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Neotropical Helminthology
Neotropical Helminthology, 2024, vol. 18 (2), 187-196
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
A NEW GEOGRAPHIC DISTRIBUTION AND MORPHOLOGIC REVISION
OF
MASTOPHORUS MURIS
(NEMATODA: SPIRURIDA), A PARASITE
OF THE STOMACH OF
RATTUS NORVEGICUS
IN RIO DE JANEIRO, BRAZIL
UNA NUEVA DISTRIBUCIÓN GEOGRÁFICA Y REVISIÓN MORFOLÓGICA
DE
MASTOPHORUS MURIS
(NEMATODA: SPIRURIDA), UN PARÁSITO
DEL ESTÓMAGO DE
RATTUS NORVEGICUS
EN RÍO DE JANEIRO, BRASIL
Ana Júlia Rapozo Dias
1
; Beatriz Elise de Andrade Silva
2
; Teresa Cristina Bergamo do Bomf m
1
;
Arnaldo Maldonado Júnior
3
& Raquel de Oliveira Simões
1
*
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.62429/rnh20242181846
Este artículo es publicado por la revista Neotropical Helminthology de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico
Villarreal, Lima, Perú auspiciado por la Asociación Peruana de Helmintología e Invertebrados Af nes (APHIA). Este es un artículo de acceso abierto,
distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/
deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original.
1
Universidade Federal Rural do Rio de Janeiro (UFRRJ). Km 07, Zona Rural, BR-465, 23890-000, Seropédica, RJ, Brasil.
2
Universidade do Estado do Rio de Janeiro (UERJ). Rua São Francisco Xavier, 524, 20550-013, Rio de Janeiro, RJ, Brasil.
3
Instituto Oswaldo Cruz (IOC). FIOCRUZ. Avenida Brasil, 4365, 21040-360. Rio de Janeiro, RJ, Brasil.
* Corresponding author: raquel83vet@gmail.com
Ana Júlia Rapozo Dias:
https://orcid.org/0009-0002-8510-9728
Beatriz Elise de Andrade Silva:
https://orcid.org/0000-0001-7866-5369
Teresa C. B. Bomf m:
https://orcid.org/0000-0002-6741-0202
Arnaldo Maldonado Júnior:
https://orcid.org/0000-0003-4067-8660
Raquel de Oliveira Simões:
https://orcid.org/0000-0001-5130-3341
ABSTRACT
T is study provides a comprehensive morphological redescription of
Mastophorus muris
Gmelin, 1790, a spirurid
nematode, based on specimens collected from
Rattus norvegicus
Berkenhout, 1769 in Nova Iguaçu municipality, Rio de
Janeiro, Brazil. Employing optical and scanning electron microscopy, we detailed morphological characteristics, including
previously unreported features such as a pair of ad-cloacal papillae and details of pseudolabia teeth. Additionally, we report
a new geographical distribution for
M. muris
in Brazil. T e low prevalence of
M. muris
observed in this study highlights
the potential impact of anthropic changes on parasite distribution. Further investigations, including molecular analyses,
are necessary to elucidate the taxonomic complexity and host-parasite relationships within the genus
Mastophorus
.
Keywords:
Morphology – Nematoda – Rodents – Scanning electron microscopy – Spirurida – Taxonomy
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RESUMEN
Este estudio proporciona una redescripción morfológica integral de
Mastophorus muris
Gmelin, 1790
,
un nematodo
del orden Spirurida, basada en especímenes recolectados de
Rattus norvegicus
Berkenhout, 1769 en el municipio de
Nova Iguaçu, Río de Janeiro, Brasil. Empleando microscopía óptica y electrónica de barrido, detallamos características
morfológicas, incluidas características no reportadas previamente, como un par de papilas adcloacales y detalles de dientes
del pseudolabio. Además, informamos de una nueva distribución geográfca para
M. muris
en Brasil. La baja prevalencia
de
M. muris
observada en este estudio resalta el impacto potencial de los cambios antropogénicos en la distribución del
parásito. Se necesitan investigaciones adicionales, incluidos análisis moleculares, para dilucidar la complejidad taxonómica
y las relaciones huésped-parásito dentro del género
Mastophorus
.
