyses were performed
with measurements taken from both studied species.

Linear regression was performed to assess polymorphism,
which occurs when variations in width and length of oocysts
are observed (Norton and Joyner 1981; Berto et al. 2011).
When R2 is higher than 0.5, it means that there is little varia-
tion in the length and width of the species, demonstrating that
the oocysts have uniform characteristics. On the other hand,
when the R2 is lower than 0.5, variation in the length and
width of the species is confirmed, thereby confirming
polymorphism.

Parasitol Res (2017) 116:2941–2956 2943



Results

Fecal samples from 38 specimens of T. fosteri and two spec-
imens of C. laticeps were obtained. Coprological prevalence
of oocysts morphologically compatible with Eimeria spp. was
40% (14 T. fosteri and two C. laticeps). We found three
morphotypes of Eimeria spp. in T. fosteri (M1, M2, and M3)
and three morphotypes of Eimeria spp. in C. laticeps (M4,
M5, and M6). Measurements of all eimerian morphotypes
from both the rodent species sampled and from other
Octodontoidea described in the literature are shown in
Table 1. Note that in the case of Eimeria opimi, the oocysts
recovered from different species of Ctenomys presented dif-
ferent measurements.

Thrichomys fosteri

We observed statistical differences in morphometrical data
among the three Eimeria morphotypes found in T. fosteri
(F = 37.6, p < 0.01). Moreover, the Hotelling test showed
significant differences between the measurements of all the
morphotypes (Online Resource 1).

Differences among the three Eimeria morphotypes in
T. fosteri were also observed in the CVA test. Online
Resource 2 displays a scatter plot of the morphotypes that
includes 100% of the variation in the data in the first two
canonical axes.

Clyomys laticeps

We observed statistical differences in morphometrical data
among the three Eimeria morphotypes found in C. laticeps
(F = 26.3, p < 0.01). The Hotelling test also showed signifi-
cant differences between all the morphotypes (Online
Resource 3).

The CVA test produced a scatter plot of the morphotypes
that includes 100% of the variation in the data in the first two
canonical axes (Online Resource 4).

The measurements of the six morphotypes observed in
T. fosteri and C. laticeps showed statistical differences
(F = 31.4, p < 0.0001). Also, the Hotelling test revealed sig-
nificant interspecific variation among the morphometrical data
of all six morphotypes (Online Resource 5). However, we
found an overlap between the measurements of M1 and M4
in the CVA test, with 92.7% of the variation in the data in the
first two canonical axes (Online Resource 6).

We found polymorphism, demonstrated by linear regres-
sion, in two Eimeria morphotypes from T. fosteri: M1
(R2 = 0.46, p = 6.372e−08) and M2 (R2 = 0.21,
p = 0.001238). M3 was the only morphotype that presented
uniform characteristics (R2 = 0.75, p = 5.139e−12) (Online
Resource 7). We also observed polymorphism in three
Eimeria morphotypes from C. laticeps: M4 (R2 = 0.25,

p = 5.139e−12), M5 (R2 = 0.28, p = 9.15e−05), and M6
(R2 = 0.36, p = 1.995e−06) (Online Resource 8).

Species descriptions

We considered M1 found in T. fosteri and M4 found in
C. laticeps to be the same species due to their similarity in
morphometrical and morphological data, as demonstrated by
statistical and morphological analyses.

Eimeria nhecolandensis n. sp.

Sporulated oocysts ovoidal, L × W (n = 105) 27.6 μm (23.3–
31.6) × 22.2 μm (19.0–25.1), shape-index (L/W) 1.2 (1.1–
1.4). Oocyst wall ~ 1.8 μm (1.4–2.5) in total thickness, bi-
layered, inner layer smooth and outer layer slightly rough.
Micropyle absent. Polar granule present with shape ranging
from spherical to elongate, highly refractile. Oocyst residuum
composed of spheroidal structures that vary in number and
shape from a single large sphere to various small spheres,
L × W (n = 31) 6.5 μm (3.7–10.2) × 5.6 μm (3.2–9.1).
Sporocysts (n = 100) ovoidal to ellipsoidal, 11.0 μm (8.6–
12.9) × 8.2 μm (6.7–9.8), with a shape-index of 1.4 (1.1–
1.7). Stieda body present, nipple-shaped. Sub-stieda and
parastieda bodies absent. A diffuse sporocyst residuum com-
posed of small granules of different sizes is present, some-
times forming a line along the sporocyst wall and/or dispersed
in the sporocyst. Sporozoites not measured (Fig. 1).

Taxonomic summary Type-host: Thrichomys fosteri
(Thomas, 1903) (Rodentia, Echimyidae).

Type-locality: Nhumirim Farm, Nhecolândia Pantanal sub-
region, municipality of Corumbá, State of Mato Grosso do
Sul, Brazil (19° 08′ 28″ S, 56° 49′ 23″ W).

Other hosts: Clyomys laticeps (Thomas, 1909).
Type-material: Phototypes are deposited and available

(http://r1.ufrrj.br/labicoc/colecao. html) in the Parasitology
Collection of the Laboratório de Biologia de Coccídios at
Universidade Federal Rural do Rio de Janeiro, located in
Seropédica, Rio de Janeiro, Brazil. Photographs of the type-
host specimen (symbiotype) are deposited in the same collec-
tion. The repository number is P-71/2017.

Sporulation time: Unknown.
Site of infection: Small intestine.
Prevalence: Found in 35% (14/40) of the animals exam-

ined (13 T. fosteri and one C. laticeps).
Etymology: The specific epithet is derived from the name

of the study area.
Remarks: The slight roughness of the oocyst wall of

E. nhecolandensis differs from the other eimerian oocysts ex-
amined in our study, which were rough (E. jansenae), strongly
rough (E. fosteri), and smooth (E. laticeps). Moreover, the
ovoidal oocysts of E. nhecolandensis differ from the

2944 Parasitol Res (2017) 116:2941–2956

http://r1.ufrrj.br/labicoc/colecao


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(1
7.
1–
26
.7
)

±
1.
5

1.
1
(0
.9
–1
.2
)
±
0.
1

SP
/S
S

1.
7
(1
.1
–2
.2
)

±
0.
2

10
.7
(8
.7
–1
2.
3)

±
0.
9

8.
1
(6
.4
–9
.2
)
±

0.
6

1.
3
(1
.0
–1
.5
)
±
0.
1

M
yo
ca
st
or

co
yp
us

b
E
.s
ei
de
li

(3
8.
4–
44
.8
)

SP
(2
5.
6–
28
.2
)

12
.8

Pe
llé
rd
y
(1
95
7)

E
.n

ut
ri
ae

20
.0
(1
9.
5–
22
.5
)

±
1.
9

16
.1
(1
5.
0–
18
.0
)

±
1.
4

1.
3
(1
.2
–1
.5
)
±
N
R

O
V
/S
S

N
R

11
.2
(1
0.
5–
12
.0
)

±
0.
3

5.
2
(4
.5
–6
.0
)
±

0.
3

N
R

Pr
as
ad

(1
96
0)

E
.m

yo
ca
st
or
i

14
.2
(1
3.
5–
15
.0
)

±
0.
3

12
.2
(1
1.
5–
13
.0
)

±
0.
3

1.
1
(1
.4
–1
.5
)
±
N
R

O
V

N
R

9.
6
(9
.0
–1
0.
5)

±
0.
2

3.
7
(3
.0
–4
.5
)
±

0.
3

N
R

P
ro
ec
hi
m
ys

gu
ay
an
en
si
s

E
.p

ro
ec
hi
m
yi

22
.9
±
N
R

17
.1
±
N
R

N
R

E
L

N
R

6.
7
±
N
R

6.
7
±
N
R

A
rc
ay
-d
e-
Pe
ra
za

(1
96
4)

E
.c
ar
ip
en
si
s

20
.0
±
N
R

20
.0
±
N
R

N
R

SP
N
R

8.
7
±
N
R

5.
5
±
N
R

N
R

C
te
no
m
ys

op
im
us

E
.g

ra
ni
fe
ra

21
.1
(1
5.
0–
26
.0
)

±
N
R

17
.2
(1
1.
0–
20
.0
)

±
N
R

1.
2
±
N
R

SS
/E
L

2.
0
±
N
R

11
.3
(8
.0
–1
4.
0)

±
N
R

7.
1
(5
.0
–9
.0
)
±

N
R

1.
6
±
N
R

L
am

be
rt
et
al
.(
19
88
)

E
.m

on
tu
os
i

24
.2
(2
1.
0–
28
.0
)

±
N
R

22
.0
(1
8.
0–
25
.0
)

±
N
R

1.
1
±
N
R

SP
3.
0
±
N
R

10
.5
(8
.0
–1
4.
0)

±
N
R

7.
3
(6
.0
–9
.0
)
±

N
R

1.
4
±
N
R

E
.o

pi
m
i

24
.3
(1
8.
0–
29
.0
)

±
N
R

21
.8
(1
5.
0–
26
.0
)

±
N
R

1.
1
±
N
R

SP
/S
S

1.
5
±
N
R

11
.6
(1
0.
0–
13
.0
)

±
N
R

7.
6
(6
.0
–9
.0
)
±

N
R

1.
6
±
N
R

E
.o

ru
ro
en
si
s

27
.3
(2
3.
0–
32
.0
)

