ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
HELMINTHS OF THE NUTRIA MYOCASTOR COYPUS (RODENTIA: MYOCASTORIDAE) IN THE
FOREST OF ARAUCARIAS, BRAZIL
HELMINTOS DE NUTRIA MYOCASTOR COYPUS (RODENTIA: MYOCASTORIDAE) EN LA MATA
DE ARAUCARIAS, BRASIL
1
Parasitology Laboratory, Federal University of the Fronteira Sul, Campus Realeza, PR, Brazil.
2 Laboratory for Parasitic Diseases of Animals, Department of Preventive Veterinary Medicine and Animal Reproduction,
School of Agrarian and Veterinarian Sciences, Paulista State University (UNESP).
*
Corresponding author: Fagner Luiz da Costa Freitas, Rua Edmundo Gaievski 1000, Acesso PR 182 km. CEP 85770-000,
Realeza, PR, Brazil. Phone: +55(46)3543 - 8377
E-mail: fagner.freitas@uffs.edu.br
1 2 2
Danise Benati ; Marcela Figuerêdo DuarteMoraes ; Estevam Guilherme Lux Hoppe ; José Hairton ;
2
Tebaldi
1,*
Iucif Abrão Fagner Luiz da Costa Freitas
1
Nascif Júnior &
ABSTRACT
Keywords: Brazilian Araucaria Forest – Helminth fauna – Indicators of infection – Neotropical Region – Rodents – Wild
The nutria (Myocastor coypus Molina, 1782) can significantly affect ecosystems, resulting in adverse
socioeconomic and health consequences for humans and animals. The present study identified the
helminth fauna of M. coypus from a region of Mata de Araucaria in the State of Paraná, Brazil. Three free-
living adult males that were found dead in the rural zone of this municipality were used. Anatomical
segments from the digestive tract, respiratory tract, heart and kidneys were sieved and the material was
fixed in Railliet and Henry solution. The helminths were identified and counted and the infection
indicators were analyzed descriptively. A total of 341 helminths was collected belonging to the Orders and
Families Trichostrongylidea: Heligmonelidae; Cestoda: Hymenolepididae; and Digenea: Notocotylidae.
The prevalence, parasite intensity and abundance of the two first helminth species were observed in the
animals evaluated. The region of study represents a new locality record for the three species diagnosed.
Myocastor coypus is a new registered host for Rondentolepis octocoronata Linstow, 1879 in Brazil. These
data contribute to the knowledge of the helminth fauna of free-living M. coypus in the Brazilian Araucaria
Forest region.
Neotropical Helminthology
377
Neotropical Helminthology, 2017, 11(2), jul-dic: 377-386
INTRODUCTION
378
RESUMEN
Palavras clave: Helmintofauna – indicadores de infección – Mata de Araucária Brasileña – Región Neotropical – Roedores – salvaje
La nutria (Myocastor coypus Molina, 1782) puede afectar significativamente los ecosistemas, resultando
en consecuencias socioeconómicas y de salud adversas para los seres humanos y los animales. El presente
trabajo identificó la helmintofauna de M. coypus oriundos de una región de Mata de Araucária en el Estado
de Paraná, Brasil. Se utilizaron tres animales de vida libre, adultos, machos, encontrados muertos en el
área rural del municipio de Dos Vizinhos-PR. Los segmentos anatómicos del tracto digestivo,
respiratorio, cardíaco y renal fueron tamizados y el contenido fijado en solución de Railliet y Henry.