Palabras clave:
Microscopía electrónica de barrido – Morfología – Nemátodos – Roedores – Spirurida – Taxonomía
INTRODUCTION
Te Spirocercidae Chitwood & Wehr, 1932 family
comprises three subfamilies with a global distribution:
Spirocercinae Chitwood & Wehr, 1932, encompassing
eight genera, parasitizes mammals and birds; Ascaropsinae
Alicata & McIntosh, 1933 including ten genera infecting
mammals and lastly, Mastophorinae Quentin, 1970,
containing the single genus
Mastophorus
Diesing, 1853
found in murid and microtid rodents, as well as various
accidental hosts (Souza, 1980; Anderson, 2009; Bain
et
al
., 2014). Actually, there is only one species belonging
to this genus:
Mastophorus muris
Gmelin, 1790. Tis
species was initially described as
Ascaris muris
, a parasite
of the rat’s stomach, by Gmelin (1790), lacking detailed
description or illustrations.
Tis nematode parasitizes the stomach of the defnitive
hosts and presents an indirect life cycle with insects of the
order Orthoptera, Diptera, Coleoptera and Siphonaptera
acting as intermediate hosts (Grzybek
et al
., 2014). Insects
get infected ingesting larvated eggs eliminated in the feces
of the rats (Grzybek
et al
., 2014). Te larva of frst stage
(L1) releases and invades the insect tissues developing
into larva of third stage (L3), the infective stage for the
defnitive host (Laferty
et al
., 2010). Te defnite host
be infected by the ingestion of the intermediate host with
infective larvae. Eggs eliminated in the feces of rodents are
larval, ellipsoid-shaped, smooth, and thick-membraned
(Rojas & Digiani, 2003).
Inconsistencies in the literature regarding
M. muris
descriptions and classifcation motivated this study. We
employed optical and scanning electron microscopy to
provide a comprehensive morphological redescription
of the parasite based on specimens collected from
Rattus
norvegicus
Berkenhout, 1769. Tus, the present study
enhances morphological details of
M. muris
reporting a
new geographical distribution obtained from the stomach
of
R. norvegicus
from Nova Iguaçu municipality, Rio de
Janeiro state, Brazil.
MATERIALS AND METHODS
Helminths were collected from
R. norvegicus
during a
1999 study on intestinal protozoa biodiversity in Nova
Iguaçu, Rio de Janeiro, Brazil (22º45’35’’S,43º27’6’’W),
resulting in the identifcation of
Eimeria nieschulzi
Dieben, 1924 and
E. separata
Becker & Hall, 1931
(Bomfm & Lopes, 1999).
Rodents were captured using Tomahawk traps (40.64
cm X 12.70 cm X 12.70 cm) and baits made with
banana, sardines, peanut candy and oats. Te traps were
positioned along a 50-point trail in two distinct habitats
located in the Fluminense microregion of Grande Rio
(FIBGE, 1985). Captured
R. norvegicus
specimens were
transported in plastic containers with access to food and
water
ad libitum
to the Laboratory of the Experimental
Station for Parasitological Research at the Institute of
Biology, Federal Rural University of Rio de Janeiro. Te
rodents were euthanized in a CO
2
chamber and, following
death, they were classifed by sex and age according to
Calhoun (1962). After that, necropsies were performed.
Nematodes recovered from the stomach were washed in
saline, sodium chloride solution (NaCl 0.9%), fxed and
conserved in AFA (2% acetic acid, 3% formaldehyde and
95% ethanol) and, posteriorly, clarifed in lactophenol
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(40% lactophenol, 20% lactic acid and 20% phenol
in 100 mL q.s.p.) for analysis in this study. Images
were captured using Olympus™ BX51 binocular light
microscope and the Olympus cellSens Standard software.
All the morphological characters were measured in
millimeters otherwise stated. Measurements were based
on twenty specimens, seven males and thirteen females.
For scanning electron microscopy imaging, four
specimens (two males and two females) were selected
and fxed using 2.5% glutaraldehyde for one hour.