±
N
R

23
.6
(2
0.
0–
28
.0
)

±
N
R

1.
2
±
N
R

SP
/S
S

2.
3–
3.
0
±
N
R

13
.2
(1
0.
0–
16
.0
)

±
N
R

8.
6
(8
.0
–1
1.
0)

±
N
R

1.
5
±
N
R

C
te
no
m
ys

bo
liv
ie
ns
is

E
.o

pi
m
i

21
.7
(1
9.
0–
25
.0
)

±
N
R

19
.4
(1
5.
0–
22
.0
)

±
N
R

1.
1
±
N
R

SP
N
R

9.
5
(7
.0
–1
1.
0)

±
N
R

6.
8
(6
.0
–8
.0
)
±

N
R

1.
4
±
N
R

G
ar
dn
er

an
d
D
us
zy
ns
ki

(1
99
0)

C
te
no
m
ys

co
no
ve
ri

20
.9
(1
9.
0–
23
.0
)

±
N
R

19
.2
(1
7.
0–
21
.0
)

±
N
R

1.
1
±
N
R

N
R

10
.3
(8
.0
–1
1.
0)

±
N
R

7.
0
(5
.0
–8
.0
)
±

N
R

1.
3
±
N
R

C
te
no
m
ys

fr
at
er

21
.7
(1
9.
0–
26
.0
)

±
N
R

19
.9
(1
6.
0–
25
.0
)

±
N
R

1.
1
±
N
R

N
R

10
.5
(9
.0
–1
3.
0)

±
N
R

7.
0
(5
.0
–8
.0
)
±

N
R

1.
5
±
N
R

C
te
no
m
ys

le
w
is
i

23
.7
(1
8.
0–
26
.0
)

±
N
R

21
.2
(1
7.
0–
25
.0
)

±
N
R

1.
1
±
N
R

N
R

10
.5
(8
.0
–1
3.
0)

±
N
R

7.
5
(5
.0
–8
.0
)
±

N
R

1.
5
±
N
R

D
at
a
pr
ov
id
ed

in
th
e
fo
llo

w
in
g
fo
rm

:m
ea
n,
ra
ng
e
(i
n
pa
re
nt
he
se
s)
,a
nd

st
an
da
rd

de
vi
at
io
n

M
1
m
or
ph
ot
yp
e
1,
M
2
m
or
ph
ot
yp
e
2,
M
3
m
or
ph
ot
yp
e
3,
M
4
m
or
ph
ot
yp
e
4,
M
5
m
or
ph
ot
yp
e
5,
M
6
m
or
ph
ot
yp
e
6,
N
R
no
tr
ep
or
te
d

a
O
oc
ys
ts
ha
pe

as
de
sc
ri
be
d—

E
L
:e
lli
ps
oi
da
l;
O
V
:o

vo
id
al
;S

P
:s
ph
er
oi
da
l;
SS

:s
ub
-s
ph
er
oi
da
l

b
E
.m

yo
po
ta
m
i,
E
.p
el
lu
ci
da
,a
nd

E
.c
oy
pi
de
sc
ri
be
d
by

Y
ak
im

of
f(
19
33
)a
nd

O
bi
tz
an
d
W
ad
ow

sk
i(
19
37
)i
n
M
yo
ca
st
or

co
yp
us

ar
e
no
td
et
ai
le
d
du
e
to
co
nt
ro
ve
rs
ia
la
nd

in
co
ns
is
te
nc
ie
s
in
th
ei
rd

es
cr
ip
tio

ns

Parasitol Res (2017) 116:2941–2956 2945



ellipsoidal oocysts of E. jansenae and E. corumbaensis and
the spheroidal oocysts of E. laticeps. Morphometrically, when
comparing E. nhecolandensis with E. caripensis and
E. proechimyi described by Arcay-de-Peraza (1964) in
Proechimys guyanensis E. Geoffroy, 1803 (Rodentia:
Echimyidae), from Venezuela, E. nhecolandensis is larger
(27.9 × 22.6 μm) than E. proechimyi (22.9 × 17.1 μm) and
E. caripensis (20.0 μm). Morphologically, these two species
differed in having ellipsoidal and spherical oocysts, respec-
t i v e l y, i n c on t r a s t t o t h e ovo i d a l oo cy s t s o f
E. nhecolandensis. Furthermore, the oocyst residuum found
in E. nhecolandensis was not observed in both species.

Additionally, E. nhecolandensis has ellipsoidal sporocysts,
in contrast to the spherical sporocysts reported in
E. proechimyi . Finally, the Stieda body found in
E. nhecolandensis and E. caripensis is absent in
E. proechimyi. The four Eimeria spp. recovered from
Ctenomys spp. Blainville, 1826 (Rodentia: Ctenomyidae)
(E. granifera, E. montuosi, E. opimi, and E. oruroensis)
(Lambert et al. 1988), all differ from E. nhecolandensis.
Morphometrically, only E. oruroensis had the oocysts close
to E. nhecolandensis, while the other species are smaller, as
shown in Table 1. Regarding oocyst shape, E. nhecolandensis
is ovoidal whereas E. granifera is sub-spheroidal to

Fig. 1 Photomicrographs and line drawing of Eimeria nhecolandensis
recovered from Thrichomys fosteri and Clyomys laticeps (a–c, j), and
E. jansenae (d–f, k) and E. fosteri (g–i, l) recovered from T. fosteri in
Brazilian Pantanal. a Note the slight roughness of the oocyst wall. b
Spheroidal polar granule (thin arrow), compact oocyst residuum
composed of numerous slightly uniform granules (arrow). c Nipple-like
Stieda body (arrow) and sporocyst residuum (thin arrow). d Note the

roughness of the oocyst wall. e Oocyst residuum composed by
spheroidal structures (arrow). f Stieda body (arrow) and polar granule
(thin arrow). g Note the strongly rough oocyst wall with plenty of
granulation (arrows). h Oocyst residuum composed by some spheroidal
structures (arrow). i Stieda body. (Obj. ×63. j Line drawing of a
sporulated oocyst of E. nhecolandensis. k Line drawing of a sporulated
oocyst of E. jansenae. l Line drawing of a sporulated oocyst of E. fosteri

2946 Parasitol Res (2017) 116:2941–2956



ellipsoidal; E. opimi and E. oruroensis are sub-spheroidal to
spheroidal, and E. montuosi is spheroidal. The ovoidal shape
and size of sporocysts recovered from E. nhecolandensis are
similar to those of E. granifera, E. montuosi, E. opimi, and
E. oruroensis as demonstrated in Table 1. In spite of the
abovementioned morphological and morphometrical differ-
ences, we also found some structural features that differentiate
E. nhecolandensis from the other species. The lack of an oo-
cyst residuum, a button-like Stieda body, and compact sporo-
cys t res iduum di ffe ren t i a tes E. grani fera f rom
E. nhecolandensis. The slight roughness of the wall and a
polar granule observed in E. nhecolandensis differ from
E. montuosi due to the oocyst wall composed of two or three
layers with large protruding bumps on the surface, and the
lack of a polar granule. While E. nhecolandensis presents a
diffuse sporocyst residuum composed of small granules of
different sizes, E. opimi differs in the uniformity and number
of granules in the oocyst (8–10 uniform granules) and sporo-
cyst residuum (2–3 granules). The same difference regarding
the sporocyst residuum was observed in E. oruroensis, which
presents a sporocyst residuum composed of two to three gran-
ules. Six species of Eimeria (E. myopotami and E. pellucida
Yakimoff 1933; E. coypiObitz andWadowski 1937; E. seideli
Pellerdy, 1957; E. nutriae; and E. myocastor Prasad 1960)
were described from the rodent Myocastor coypus (Molina,
1782) (Rodentia: Echimyidae). In spite of some controversy
and discussion about E. myopotami, E. pellucida, and E. coypi
in subsequent works (Levine and Ivens 1965), none of the six
eimerians mentioned are similar to the new species reported in
our study, since all of them differ in structural details: absence
of an oocyst residuum in all six Eimeria spp. recovered from
M. coypus; presence of micropyle in E. myocastori and
E. pellucida; lack of a polar granule in E. myocastori,
E. seideli, and E. myopotami; and lack of a Stieda body in
E. myocastori, E. nutriae, E. coypi, and E. myopotami.
These four morphological characters differ from those of the
new species described in this study, besides the size and shape
of oocysts of some species, as shown in Table 1.

Eimeria jansenae n. sp.

Sporulated oocysts (n = 45) ellipsoidal, L ×W 31.4μm (27.1–
37.7) × 22.6 μm (19.6–24.9), shape-index (L/W) 1.4 (1.3–
1.6). Oocyst wall composed of at least two layers, 1.9 μm
(1.4–2.7) thick, inner layer smooth and outer layer rough.
Micropyle absent. Polar granule present, usually spherical,
highly refractile. Oocyst residuum composed of spheroidal
structures that vary in number, form, and size, L × W
(n = 31) 8.7 μm (6.7–13.8) × 7.6 μm (5.6–9.9). Sporocysts
(n = 45) ovoidal, 11.9 μm (9.5–15.6) × 8.3 μm (7.1–10.2),
with a shape-index of 1.4. Stieda body present, nipple-shaped.
Sub-stieda and parastieda bodies absent. Sporocyst residuum

composed of small granules distributed in the sporocysts.
Sporozoites not measured.