Después de la identificación y recuento de los helmintos, se elaboró un análisis descriptivo de los
indicadores de infección. Se recogieron 341 helmintos, pertenecientes al Orden y Familia:
Trichostrongylidea: Heligmonelidae, Cestoda: Hymenolepididae y Digenea: Notocotylidae. La
prevalencia, intensidad y abundancia parasitaria media de las dos primeras especies de helmintos fueron
las mayores observadas en los animales evaluados. La región de estudio representa un nuevo registro de
localidad para las tres especies diagnosticadas. Myocastor coypus es un nuevo huésped registrado para
Rondentolepis octocoronata Linstow, 1879, en Brasil. Estos datos contribuyen al conocimiento de la
helmintofauna de M. coypus de vida libre en la región de la Mata de Araucária Brasileña.
being part of this ecosystem. Predominates the
subtropical climate, which presents/screens
rigorous winters and hot summers, with rainfall
indexes relatively high and well distributed during
the year (Basso, 2010, IBGE, 2012).
The species of parasites and indicators of parasitic
infection (prevalence, abundance, mean intensity
and variation of intensity) observed in M. coypus
vary according to the geographical region they
inhabit, it is considered that cold temperatures are a
limiting factor for the geographical distribution of
the populations of coypus (Baroch et al., 2002).
Microbial and endoparasite infections can cause
considerable mortality, especially in times of high
population density. Endoparasites rarely kill their
host but may reduce the ability of coypus
populations to slow population growth (Sheffels,
2013; Zanzani et al., 2016).
The helminth fauna of M. coypus has been
described in studies conducted in North America,
Europe and some countries of South America.
Cases of natural infection with the following have
been described: Graphidioides myocastoris
(Babero, 1979), Trichuris myocastoris (Baruš et al.
1975), Dipetalonema sp. (Grassi, 1890),
Hippocrepis myocastoris (Cabello & Kinoed,
1979), Rodentolepis sp. (Yamaguti, 1959),
Heligmosomoides sp. (Büchner, 1889),
Coypus (Myocastor coypus Molina, 1782) are
rodents belonging to the family Capromyidae,
natives to the South America(Woods et al., 1992;
Carter & Leonard, 2002). They live on the banks of
rivers and lakes and are herbivores with nocturnal
habits (Gosling & Baker, 1981; Rodrigues &
Ferigolo, 2004). They are considered opportunistic
animals, known to use different food sources,
depending on the vegetation present in the region,
are general herbivores capable of consuming up to
25% of their body mass daily, using both aquatic
and terrestrial vegetation (Gosling & Baker, 1981;
Christen, 1978; Guichón et al., 2003). They cause
adverse impacts on the ecosystem such as
disruption of ecological processes, competition
with native species for resources and reduction of
biodiversity (Elton, 1958; Mack & D'antonio,
1998).
The Araucaria forest, a typical phytophysiognomy
of the Southern Region of Brazil and also found in
the highest relief points of the Southeastern
Region, whose characteristic species is the Paraná
Pine (Araucaria angustifolia), (IBGE, 2012)
presents remnants dispersed in small capons, some
of which are still conserved characteristics of
primary forest with a flora of Pteridophytes own
Neotropical Helminthology, 2017, 11(2), jul-dic Benati et al.
379
Neotropical Helminthology, 2017, 11(2), jul-dic Helminths of the Myocastor coypus
Strongyloides myopotami (Artigas & Pacheco,
1933), Trichuris sp. (Roederer, 1761), Capillaria
hepatica (Bancroft, 1893), Trichostrongylus
colubriformis (Leiper, 1909), Trichostrongylus sp.
(Leiper, 1909), Trichostrongylus duretteae
(Leiper, 1909), Rodentolepis avetjanae
(Akhumian, 1956), Anoplocephala sp. (Goeze,
1782), Hymenolepis octocoronata (Linstow,
1879), Dicrocoelium lanceolatum (Braun, 1902),
Dicrocoelium sp. (Braun, 1902) and Fasciola
hepatica (Linnaeus, 1758) (Wenzel, 1982; Silva et
al., 2007; El-Kouba, et al., 2009; Guerreiro et al.,
2014). In Brazil, infection by Hippocrepis
fuelleborni (Travassos & Vogelsang, 1930) and
Trichuris travassoi (Linnaeus , 1771) has been
described, along with infection by the protozoa
Giardia sp. (Kunstler, 1882), Cryptosporidium sp.