Taxonomic summary Type-host: Thrichomys fosteri
(Thomas, 1903) (Rodentia, Echimyidae).

Type-locality: Nhumirim Farm, Nhecolândia Pantanal sub-
region, municipality of Corumbá, State of Mato Grosso do
Sul, Brazil (19° 08′ 28″ S, 56° 49′ 23″ W).

Type-material: Phototypes are deposited and available
(http://r1.ufrrj.br/labicoc/colecao.html) in the Parasitology
Collection of the Laboratório de Biologia de Coccídios at
Universidade Federal Rural do Rio de Janeiro, located in
Seropédica, Rio de Janeiro, Brazil. Photographs of the type-
host specimen (symbiotype) are deposited in the same collec-
tion. The repository number is P-72/2017.

Sporulation time: Unknown.
Site of infection: Small intestine.
Prevalence: Found in 20% (8/40) of the animals examined.
Etymology: The specific epithet is derived from the name

of the great parasitologist Ana Maria Jansen (1945), research-
er of Fundação Oswaldo Cruz, Rio de Janeiro, Brazil.

Remarks: Eimeria jansenae is the largest of the Eimeria
spp. described in this study. It differs from the other species
that parasitize T. fosteri in having ellipsoidal oocysts. Among
the eimerian oocysts recovered from C. laticeps, the morpho-
logical characteristics of E. jansenae are similar to
E. corumbaensis. The oocyst wall is somewhat rougher in
E. jansenae than in E. corumbaensis. In addition,
E. jansenae is larger than E. corumbaensis. In comparison to
E. proechimyi described in P. guyanensis, E. jansenae is larger
(31.4 × 22.6 μm) than E. caripensis (20.0 μm) and
E. proechimyi (22.9 × 17.1 μm). Morphologically, it differs
in having an oocyst residuum, ellipsoidal sporocysts (as op-
posed to spherical sporocysts), and a Stieda body. The ellip-
soidal oocyst and the oocyst residuum in E. jansenae differs
from the spherical oocyst and lack of oocyst residuum in
E. caripensis. Oocysts of E. jansenae are also larger than the
other four species of Eimeria recovered from Ctenomys
opimus Wagner, 1848 (Rodentia: Ctenomyidae) (Lambert
et al. 1988), as shown in Table 1. Morphologically,
E. jansenae differs in having ellipsoidal oocysts, while in
E. montuosi they are spheroidal, in E. granifera oocysts are
sub-spheroidal to ellipsoidal, and in E. opimi and
E. oruroensis oocysts are spheroidal to sub-spheroidal. In ad-
dition to morphometry and shape, other morphological char-
acteristics differentiate E. jansenae from Eimeria spp. recov-
ered from C. opimus. While E. jansenae presents a variable
oocyst residuum, a nipple-like Stieda body, and sporocyst re-
siduum composed by small granules, E. granifera lacks an
oocyst residuum, a button-like Stieda body, and compact spo-
rocyst residuum. When comparing to E. montuosi, an oocyst
wall with large protruding bumps on the surface and the lack
of polar granules differentiate this species from E. jansenae.

Parasitol Res (2017) 116:2941–2956 2947

http://r1.ufrrj.br/labicoc/colecao.html


While E. jansenae presents a variable oocyst residuum with
one or more spheroidal structures that vary in size, number,
and shape, E. opimi presents a compact oocyst residuum with
8–10 uniform granules. The species of Eimeria recorded from
M. coypus differ from E. jansenae in the same structural de-
tails of oocysts as E. nhecolandensis, as pointed out in our
previous remarks.

Eimeria fosteri n. sp.

Sporulated oocysts (n = 41) ovoidal, L × W 25.1 μm (20.9–
37.3) × 20.1 μm (16.7–30.1), shape-index (L/W) 1.2 (1.2–
1.3). Oocyst wall strongly rough, bi-layered, 1.8 μm (1.0–
3.4) in total thickness. Micropyle absent. Polar granule pres-
ent, varying from sub-spherical to elongate in shape. Oocyst
residuum composed of spheroidal structures that vary from a
single large sphere to two to eight spheroidal structures of
different sizes, L × W (n = 24) 6.8 μm (4.9–8.3) × 5.9 μm
(4.0–7.1). Sporocysts (n = 41) ovoidal, 10.0 μm (7.6–
16.0) × 7.2 μm (5.1–11.1), with a shape-index of 1.4 (1.2–
1.7). Stieda body present, nipple-shaped. Sub-stieda and
parastieda bodies absent. Sporocyst residuum composed of
small granules distributed along the sporozoites, sometimes
forming a line. Sporozoites not measured.

Taxonomic summary Type-host: Thrichomys fosteri
(Thomas, 1903) (Rodentia, Echimyidae).

Type-locality: Nhumirim Farm, Nhecolândia Pantanal sub-
region, municipality of Corumbá, State of Mato Grosso do
Sul, Brazil (19° 08′ 28″ S, 56° 49′ 23″ W).

Type-material: Phototypes are deposited and available
(http://r1.ufrrj.br/labicoc/colecao.html) in the Parasitology
Collection of the Laboratório de Biologia de Coccídios at
Universidade Federal Rural do Rio de Janeiro, located in
Seropédica, Rio de Janeiro, Brazil. Photographs of the type-
host specimen (symbiotype) are deposited in the same collec-
tion. The repository number is P-73/2017.

Sporulation time: Unknown.
Site of infection: Small intestine.
Prevalence: Found in 10% (4/40) of the animals examined.
Etymology:The specific epithet is derived from the specific

name of the host.
Remarks: Eimeria fosteri differs from the other species

found in T. fosteri and C. laticeps in having a strongly
rough oocyst wall with deep grooves. In addition, the
ranges of the oocyst length and width and of the wall
thickness were higher than in other species (Table 1).
The only two species previously described in echimyid
rodents (E. proechimyi and E. caripensis) (Arcay-de-
Peraza 1964) differ from E. fosteri. When compared to
E. fosteri, E. proechimyi differs in having an ellipsoidal
oocyst shape (as opposed to ovoidal), in lacking an
oocyst residuum, in having spherical sporocysts (as

opposed to ellipsoidal), and in lacking a Stieda body.
Eimeria caripensis differs from E. fosteri in having
spherical oocysts and in lacking an oocyst residuum.
Unlike the Eimeria spp. recovered from C. opimus,
E. fosteri has ovoidal oocysts. Differences between
E. fosteri and E. granifera: ovoidal vs. spheroidal/
ellipsoidal oocysts, strongly rough oocyst walls vs.
smooth, presence of oocyst residuum and polar granule
vs. lack of both structures, and nipple-like vs. button-
like Stieda body. Differences between E. fosteri and
E. montuosi: ovoidal oocysts vs. spheroidal, strongly
rough oocyst wall vs. large protruding bumps on the
surface, and polar granule sub-spherical to elongate vs.
lack of a polar granule. Differences between E. fosteri
and E. opimi: oocysts ovoidal vs. spheroidal to sub-
spheroidal, strongly rough walls vs. finely sculptured
w a l l s . D i f f e r e n c e s b e tw e e n E . f o s t e r i a n d
E. oruroensis: oocysts ovoidal vs. spheroidal to sub-
spheroidal. The species of Eimeria recorded from
M. coypus differ from the E. fosteri in the same struc-
tural details of oocysts as E. nhecolandensis, as pointed
out in our previous remarks.

Eimeria corumbaensis n. sp.

Sporulated oocysts ellipsoidal, L ×W (n = 49) 28.9μm (20.7–
33.4) × 20.2 μm (15.0–22.8), shape-index (L/W) 1.4 (1.1–
1.7). Oocyst wall 1.67 μm (1.1–2.2) thick, bi-layered, slightly
rough. Micropyle absent. Polar granule present, ranging from
sub-spherical to ovoidal. Oocyst residuum composed in most
cases of a large sphere, but sometimes 1–10 small spheres,
L × W (n = 8) 5.3 μm (4.4–6.5) × 4.8 μm (2.8–6.5).
Sporocysts (n = 49) ovoidal to ellipsoidal, 11.3 μm (9.0–
12.9) × 8.4 μm (7.2–9.4), with a shape-index of 1.3. Stieda
body present, nipple-shaped. Sub-stieda and parastieda bodies
absent. Sporocyst residuum composed of small granules
sometimes forming a line along the sporocyst wall.
Sporozoites not measured (Fig. 2).

Taxonomic summary Type-host: Broad-headed spiny rat
Clyomys laticeps (Thomas, 1909) (Rodentia, Echimyidae).

Type-locality: Nhumirim Farm, Nhecolândia Pantanal sub-
region, municipality of Corumbá, State of Mato Grosso do
Sul, Brazil (19° 08′ 28″ S, 56° 49′ 23″ W).

Type-material: Phototypes are deposited and available
(http://r1.ufrrj.br/labicoc/colecao.html) in the Parasitology
Collection of the Laboratório de Biologia de Coccídios at
Universidade Federal Rural do Rio de Janeiro, located in
Seropédica, Rio de Janeiro, Brazil. Photographs of the type-
host specimen (symbiotype) are deposited in the same collec-
tion. The repository number is P-74/2017.

Sporulation time: Unknown.
Site of infection: Small intestine.

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http://r1.ufrrj.br/labicoc/colecao.html


Prevalence: Found in 1/40 (2.5%) of the animals
examined.

Etymology: The specific epithet is derived from the name
of the municipality where the study area is located.

Remarks: Eimeria corumbaensis differs from the other
Eimeria spp. described in this study mainly regarding the
shape of oocysts, except E. jansenae which is also ellip-
soidal. Nevertheless, E. corumbaensis is smaller than
E. jansenae, and has a slightly rough oocyst wall, while
E. jansenae has a rough oocyst wall. Among the species
described for the superfamily Octodontoidea, the one that
most resembles E. corumbaensis is E. proechimyi recov-
ered from P. guyanensis due to its ellipsoidal shape.
Moreover, E. corumbaensis is larger than E. proechimyi
(28.9 × 20.2 vs. 22.9 × 17.1, respectively). Yet, sporulated
oocys ts of E. proechimyi di ffe r f rom those of

E. corumbaensis by having spherical sporocysts without
Stieda body and oocyst residuum. Sporulated oocysts of
E. caripensis differ from those of E. corumbaensis in
shape (spherical vs. ellipsoidal), lack of oocyst residuum,
and size (20.0 vs. 28.9 × 20.2). All the species of Eimeria
found in Ctenomys spp. are different in shape, besides the
lack of oocyst residuum and shape of Stieda body (button-
like Stieda body) in E. granifera. In addition, the oocyst
wall of E. corumbaensis is slightly rough, while in
E. granifera the wall is smooth. In E. montuosi, the oo-
cyst wall has large protruding bumps on the surface, and
lacking polar granule, whereas in E. oruroensis the oocyst
wall is rough. The species of Eimeria recorded from
M. coypus differ from the E. corumbaensis in the same
structural details of oocysts of E. nhecolandensis, as pre-
viously pointed out.

Fig. 2 Photomicrographs and line drawing of Eimeria corumbaensis (a–
c, g) and Eimeria laticeps (d–f, h) recovered from Clyomys laticeps in
Brazilian Pantanal. a Note the slightly rough wall with a discrete
granulation. b Oocyst residuum composed by three spheroidal
structures (arrow). c Note the by layered oocyst wall. Nipple-like Stieda
body (thin arrow), spheroidal polar granule (arrow), and sporocyst
residuum composed by small granules diffusely distributed

(arrowhead). d, e Note the smooth oocyst wall without granulation, the
oocyst residuum composed by a single spheroidal structure (arrow), and
the spheroidal polar granule (thin arrow). f Sporocyst residuum composed
by small granules forming a line along the sporozoites (head arrow). Obj.
63×. g Line drawing of a sporulated oocyst of E. corumbaensis. h Line
drawing of a sporulated oocyst of E. laticeps

Parasitol Res (2017) 116:2941–2956 2949



Eimeria laticeps n. sp.

Sporulated oocysts spherical to sub-spherical, L × W (n = 52)
23.9 μm (19.2–27.3) × 21.6 μm (17.1–26.7), shape-index
(L/W) 1.1 (0.9–1.2). Oocyst wall 1.7 μm (1.1–2.2) thick, bi-
layered and smooth. Micropyle absent. Polar granule present,
spherical to sub-spherical, located close to the wall. Oocyst
residuum compact, in most cases composed of a large sphere,
L × W (n = 6) 5.1 μm (4.4–6.0) × 4.2 μm (3.9–4.4).
Sporocysts (n = 52) ovoidal to ellipsoidal, 10.7 μm (8.7–
12.3) × 8.1 μm (6.4–9.2), with a shape-index of 1.3. Stieda
body present, nipple-shaped. Sub-stieda and parastieda bodies
absent. Sporocyst residuum composed of small granules.
Sporozoites ovoidal but not measured.

Taxonomic summary Type-host: Broad-headed spiny rat
Clyomys laticeps (Thomas, 1909) (Rodentia, Echimyidae).

Type-locality: Nhumirim farm, Nhecolândia Pantanal sub-
region, municipality of Corumbá, State of Mato Grosso do
Sul, Brazil (19° 08′ 28″ S, 56° 49′ 23″ W).

Type-material: Phototypes are deposited and available
(http://r1.ufrrj.br/labicoc/colecao.html) in the Parasitology
Collection of the Laboratório de Biologia de Coccídios at
Universidade Federal Rural do Rio de Janeiro, located in
Seropédica, Rio de Janeiro, Brazil. Photographs of the type-
host specimen (symbiotype) are deposited in the same collec-
tion. The repository number is P-75/2017.

Sporulation time: Unknown.
Site of infection: Small intestine.
Prevalence: Found in 5% (2/40) of the animals examined.
Etymology:The specific epithet is derived from the specific

name of the host species.
Remarks: Eimeria laticeps is the only Eimeria species that

possessed spherical oocysts and smooth walls in this study.
The morphological characteristics of E. proechimys, with its
ovoidal oocysts, absence of oocyst residuum, and spherical
sporocysts, differ from E. laticeps. The lack of an oocyst re-
siduum and Stieda body differentiate E. caripensis from
E. laticeps. The lack of an oocyst residuum and a polar granule
and the button-like Stieda body of E. granifera differentiate it
from E. laticeps. The oocyst wall composed of large protrud-
ing bumps on the surface and the absence of a polar granule of
E. montuosi differentiate this species from E. laticeps.
Regarding E. oruroensis, the rough wall composed of three
layers and the size of the oocysts (27.3 × 23.6 vs. 23.9 × 21.7)
differentiate this species from E. laticeps. The species that is
closest morphologically and morphometrically to E. laticeps
is E. opimi, but the more pronounced roughness of the wall of
E. opimi and the oocyst residuum composed by a compact
mass of 8–10 uniform granules differentiate this species from
E. laticeps. The species of Eimeria recorded from M. coypus
differ from the E. laticeps in the same structural details of
oocysts as E. nhecolandensis, as detailed above.

Epidemiological data

Eimerian oocysts were found in 40% of sampled rodents
(n = 40): 14 T. fosteri and two C. laticeps. In T. fosteri, the
prevalence found in males was 45% (13/29), and in females
we recorded a prevalence of 13% (1/8). It was not possible to
identify the sex of one specimen of T. fosteri. Five new
Eimeria spp. were described in our study. We found three
species parasitizing T. fosteri (E. nhecolandensis ,
E. jansenae, and E. fosteri) and three species parasitizing
C. laticeps (E. nhecolandensis, E. corumbaensis, and
E. laticeps). Eimeria nhecolandensis was the most prevalent
species in T. fosteri (12/38, 32%), followed by E. jansenae
(8/38, 21%) and E. fosteri (4/38, 11%). In C. laticeps,
E. nhecolandensis and E. laticeps were observed in both in-
dividuals and E. corumbaensis was found in only one.

We found a single infection by E. nhecolandensis and
E. fosteri in five individuals and one individual of T. fosteri,
respectively. Furthermore, we recorded co-infections in
T. fosteri by E. nhecolandensis and E. jansenae (n = 5),
E. jansenae and E. fosteri (n = 1), and E. nhecolandensis +
E. jansenae + E. fosteri (n = 2). In C. laticeps, we found co-
infection by E. nhecolandensis and E. laticeps in one individ-
ual, and by E. nhecolandensis + E. corumbaensis + E. laticeps
in another single individual.

Histopathological analysis

Endogenous stages (meront, immature gametocyte,
macrogamont, microgametocyte, and oocyst) were observed
in the small intestines of 69% (11/16) of the coprologically
positive animals. Two T. fosteri (8.3%) that were negative for
the coprological test presented endogenous stages in the tissue
sections (meront and immature gametocyte) . All
monoinfections were observed only in T. fosteri, and among
them endogenous stages (n = 13) were detected in only one
specimen. Conversely, in all co-infected animals we recorded
developmental forms ranging from 1 to 596. Moreover, in the
two C. laticeps specimens, we observed endogenous stages.

Host: Thrichomys fosteri

Single infections Just one individual from among the five that
were eliminating oocysts of E. nhecolandensis possessed
endogenous stages (n = 13) of coccidians in the
enterocyte villi of the small intestine, including
macrogamonts and immature gametocytes. In general,
in the lamina propria of the small intestine of this ani-
mal, a mild to intense inflammatory reaction was also
observed, multifocal to diffuse, composed predominantly
of macrophages, a few eosinophils, lymphocytes,
plasmocytes, and basophils. The most prominent lesions

2950 Parasitol Res (2017) 116:2941–2956

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were hyperplasia of the epithelium, incipient necrosis of
the apical portion, and merger of the villi.

Endogenous stages of coccidia were not observed in the
individual that was eliminating oocysts of E. fosteri.
However, we observed an intense and diffuse inflammatory
reaction composed of macrophages, lymphocytes, and a few
basophils and eosinophils in the lamina propria of the villi of
the small intestine. In addition, we observed an atrophy of the
villi.