(Levine, 1984) and Cystoisospora sp. (Frenkel,
1977) (Silva et al., 2007; Sheffels & Sytma, 2007;
Rocha et al., 2012).
Thus, because of the need to expand knowledge
regarding helminth parasites of Myocastor coypus
in Brazil, the present study had the objective of
identifying the helminth fauna of coypus from the
region of Forest in Araucaria.
Study area
The research was conducted in the Araucarias
Forest, located in the southwestern region of the
state of Paraná, between the parallels 25° 44 'and
5°S and the meridians 53°3' and 31º W, in the
municipality of Dois Vizinhos, Paraná, Brazil (Fig.
1).
The Subtropical Forest, also known as Forest in the
Araucaria, Pine tree of Paraná among other names,
has preference in areas of higher altitude (above
500m), where the temperature is milder. Although
Araucaria predominates, other vegetables such as
Imbuia and Mate herb are also associated with it.
Currently it is reduced to approximately 3% of the
initial area (IBGE, 2012).
Animals
In the period from 2013 to 2014, three free-living
male adults (M. coypus) were found dead in the
rural area of the municipality of Dois Vizinhos,
Southwest of the State of Paraná, and donated by
rural producers to the Laboratory of Parasitology
of the Federal University of the Fronteira Sul,
Campus Realeza-PR.
Parasitological methods
The animals were stored in a freezer at -20 °C until
the time of necropsy. Then the specimens were
thawed at room temperature. Necropsies were
performed at the Laboratory of Parasitology of the
Federal University of the Fronteira Sul, Campus
Realeza - PR. The anatomical segments of the
digestive tract (esophagus, stomach, small
intestine and large intestine), along with the
trachea, heart, lung, liver, pancreas and kidneys,
were sectioned separately and the material
obtained was sieved using a Tyler 100 mesh and
was fixed in Railliet & Henry solution, for
subsequent identification of the helminths with the
aid of a stereoscopic microscope.
The helminths were diaphanized in 80% acetic acid
solution and, if necessary, diaphanized in beech
creosote for studies in optical microscopy on
temporary slides. For each species, at least 10
specimens of each sex were measured. In case of
species with few specimens, all specimens
obtained were evaluated. To obtain morphometric
and morphological characteristics, we used a clear
camera equipped microscope and the images of the
specimens obtained with an Olympus BX-51
microscope equipped with a Q-Color 3 digital
camera and the images were processed by the
image analyzer software Image-Pro Plus 4.0 ,
The taxonomic identification of helminths was
made following keys proposed by Linstow (1879),
Travassos & Vogelsang (1930) and Artigas &
Pacheco (1933). After identification and counting
of the helminths, a descriptive analysis of the
infection indicators according to Bush et al. (1997).
Specimens of each species diagnosed were
deposited in the collection of the Laboratory of
Parasitology of the Federal University of the
Fronteira Sul, Campus Realeza-PR.
Ethical issues
This study was approved through the Sistema de
Autorização e Informação em Biodiversidade -
SISBIO (Protocol N°. 45.720) and the Ethics
Committee for Animal Use UFFS/Realeza
(Protocol N°. 23205.005173/2014-81).
MATERIALS AND METHODS
(Adapted from WWF, 2012 and Government of the state of Paraná, 2017).
Figure 1. Map representing the Araucaria Forest in Brazil, highlighting the Municipality of Dois Vizinhos, PR – Brazil.
Neotropical Helminthology, 2017, 11(2), jul-dic
diagnosed. Still, M.coypus is a new registered host
for R. octocoronata in Brazil.
Pudica maldonadoi Artigas & Pacheco, 1933
(Trichostrongyloidea: Heligmonelidae)
Thin, spiraled nematode was attenuated anterior
ending; mouth small, with poorly visible papillae.