Co-infections Endogenous stages (n = 84) were observed in
tissue sections of the individual that was eliminating oocysts
of E. jansenae and E. fosteri in the feces. Developmental
stages were observed in the epithelium of the villi, and one
single oocyst was observed in the external muscle layer (Fig.
3a). A moderate to intense mixed inflammatory reaction,
mainly composed of macrophages, lymphocytes,
plasmocytes, and eosinophils, diffusely distributed, was seen
in the lamina propria. Hyperplasia of the mucosal epithelium
(Fig. 3b) and atrophy of the villi were also observed.

In the individuals parasitized by E. nhecolandensis and
E. jansenae, all the endogenous coccidian stages were ob-
served (ranging from 1 to 109). The inflammatory reaction
in the lamina propria was mild to intense (Fig. 3c), multifocal
to diffuse, and composed of macrophages, fewer lympho-
cytes, eosinophils, and some interspersed plasmocytes. The
most prominent morphological changes in the villi were epi-
thelial hyperplasia, atrophy, incipient necrosis of the apical
region, merger (Fig. 3d), and destruction.

We found a very large number of endogenous developing
coccidian stages in the small intestines of the two individuals
that were eliminating concomitantly the oocysts of
E. nhecolandensis, E. jansenae, and E. fosteri in the feces.
In the individual with 131 developmental forms, we only ob-
served meronts containing merozoites and immature gameto-
cytes in the villi enterocytes. In the lamina propria, a multifo-
cal, mild to intense inflammatory infiltrate consisting of mac-
rophages, lymphocytes, and eosinophils was evident. In the
other animal, we found that 596 developmental forms, includ-
ing immature gametocytes, different stages of microgamonts
and macrogamonts, and oocysts (Fig. 3e), had invaded most
of the epithelial cells of the villi, displacing the nucleus pe-
ripherally, and they were also present in the lamina propria
(Fig. 3f) and in the lumen. In this animal, the inflammatory
reaction was intense and diffuse, composed predominantly of
macrophages, lymphocytes, and some plasmocytes, located in
the lamina propria (Fig. 3g).

An enlargement of some villi by inflammatory cell accu-
mulation as well as architecture loss due to the destruction of
the epithelium of the villi and the presence of numerous in-
flammatory cells were also observed (Fig. 3h). In addition, we
observed fibrosis foci and the absence of some villi.

Host: Clyomys laticeps

All endogenous coccidian stages at different phases of devel-
opment (n = 124) were observed in the villi and the crypts of
Lieberkühn enterocytes as well as in the lumen of the small
intestine of the individual that showed E. nhecolandensis and
E. laticeps oocysts in the feces. Another C. laticeps that was
found co-infected by three eimerian species presented 58 de-
velopmental forms including meronts containing merozoites,
immature gametocytes, and macrogamonts and microgamonts
in the epithelium of the villi.

Overall, the animals presented a mild to moderate multifo-
cal inflammatory reaction in the lamina propria (Fig. 4a), com-
posed of mononuclear cells (lymphocytes, macrophages, and
a few plasmocytes). The morphological changes observed in
both individuals were denudation, hyperplasia, and merger of
the villi (Fig. 4b). In addition, atrophy and epithelial destruc-
tion were observed in the animal parasitized by two eimerian
species, and incipient necrosis of the apical region of the villi
was found in the other.

Discussion

Our study has documented five new eimerian species infect-
ing echimyid rodents in their natural environment.
Furthermore, our histopathological analysis showed that these
eimerians can threaten the health of the parasitized animals.
Although Eimeria spp. have a high specificity (Kogut 1990),
Duszynski and Wilber (1997) indicated that the identification
of coccidia species should be performed using all species
found in the host family. Nevertheless, to date, only a single
study was conducted in South America describing species of
Eimeria (E. proechimyi and E. caripensis) infecting the cay-
enne spiny rat (Echimyidae) P. guyanensis in Venezuela
(Arcay-de-Peraza 1964). Other studies carried out in Europe
described six species of Eimeria infecting the rodent
M. coypus: E. myopotami, E. pellucida, E. coypi, E. seideli,
E. nutriae, and E. myocastori. However, only three of these
have an informative description (Table 1).

The comparison of eimerian oocysts observed in our study
with oocysts of E. proechimyi and E. caripensis found in
Venezuela was difficult because only mean oocyst and sporo-
cyst width and length measurements were reported. In addi-
tion, it was quite impossible to visualize the morphological
characteristics described for these species due to the absence
of detailed images.

Due to the scarcity of knowledge on coccidia in echimyid
rodents, and in order to increase the number of comparisons,
we also compared our findings with those reported from other
members of the Octodontoidea superfamily, due to their phy-
logenetic proximity to the family Echimyidae. Octodontoidea
is composed by the families Abrocomyidae (including

Parasitol Res (2017) 116:2941–2956 2951



Cuscomys), Ctenomyidae, Octodontidae, Capromyidae, and
Echimyidae (including Myocastor) (Upham and Patterson
2015). Despite the great diversity of this superfamily, only
two studies have been reported describing infection by
Eimeria spp. in Ctenomyidae rodents (Lambert et al. 1988;

Gardner and Duszynski 1990), in addition to the studies on
echimyid rodents (Yakimoff 1933; Obitz and Wadowski
1937; Seidel 1954; Prasad 1960; Arcay-de-Peraza 1964).
Among the four species of Eimeria from Ctenomys spp.,
E. opimi most closely resembled E. laticeps as described in

Fig. 3 Photomicrographs of small intestine of Thrichomys fosteri from
Brazilian Pantanal naturally co-infected by two (a–d) and three (e–h)
Eimeria spp. a Oocyst in the muscular external layer (arrow). b
Hyperplasia of the epithelium of the villi (star) and endogenous stages
(oocyst, macrogamont, and immature gametocyte) in the epithelium and
lumen (arrows). c Villi with endogenous stages (arrows) without
lymphocytic infiltration. d Merging of the villi; note the fused villi,
endogenous stages (arrows) and inflammatory reaction. e
Macrogamonts in different stages of development with eosinophilic

wall-forming bodies (large arrow), microgamont containing many
microgametes (arrowhead), immature gametocytes (curve arrow), and
oocysts (thin arrow). Note the inflammatory reaction in the lamina
propria. (H&E, ×40). f Endogenous stages developing in the epithelium
of the villus and in the lamina propria (arrows). (H&E, ×20). g Intense
inflammatory reaction diffusely distributed. (H&E, ×10). hDestruction of
the villi and an intense mononuclear inflammatory reaction. Various
macrogamonts (arrows) of Eimeria spp. and an oocyst (arrowhead) can
be seen in the inflammatory reaction and in the lumen. (H&E, ×20)

2952 Parasitol Res (2017) 116:2941–2956



our study, but with differences in the oocyst wall and oocyst
residuum.

Since the late 1960s, phenotypic characters and host spec-
ificity data have been the main parameters for the description
of eimeriid coccidia (Duszynski andWilber 1997; Tenter et al.
2002). However, the development of molecular techniques
has contributed to the more precise taxonomic classification
(Hafeez et al. 2015; Tan et al. 2017). Moreover, studies have
demonstrated variation in the size of Eimeria oocysts across
their host range (Duszynski 1971; Parker and Duszynski
1986; Gardner and Duszynski 1990; Flausino et al. 2014). In
fact, polymorphism among oocysts has already been reported
in different species (e.g., Gardner and Duszynski 1990; Berto
et al. 2008; Flausino et al. 2014). This characteristic was also
observed in the present study. We detected no polymorphism
in only one new species of coccidian, E. fosteri. Our analysis
showed polymorphism in oocysts of E. nhecolandensis,
E. jansenae , E. corumbaens is , and E. la t iceps .
Polymorphism has been associated with the physiological
conditions of the hosts, as well as with environment condi-
tions (Duszynski 1971; Catchpole et al. 1975; Fayer 1980;
Joyner 1982; Parker and Duszynski 1986; Gardner and
Duszynski 1990).

In nature, some free-living individuals may accidentally
ingest oocysts from other true natural hosts, and these individ-
uals may thereby develop a simple pseudoparasitism, which is
rarely reported in the scientific literature. To avoid these mis-
takes, it is advisable to include in the description of the para-
sites at least the endogenous stages and their location in the
hosts (Levine 1988; Tenter et al. 2002; Yang et al. 2013). In
our study, endogenous developmental stages were seen in
most of the histological samples of animals that were positive
in the coprological analysis, which led us to infer that the
rodents in our study are natural hosts for the Eimeria species
described here.

Endogenous development occurred in most cases in the
epithelium of the villi of the small intestine, which is in agree-
ment with the findings of Arcay-de-Peraza (1964) on

eimerians found in echimyid rodents. However, we also found
an immature gametocyte developing in the crypts of
Lieberkühn, stages of gametogony in the lamina propria, and
an oocyst in the muscularis externa layer of the small intestine.
The development of endogenous stages of Eimeria spp. has
been reported in different animal species as occurring within
epithelial cells at the site of entry. Other studies have described
eimerian coccidians developing in both epithelial and non-
epithelial cells across the small intestine; for example, endog-
enous stages found in the lamina propria, crypts of
Lieberkühn, and endothelium of the lacteal cells (Stockdale
1976; Hammond 1982; Dubey et al. 2008).

Some samples that were positive at coprological analysis
did not display developmental endogenous stages in any of
the histological sections evaluated. In these cases, develop-
ment may have been occurring in a segment of intestine that
had not been prepared for histology, given the length of the
enteric tract. In addition, inflammatory responses, necrosis,
and destruction of the epithelium of the villi were observed
in some animals that did not show endogenous stages. In those
cases, we can hypothesize that development has occurred and
just the lesions consequent to the parasitism remained. Also,
four animals coprologically negative had endogenous stages
of a coccidian (meronts and immature gametocytes) in the
tissue, which we could not identify to genus. This finding
demonstrates that parasitism should not be defined only by
the presence or absence of oocysts in the feces, since an in-
fection could be in its initial stage and the development cycle
would have not been completed.

The parasite load in the small intestine was more intense in
co-infected animals. Thrichomys fosteri co-infected by three
Eimeria spp. (E. nhecolandensis, E. jansenae, and E. fosteri)
presented the highest number of endogenous stages and large
areas of tissue damage. By contrast, C. laticeps infected by
two morphotypes (E. nhecolandensis and E. laticeps) had
more endogenous stages than those infected by three
morphotypes (E. nhecolandensis, E. corumbaensis, and
E. laticeps), although the tissue damage was similar in both

Fig. 4 Photomicrographs of small intestine of Clyomys laticeps from the
Brazilian Pantanal naturally co-infected by Eimeria spp. a Note the
mononuclear inflammatory reaction in the lamina propria associated

with endogenous stages (arrows). b Inflammatory reaction and
epithelial hyperplasia. (H&E, ×10)

Parasitol Res (2017) 116:2941–2956 2953



individuals. A single species may be the major pathogenic
agent, but associations with others may contribute to tissue
damage, high numbers of oocysts eliminated in feces, and
disease development. Oocyst production may be increased
when co-infections occur or may remain at the same level as
in a single infection. The occurrence of associated infections
and the intensity of the lesions are dependent on the parasite
species involved and their pathogenicity as well as on factors
inherent to the host (Duszynski 1972; Marquardt 1976; Joyner
and Norton 1983; Gregory 1990; Répérant et al. 2012; Naciri
et al. 2014). Nevertheless, species interactions are important in
the pathogenesis and epidemiology of coccidia infections and
should be studied in more detail since little is known about the
pathogeny of co-infections.

Tissue damage was variable in the different combinations
of infections. The lesions observed are in agreement with
those described from coccidia infections in other animal
groups (Friend and Stockdale 1980; Gregory and Catchpole
1990; Kheirandish et al. 2014), but it is not possible to affirm
that particular morphological changes were associated with
one or another species of Eimeria since most individuals were
parasitized by more than one species. The mechanism of the
pathologic effect of the coccidia is not entirely clear; besides
the damage caused by the parasites themselves, a severe host
reaction may be more harmful (Gregory 1990). In fact, the
vascular and cellular responses of inflammation are mediated
by chemical factors that act singly, in combination, or in se-
quence, and then amplify the inflammatory response, leading
in turn to villi epithelium destruction and hyperplasia (Jubb
and Kennedy 1970; Gregory 1990), changes that were dem-
onstrated in our study. In addition, in the case of natural infec-
tion, aspects of pathogenesis such as lesion extent and inflam-
matory pattern cannot be attributed exclusively to parasitism
by eimerians, since associations with other parasites may also
be occurring. The effects of parasitism by different enteric
coccidian species on host health may be unpredictable and
may depend on individual characteristics such as age, sex,
and/or reproductive status, as well as on co-infections and
environmental conditions (Gregory 1990; Ruff and Allen
1990; Gibson et al. 2011).

Conclusion

This is the first report of infection by Eimeria spp. in the
rodents T. fosteri and C. laticeps. We identified five new
eimerian species and described the morphological,
morphometrical, and pathological aspects of simple and con-
comitant infections. Our results showed that the echimyid ro-
dents T. fosteri and C. laticeps from the Brazilian Pantanal
play an important role in the maintenance of enteric coccidian
parasites. Furthermore, this parasitism may result in important
tissue lesions.

Acknowledgements First author thanks the Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior (CAPES) by the grant
support (grant number 00.889.834/0001-08).

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict of
interest.

Ethical approval All applicable international, national, and institution-
al guidelines for the care and use of animals were followed.

All procedures performed in studies involving animals were in accor-
dance with the ethical standards of the institution or practice at which the
studies were conducted.

This article does not contain any studies with human participants
performed by any of the authors.

References

Abdon M d M, Da Silva JDSV, Pott VJ, Pott A, da Silva MP (1998)
Utilização de dados analógicos do landsat-tm na discriminação da
vegetação de parte da sub-região da Nhecolândia no Pantanal.
Pesqui Agropec Bras 33:1799–1813

Alho CJR, Lacher TE Jr, Campos ZMS, Gonçalves HC (1987)
Mamíferos da Fazenda Nhumirim, sub-região de Nhecolândia,
Pantanal do Mato Grosso do Sul: I - levantamento preliminar de
espécies. Rev Bras Zool 4:151–164. https://doi.org/10.1590/
S0101-81751987000200007

de Almeida LB, Galetti M (2007) Seed dispersal and spatial distribution
of Attalea geraensis (Arecaceae) in two remnants of Cerrado in
Southeastern Brazil. Acta Oecol 32:180–187. https://doi.org/10.
1016/j.actao.2007.04.001

Andreazzi CS, Rademaker V, Gentile R, Herrera HM, Jansen AM,
D'Andrea PS (2011) Population ecology of small rodents and mar-
supials in a semi-deciduous tropical forest of the southeast Pantanal,
Brazil. Zoologia 28:762–770. https://doi.org/10.1590/S1984-
46702011000600009

Antunes PC, Oliveira-Santos LGR, Tomas WM, Forester JD, Fernandez
FAS (2016) Disentangling the effects of habitat, food, and intraspe-
cific competition on resource selection by the spiny rat, Thrichomys
fosteri. J Mammal gyw140. https://doi.org/10.1093/jmammal/
gyw140

Arcay-de-Peraza L (1964) Tres nuevas especies de Eimeria (Protozoa,
Coccidia Eimeriidae) de roedores silvestres de Venezuela. Acta Biol
Venez 4:185–203

Avila-Pires FD, Wutke MRC (1981) Taxonomia e evolução de Clyomys
Thomas, 1916 (Rodentia, Echimyidae). Rev Bras Biol 4:529–534

Berto B, Mcintosh D, Lopes CWG (2014) Studies on coccidian oocysts
(Apicomplexa: Eucoccidiorida). Rev Bras Parasitol Vet 23:1–15

Berto BP, FlausinoW,Almeida CRR, Lopes CWG (2008) Polymorphism
of Tyzzeria parvula (Kotlán, 1933) Klimes, 1963 (Apicomplexa:
Eimeriidae) oocysts from the greylag geese Anser anser L., 1758
from two distinct sites. Rev Bras Med Vet 30:215–219

Berto BP, Luz HR, Flausino W, Teixeira-Flho WL, Ferreira I, Lopes
CWG (2011) Isosporoid coccidia (Apicomplexa: Eimeriidae) para-
sites of tanagers (Passeriformes: Thraupidae) from the Marambaia
Island, Brazil. Pesqui Veterinária Bras 31:798–805. https://doi.org/
10.1590/S0100-736X2011000900012

Bezerra AMR, de Oliveira JA, Bonvicino CR (2016) Clyomys laticeps
(Rodentia: Echimyidae). Mamm Species 48:83–90. https://doi.org/
10.1093/mspecies/sew009

Bezerra AMR, De Oliveira JOA (2010) Taxonomic implications of cra-
nial morphometric variation in the genus Clyomys Thomas, 1916

2954 Parasitol Res (2017) 116:2941–2956

https://doi.org/10.1590/S0101-81751987000200007
https://doi.org/10.1590/S0101-81751987000200007
https://doi.org/10.1016/j.actao.2007.04.001
https://doi.org/10.1016/j.actao.2007.04.001
https://doi.org/10.1590/S1984-46702011000600009
https://doi.org/10.1590/S1984-46702011000600009
https://doi.org/10.1093/jmammal/gyw140
https://doi.org/10.1093/jmammal/gyw140
https://doi.org/10.1590/S0100-736X2011000900012
https://doi.org/10.1590/S0100-736X2011000900012
https://doi.org/10.1093/mspecies/sew009
https://doi.org/10.1093/mspecies/sew009


(Rodentia: Echimyidae). J Mammal 91:260–272. https://doi.org/10.
1644/08-MAMM-A-320R1.1

Bianchi R d C, Campos RC, Xavier-Filho NL, Olifiers N, Gompper ME,
Mourão G (2014) Intraspecific, interspecific, and seasonal differ-
ences in the diet of three mid-sized carnivores in a large neotropical
wetland. Acta Theriol (Warsz) 59:13–23. https://doi.org/10.1007/
s13364-013-0137-x

Bishop IR (1974) An annotated list of caviomorph rodents collected in
North-Eastern Mato Grosso Brazil. Mammalia 38:489–502

Blanga-Kanfi S, Miranda H, Penn O, Pupko T, Debry RW, Huchon D
(2009) Rodent phylogeny revised: analysis of six nuclear genes
from all major rodent clades. BMC Evol Biol 9:71. https://doi.org/
10.1186/1471-2148-9-71