Thick cuticle along the body was transversal
striated and in cross-section, at midbody 12
cuticular crests with uniform striations may be
observes. The male body length is 4.98 mm ± 0.40,
width 0.069 mm ± 8.5. The cephalic vesicle is
0.074 mm ± 0.0095, excretory pore is 0.55 mm ±
0.17 (from the anterior ending). Long, and the
esophagus is 0.43 mm ± 0.012, long and the nerve
ring is 0.21 mm ± 0.022. From the anterior ending
the copulatory pouch is asymmetrical, and the thin
spicules are thin, is 0.46 mm ± 0.1 in length. The
female is longer than the male, with total length of
10.5 mm ± 0.06, and 0.11 mm ± 0.008 wide. The
vulva is at 0.13 m ± 0.023, from tail anus. Distance
from the anus to the posterior extremity is 0.05 mm
± 0.026, with simple genital apparatus and acute
conical tail, without a terminal spine. The caudal
RESULTS
A total of 341 specimens of three species
representing the groups Digenea, Cestoidea and
Nematoda were identified. The three species that
were identified as parasitizing M. coypus in the
st ud y ar ea w ere P u d i c a m a l d o n a d o i
(Trichostrongylidea: Heligmonelidae ),
R o d e n t o l e p i s o c t o c o ro n a t a ( Cesto da :
Hymenolepididae) and Hippocrepis fuelleborni
(Diginea: Notocotylidae) (Table 1).
The nematode P. maldonadoi was the most
abundant species among the samples, with the
higher prevalence, mean intensity and abundance
rates. Although it presented the same prevalence as
the cestode R. octocoronata, it was observed that
the latter presented abundance and mean intensity
lower than the former. The digenetic H. fuelleborni
was the species with the lowest descriptions of
infections among the animals evaluated.
The region of study represents a new record of
locality for the three species of helminths
380
Benati et al.
Neotropical Helminthology, 2017, 11(2), jul-dic Helminths of the Myocastor coypus
extremity presents an intumescent cuticle at the
level of the vulva that forms dorsal a foreskin-
shaped fold (Fig. 2).
Taxonomic summary:
Host: Myocastor coypus
Location of infection: Small intestine
Locality: Dois Vizinhos, state of Paraná, Brazil
Prevalence: 100%
Abundance: 65.3 parasites/host
Mean intensity: 65.3 parasites/host
Variation of intensity:11 to 54 parasites
Rodentolepis octocoronata Linstow, 1879
(Cestoidea, Hymenolepididae)
Scolex was four oval suction cups and a face with
eight prominent hooks, meander 0.062 mm in
lenght. The cirrus pouch is perpendicular is the
proglottids. The cirrus is long and tangled. Each
proglottids has a uterus and three well-developed
testicles (Fig. 3).
Taxonomic summary:
Host: Myocastor coypus
Figure 2. Morphology of Pudica maldonadoi: A) Copulatory bursa of the male; B) Anterior extremity; C) Cross-section through
the synlophe. Scale bar: A and C: 50µm, B: 100µm.
381
Table 1. Helminth species and descriptor of infection indicators identied in three adults coypus (Myocastor coypus)
that originated from the municipality of Dois Vizinhos, state of Paraná, Brazil.
Helminths Site of
infection Prevalence
Abundance Mean
intensity
Range of
intensity No
Nematoda
Trichostrongyloidea
Pudica maldonadoi
Small
intestine 100 65.3 65.3 11 -
54
196
Cestoda
Hymenolepididae
Rodentolepis octocoronata
Small
intestine 100 37 37 24 -
55
111
Digenea
Notocotylidae
Hippocrepis fuelleborni
Large
intestine
66.6 8 2 2 -12 34
Location of infection: Small intestine
Locality: Dois Vizinhos, state of Paraná, Brazil
Prevalence: 100%
Abundance: 37 parasites/host
Mean intensity: 37 parasites/host
Variation of intensity: 24 to 55 parasites
Hippocrepis fuelleborni Travassos & Vogelsang,
1930 (Digenea, Notocotylidae)
Elongated body was 3.02 mm ± 1.14 in length, the
anterior with is 0.33 mm ± 0.09, becoming widow
at middle is 0.47 mm ± 0.19, and posterior portion
of 0.55 mm ± 0.16. The oral sucker is 0.27 ± 0.08 x
0.29 ± 0.09 mm was the presence of ventral
papillae. Pharynx absent and esophagus short.