Bonvicino CR, De Oliveira JA, D’andrea PS (2008) Guia dos roedores do
Brasil, com chaves para gêneros baseadas em caracteres externos.
Centro Pan-Americano de Febre Aftosa - OPAS/OMS, Rio de
Janeiro

Cadavid GEA (1984) O clima do Pantanal Mato-Grossense. EMBRAPA-
CPAP Circular técnica 14 Corumbá: EMBRAPA-CPAP https://
www.embrapa.br/busca-de-publicacoes/-/publicacao/787712/o-
clima-no-pantanal-mato-grossense Acessed 20 June 2016

Camilo-Alves CDSEP, Mourão GDM (2009) Palms use a bluffing strat-
egy to avoid seed predation by rats in Brazil. Biotropica 42:1–7.
https://doi.org/10.1111/j.1744-7429.2009.00548.x

Carvalho CT, Bueno RA (1975) Animais causando danos em plantios
(Mammalia, Rodentia). Silvicultura 9:39–46

Catchpole J, Norton CC, Joyner LP (1975) The occurrence of Eimeria
weybridgensis and other species of coccidia in lambs in England and
Wales. Br Vet J 131:392–401

D’Elía G, Myers P (2014) On Paraguayan Thrichomys (Hystricognathi:
Echimyidae): the distinctiveness of Thrichomys fosteri Thomas,
1903. Therya 5:153–166. 10.12933/therya-14-182

Dubey JP, Wouda W, Muskens J (2008) Fatal intestinal coccidiosis in a
three week old buffalo calf (Bubalus bubalus). J Parasitol 94:1289–
1294. https://doi.org/10.1645/GE-1660.1

Duszynski DW (1971) Increase in size of Eimeria separata oocysts dur-
ing patency. J Parasitol 57:948–952

Duszynski DW (1972) Host and parasite interactions during single and
concurrent infections with Eimeria nieschulzi and E. separata in the
rat. J Protozool 19:82–88

Duszynski DW, Wilber PG (1997) A guidelines for the preparation of
species description in the Eimeriidae. J Parasitol 83:333–336

Eisenberg JF, Redford KH (1999) The Central Neotropics: Ecuador, Peru,
Bolivia

Emmons LH, Feer F (1997) Neotropical rainforest mammals: a field
guide. University Of Chicago Press, Chicago

Fayer R (1980) Epidemiology of protozoan infections: the coccidia. Vet
Parasitol 6:75–103. https://doi.org/10.1016/0304-4017(80)90039-4

Flausino G, Berto BP, Mcintosh D, Furtado TT, Teixeira-Filho WL,
Lopes CWG (2014) Phenotypic and genotypic characterization of
Eimeria caviae from guinea pigs (Cavia porcellus). Acta Protozool
53:269–276. https://doi.org/10.4467/16890027AP.14.024.1999

Friend SC, Stockdale PH (1980) Experimental Eimeria bovis infection in
calves: a histopathological study. Can J Comp Med Rev Can Med
Comp 44:129–140

Gardner SL, Duszynski DW (1990) Polymorphism of eimerian oocysts
can be a problem in naturally infected hosts: an example from sub-
terranean rodents in Bolivia. J Parasitol 76:805–811

Gibson AK, Raverty S, Lambourn DM, Huggins J, Magargal SL, Grigg
ME (2011) Polyparasitism is associated with increased disease se-
verity in Toxoplasma gondii-infected marine sentinel species. PLoS
Negl Trop Dis 5:e1142. https://doi.org/10.1371/journal.pntd.
0001142

Gregory MW (1990) Pathology of coccidial infections. In: Long PL (ed)
Coccidiosis of man and domestic animals. CRC Press, Boca Raton,
pp 236–238

Gregory MW, Catchpole J (1990) Ovine coccidiosis: the pathology of
Eimeria crandallis infection. Int J Parasitol 20:849–860. https://doi.
org/10.1016/0020-7519(90)90022-F

Hafeez MA, Shivaramaiah S, Dorsey KM, Ogedengbe ME, El-Sherry S,
Whale J, Cobean J, Barta JR (2015) Simultaneous identification and
DNA barcoding of six Eimeria species infecting turkeys using PCR
primers targeting the mitochondrial cytochrome c oxidase subunit I
(mtCOI) locus. Parasitol Res 114:1761–1768. https://doi.org/10.
1007/s00436-015-4361-y

Hammond DM (1982) Life cycles and development of coccidia. In: Long
PL (ed) The coccidia. University Park Press, Baltimore, p 45

Herrera HM, Rademaker V, Abreu UG, D'Andrea PS, Jansen AM (2007)
Variables that modulate the spatial distribution of Trypanosoma
cruzi and Trypanosoma evansi in the Brazilian Pantanal. Acta
Trop 102:55–62. https://doi.org/10.1016/j.actatropica.2007.03.001

Joyner L (1982) Host and site specificity. In: The biology of the coccidia.
University Park Press, Baltimore, pp 35–62

Joyner LP, Norton CC (1983) Eimeria mitis in mixed infections with E.
acervulina and E. brunetti in the fowl. Parasitology 86(Pt 3):381–
390. https://doi.org/10.1017/S0031182000050575

Jubb KV, Kennedy PC (1970) Pathology of domestic animals. Academic
Press, New York

Kheirandish R, Nourollahi-Fard SR, Yadegari Z (2014) Prevalence and
pathology of coccidiosis in goats in southeastern Iran. J Parasit Dis
38:27–31. https://doi.org/10.1007/s12639-012-0186-0

Kogut MH (1990) Host specificity of the coccidia. In: Long PL (ed)
Coccidiosis of man and domestic animals.1. CRC Press, Boca
Raton, pp 44–55

Lacher T (2016) Thrichomys pachyurus. The IUCN Red List of
Threatened Species 2016: e.T136245A22206322

Lacher TE, Alho CJR (1989) Microhabitat use among small mammals in
the Brazilian Pantanal. J Mammal 70:396–401. https://doi.org/10.
2307/1381526

Lambert CR, Gardner SL, Duszynski DW (1988) Coccidia
(Apicomplexa: Eimeriidae) from the subterranean rodent
Ctenomys opimus Wagner (Ctenomyidae) from Bolivia, South
America. J Parasitol 74:1018–1022

Lessa LG, Costa FN (2009) Food habits and seed dispersal by
Thrichomys apereoides (Rodentia: Echimyidae) in a Brazilian
Cerrado reserve. Mastozoología Neotrop 16:459–463

Levine ND (1988) The protozoan phylum Apicomplexa. CRC Press,
Boca Raton

Mares MA, Ojeda RA (1982) Patterns of diversity and adaptation in
South American hystricognath rodents. Mammalian Biology in
South America, South America, pp 393–432

MarquardtWC (1976) Some problems of host and parasite interactions in
the Coccidia. J protozool 23:287–290

Moolenbeek C, Ruitenberg EJ (1981) The BSwiss roll^: a simple tech-
nique for histological studies of the rodent intestine. Lab Anim 15:
57–59. https://doi.org/10.1258/002367781780958577

Naciri M, Fort G, Briant J, Duperray J, Benzoni G (2014) Incidence of
single and mixed infections with Eimeria kofoidi, E. caucasica and
E. legionensis on the health of experimentally infected red-legged
partridges (Alectoris rufa). Vet Parasitol 205:77–84. https://doi.org/
10.1016/j.vetpar.2014.06.013

Norton CC, Joyner LP (1981) Eimeria acervulina and E. mivati: oocysts,
life-cycle and ability to develop in the chicken embryo. Parasitology
83(Pt2):269–279

Obitz K, Wadowski S (1937) Eimeria coypi n. sp. parozyt nutrii
Myocastor coypu (Mol). Wydz Wet 1:98–99

Oliveira JA, Bonvicino CR (2011) Ordem Rodentia. In: Mamíferos do
Brasil, 2nd edn. Londrina, pp 358–415

Parker BB, Duszynski DW (1986) Polymorphism of eimerian oocysts: a
dilemma posed by working with some naturally infected hosts. J
Parasitol 72:602–604

Parasitol Res (2017) 116:2941–2956 2955

https://doi.org/10.1644/08-MAMM-A-320R1.1
https://doi.org/10.1644/08-MAMM-A-320R1.1
https://doi.org/10.1007/s13364-013-0137-x
https://doi.org/10.1007/s13364-013-0137-x
https://doi.org/10.1186/1471-2148-9-71
https://doi.org/10.1186/1471-2148-9-71
https://www.embrapa.br/busca-de-publicacoes/-/publicacao/787712/o-clima-no-pantanal-mato-grossense
https://www.embrapa.br/busca-de-publicacoes/-/publicacao/787712/o-clima-no-pantanal-mato-grossense
https://www.embrapa.br/busca-de-publicacoes/-/publicacao/787712/o-clima-no-pantanal-mato-grossense
https://doi.org/10.1111/j.1744-7429.2009.00548.x
https://doi.org/10.12933/therya-14-182
https://doi.org/10.1645/GE-1660.1
https://doi.org/10.1016/0304-4017(80)90039-4
https://doi.org/10.4467/16890027AP.14.024.1999
https://doi.org/10.1371/journal.pntd.0001142
https://doi.org/10.1371/journal.pntd.0001142
https://doi.org/10.1016/0020-7519(90)90022-F
https://doi.org/10.1016/0020-7519(90)90022-F
https://doi.org/10.1007/s00436-015-4361-y
https://doi.org/10.1007/s00436-015-4361-y
https://doi.org/10.1016/j.actatropica.2007.03.001
https://doi.org/10.1017/S0031182000050575
https://doi.org/10.1007/s12639-012-0186-0
https://doi.org/10.2307/1381526
https://doi.org/10.2307/1381526
https://doi.org/10.1258/002367781780958577
https://doi.org/10.1016/j.vetpar.2014.06.013
https://doi.org/10.1016/j.vetpar.2014.06.013


Pellerdy L (1957) On the homonymy of Eimeria fulva Farr, 1953 and
Eimeria fulva Seidel, 1954. J Parasitol 43:591

Pessôa LM, Tavares WC, Neves ACA, Silva ALG (2015) Genus
Thrichomys E.- L. Trouessart, 1880. Mamm South Am 2:989–999

Porfirio G, Foster VC, Fonseca C, Sarmento P (2016) Activity patterns of
ocelots and their potential prey in the Brazilian Pantanal. Mamm
Biol 81:511–517. https://doi.org/10.1016/j.mambio.2016.06.006

Prasad H (1960) Two new species of coccidia of the coypu. J Protozool 7:
207–210. https://doi.org/10.1111/j.1550-7408.1960.tb00731.x

Redford KH, Eisenberg JF (1992) Mammals of the Neotropics. Vol. 2.
The Southern Cone: Chile, Argentina, Uruguay, Paraguay.
University of Chicago Press, Chicago

Répérant JM, Dardi M, Pagès M, Thomas-Hénaff M (2012)
Pathogenicity of Eimeria praecox alone or associated with
Eimeria acervulina in experimentally infected broiler chickens.
Vet Parasitol 187:333–336. https://doi.org/10.1016/j.vetpar.2011.
12.009

Ruff MD, Allen PC (1990) Pathophysiology. In: Long PL (ed)
Coccidiosis of man and domestic animals. CRC Press, Boca
Raton, pp 263–280

Seidel E (1954) Einiges iiher neue Parasiten funde beim Sumpfbiber.
Deut Pdatiwzucht 28:190–191

Simões R, Gentile R, Rademaker V, D'Andrea PS, Herrera HM, Freitas T,
Lanfredi R, Maldonado A Jr (2010) Variation in the helminth com-
munity structure of Thrichomys pachyurus (Rodentia: Echimyidae)
in two sub-regions of the Brazilian Pantanal: the effects of land use
and seasonality. J Helminthol 84:266–275. https://doi.org/10.1017/
S0022149X09990629

Solano-Gallego L, Fernández-Bellon H,Morell P, Fondevilla D, Alberola
J, Ramis A, Ferrer L (2004) Histological and immunohistochemical
study of clinically normal skin of Leishmania infantum-infected
dogs. J Comp Pathol 130:7–12. https://doi.org/10.1016/S0021-
9975(03)00063-X

Soriano BMA and Alves MJM (2005) Boletim agrometereológico ano
2002 para a sub-região da Nhecolândia, Pantanal, Mato Grosso do
Sul, Brasil. Corumbá:EMBRAPA-CPAP. http://www.cpap.
embrapa.br/publicacoes/online/DOC76.pdf. Acessed 20 June 2016

Stockdale PHG (1976) Schizogony and gametogony of Eimeria zuernii
(Rivolta, 1878) Martin, 1909. Vet Parasitol 1:367–376. https://doi.
org/10.1016/0304-4017(76)90039-X

Tan L, Li Y, YangX, KeQ, LeiW,Mughal MN, Fang R, Zhou Y, Shen B,
Zhao J (2017) Genetic diversity and drug sensitivity studies on
Eimeria tenella field isolates from Hubei Province of China.
Parasit Vectors 10:137. https://doi.org/10.1186/s13071-017-2067-y

Tenter AM, Barta JR, Beveridge I, Duszynski DW,Melhorn H, Morrison
DA, Thompson RC, Conrad PA (2002) The conceptual basis for a
new classification of the coccidia. Int J Parasitol 32:595–616. https://
doi.org/10.1016/S0020-7519(02)00021-8

UphamNS, Patterson BD (2012) Diversification and biogeography of the
Neotropical caviomorph lineage Octodontoidea (Rodentia:
Hystricognathi). Mol Phylogenet Evol 63:417–429. https://doi.org/
10.1016/j.ympev.2012.01.020

Upham NS, Patterson BD (2015) Evolution of the caviomorph rodents: a
complete phylogeny and timetree of living genera. In: Biology of
caviomorph rodents: diversity and evolution. SAREM Series A,
Buenos Aires, pp 63–120

Verçosa BLA, Melo MN, Puerto HL, Mendonça IL, Vasconcelos AC
(2012) Apoptosis, inflammatory response and parasite load in skin
of Leishmania (Leishmania) chagasi naturally infected dogs: a
histomorphometric analysis. Vet Parasitol 189:162–170. https://
doi.org/10.1016/j.vetpar.2012.04.035

Vieira AS, Rosinha GMS, Vasconcellos SA, de Moaris ZM, Viana RC,
Oliveira CE, Soares CO, Araújo FR, Mourão GM, Bianchi RC,
Olifiers N, Rademaker V, Rocha FL, Pellegrin AO (2013)
Identificação de mamíferos silvestres do Pantanal sul-mato-
grossense portadores de Leptospira spp. Ciência Anim Bras 14:
373–380. https://doi.org/10.5216/cab.v14i3.17147

Vieira MV (1997) Dynamics of a rodent assemblage in a cerrado of
southeast Brazil. Rev Bras Biol 57:99–107

Vieira MV (2003) Seasonal niche dynamics in coexisting rodents of the
Brazilian Cerrado. Stud Neotrop Fauna Environ 38:7–15. https://
doi.org/10.1076/snfe.38.1.7.14034

Wolf RW, Aragona M, Muñoz-Leal S, Pinto LB, Melo AL, Braga IA,
Costa JS, Martins TF, Marcili A, Pacheco RC, Labruna MB, Aguiar
DM (2016) Novel Babesia and Hepatozoon agents infecting non-
volant small mammals in the Brazilian Pantanal, with the first record
of the tick Ornithodoros guaporensis in Brazil. Ticks Tick Borne Dis
7:449–456. https://doi.org/10.1016/j.ttbdis.2016.01.005

Yakimoff WL (1933) Die Coccidiose der Nutrien. Landw Pelztierz 4:
189–190

Yang R, Brice B, Bennett MD, Eliott A, Ryan U (2013) Novel Eimeria
sp. isolated from a King’s skink (Egernia kingii) in Western
Australia. Exp Parasitol 133:162–165. https://doi.org/10.1016/j.
exppara.2012.11.004

Zucco CA, Mourão GM (2009) Low-cost global positioning system har-
ness for pampas deer. JWildlManag 73:452–457. https://doi.org/10.
2193/2007-492

2956 Parasitol Res (2017) 116:2941–2956

https://doi.org/10.1016/j.mambio.2016.06.006
https://doi.org/10.1111/j.1550-7408.1960.tb00731.x
https://doi.org/10.1016/j.vetpar.2011.12.009
https://doi.org/10.1016/j.vetpar.2011.12.009
https://doi.org/10.1017/S0022149X09990629
https://doi.org/10.1017/S0022149X09990629
https://doi.org/10.1016/S0021-9975(03)00063-X
https://doi.org/10.1016/S0021-9975(03)00063-X
http://www.cpap.embrapa.br/publicacoes/online/DOC76.pdf
http://www.cpap.embrapa.br/publicacoes/online/DOC76.pdf
https://doi.org/10.1016/0304-4017(76)90039-X
https://doi.org/10.1016/0304-4017(76)90039-X
https://doi.org/10.1186/s13071-017-2067-y
https://doi.org/10.1016/S0020-7519(02)00021-8
https://doi.org/10.1016/S0020-7519(02)00021-8
https://doi.org/10.1016/j.ympev.2012.01.020
https://doi.org/10.1016/j.ympev.2012.01.020
https://doi.org/10.1016/j.vetpar.2012.04.035
https://doi.org/10.1016/j.vetpar.2012.04.035
https://doi.org/10.5216/cab.v14i3.17147
https://doi.org/10.1076/snfe.38.1.7.14034
https://doi.org/10.1076/snfe.38.1.7.14034
https://doi.org/10.1016/j.ttbdis.2016.01.005
https://doi.org/10.1016/j.exppara.2012.11.004
https://doi.org/10.1016/j.exppara.2012.11.004
https://doi.org/10.2193/2007-492
https://doi.org/10.2193/2007-492

	New...
	Abstract
	Introduction
	Material and methods
	Study area and sampling procedures
	Coprological analysis
	Histological analysis
	Data analysis

	Results
	Thrichomys fosteri
	Clyomys laticeps
	Species descriptions
	Eimeria nhecolandensis n. sp.
	Eimeria jansenae n. sp.
	Eimeria fosteri n. sp.
	Eimeria corumbaensis n. sp.
	Eimeria laticeps n. sp.

	Epidemiological data
	Histopathological analysis
	Host: Thrichomys fosteri
	Host: Clyomys laticeps


	Discussion
	Conclusion
	References