Male reproductive system with presence of
elongated cirrus pouch, with small spines
measuring 0.49 mm ± 0.16 in length. The testicules
are lobates and displace diagonary. The left testicle
is 0.23 ± 0.14 x 0.22 ± 0.16 mm and the right
testicle is 0.21 ± 0.18 x 0.25 ± 0.15 mm. The
insertion ceca join together in the end portion
between the testicles. The female reproductive
system is formed by a well-developed uterus and
pre-testicular ovary of 0.17 ± 0.13 x 0.16 ± 0.14
mm (Fig. 4).
Taxonomic summary:
Host: Myocastor coypus
Location of infection: Large intestine
Locality: Dois Vizinhos, state of Paraná, Brazil
Prevalence: 66.6%
Abundance: 8 parasites/host
Mean intensity: 12 parasites/host
Variation of intensity: 2 to 22 parasites
Neotropical Helminthology, 2017, 11(2), jul-dic
Figure 3. Morphology of Rodentolepis octocoronata: A) Presence of eight thorns; B) Immature proglottid. Scale bar: A: 50µm,
B: 250 µm.
382
Benati et al.
Neotropical Helminthology, 2017, 11(2), jul-dic Helminths of the Myocastor coypus
Figure 4. Hippocrepis fuelleborni: A) and C) Posterior extremity reproductive system; B) Anterior extremity. Scale bar: A and
B: 300µm, C: 500 µm.
383
Artigas, P & Pacheco, G. 1933. Longistriata
m a l d o n a d o i n . s p . ( N e m a t o d a :
Trichostrongylidae) parasite of Myocastor
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Babero, BB & Lee, J W. 1961. Studies on the
helminths of nutria, Myocastor coypus
(Molina), in Louisiana with check-list of
other worm parasites from this host. Journal
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Poché, RM. 2002. Nutria (Myocaster
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BIBLIOGRAPHIC REFERENCES
Graphidioides myocastoris and Trichuris
myocastoris. However, in Argentina, the most
prevalent digenean found in coypus was Fasciola
hepatica (Artigas & Pacheco, 1933). It is important
to emphasize that the helminths identified in M.
coypus in the municipality of Dois Vizinhos,
Paraná, were specific parasites for this host. There
are still no records in the literature regarding the
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species of mammals.
The helminthological fauna of M. coypus reported
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digeneans, 21 species of cestodes, one species of
Acanthocephala and 31 species of nematodes
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This study describes the helminths of coypus
(Myocastor coypus) in the municipality of Dois
Vizinhos, Paraná, Brazil. These data contribute to
the knowledge of the helminth fauna of wild M.
coypus in the primary habitat of this species and
register the first occurrence of Rodentolepis
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Neotropical Helminthology, 2017, 11(2), jul-dic
DISCUSSION
The nematode P. maldonadoi was the most
abundant species among the samples, with the
higher prevalence, mean intensity and abundance
rates. Although it presented the same prevalence as
the cestode R. octocoronata, it was observed that
the latter presented lower abundance and mean
intensity. The digenean H. fuelleborni was the
species with the lowest descriptors of infection
among the animals evaluated. The region of study
represents a new locality record for the three
parasite species diagnosed. Nevertheless,
M.coypus is a new host record for R. octocoronata.
Higher prevalence of nematodes than of other
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(Martino et al., 2012). Most cestode parasites of
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pathogenic towards their hosts. However, because
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mollusks or fish form intermediate hosts, coypus
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helminths, consequent to their habitat and diet
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