Subsequently, the nematodes were washed and immersed
in Na-cacodylate bufer solution and also washed. Te
specimens were then post-fxed in 1% osmium tetroxide
and 0.1M Na-cacodylate for 3 hours at room temperature
(Mafra & Lanfredi, 1998). Te material was dehydrated
using increasing ethanol series and dried with CO
2
using
the critical point method. Finally, the mounting was
performed using aluminum stubs and sputter coated
with a 20 nm thick gold layer on silver cellophane. Tus,
the specimens were examined using a Jeol JSM-6390
LV microscope with an accelerating voltage of 15kV
at the Oswaldo Cruz Institute (Rudolf Barth Electron
Microscopy Platform) in Rio de Janeiro, Brazil. Vouchers
specimens were deposited in the Helminthology
Collection of the Institute Oswaldo Cruz (CHIOC).
Ethic aspects
: Tis study was conducted after project
approval by the Federal Rural University of Rio de
Janeiro, in compliance with Brazilian legislation on
Animal Experimentation, in force at the time of the study.
RESULTS
TAXONOMIC SUMMARY
Species: Mastophorus muris
Gmelin, 1971
Host
:
Rattus norvegicus
(Berkenhout, 1769)
Locality
: Nova Iguaçu, Rio de Janeiro state
(22º45’35’’S,43º27’6’’W)
Site of infection
: Stomach
Prevalence
: 0.5% (1 rodent infected/ 173 rodents
collected)
Intensity
: 20 (13 females and 7 males)
Deposited:
CHIOC number 39679
General
: Te nematodes are large, females being longer
and thicker than males. Cephalic and body cuticle with
transverse striation, males showing ornamentation in
the posterior ventral region (Figure 2A). Anterior region
composed of two lateral pseudolobias, each formed by
three lobes (two submedian lobes slender and slightly
rounded and one lateral larger and quadrangular in
shape) (Figure 1A). A pair of cephalic papillae near to
the external base of each submedian lobe and a porous
structure present in submedian lobe (Figure 1B). Amphids
at the base of the lateral lobe (Figure 1B). Te internal
margin of each lobe of the pseudolabia is armed with
teeth variable in number (5 to 9), constantly presenting
a larger and developed tooth in the center (Figure 1C).
Teeth with pointed ends that can be either cleft in two or
three cusps in diferent sizes in the distal region located
in the internal border of the pseudolo no bia (Figure 1D,
4D). A rectangular, thick-walled mouth capsule, presence
of two derids anterior to excretory pore and nerve ring
near excretory pore (Figure 4A, B, E, F). Te stoma
elongated and cylindrical with thick walls (Figure 4C).
Males.
Total body length 27 - 41 (32.7) (n= 7) and wide
at mid-body 0.58 – 2.86 (1.08) (n=7). Nerve ring 0.35
– 0.54 (0.42) (n=7), excretory pore 0.41 – 0.57 (0.47)
(n=7) and derids 0.29 – 0.47 (0.38) (n= 4) from the
anterior end. Stoma 0.15 long and 0.07 wide (n=1).
Oesophagus 6.18 length (n=1). Spicules are unequal,
sclerotized, fliform with diferent sizes; right 0.834 long
and 0.019 wide (n=1) elongated and blunt-ended and
left 0.651 long and 0.018 wide (n=1) slightly smaller
and tapered-ended. Te length of the shorter spicule is
78.3 percent that of the longer one. Elongated tail with
four pairs of pedunculated precloacal papillae and a single
papilla at the anterior border of the cloaca (Figure 2A).
One pair ad-cloacal papillae and two pairs pedunculated
post-cloacal papillae (Figure 2B). Distal end of tail not
ornamented with four pairs of sessile papillae and a pair
of phasmid (Figure 3A). Gubernaculum present. Tail
0.31-0.51 (0.41) long (n=5).
Females
. Total body length 27 - 96 (63) (n=11) and wide
at mid-body 0.42 – 3.28 (1.75) (n=11). Stoma 0.17 long
and 0.093 wide (n=2). Oesophagus 6.2 length (n=1).
Nerve ring 0.29 – 0.93 (0.49) (n=11), excretory pore
0.4
– 0.66 (0.52) (n=11) and derids 0.54 – 0.59 (0.58) (n=4)
at anterior end. Vulva at 11 - 31 (24) (n=5) from the
anterior end (Figure 3B). Tail 0.28 – 0.74 (0.43) (n=11).
Presence of a pair of phasmid in the tip of tail (Figure
3A). Eggs are elliptic with thick shell 41 - 53 µm (44.3
µm) long and 26 - 32 µm (29 µm) wide (Figure 3C).
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Figure 1.
Scanning electron micrographs of
Mastophorus muris
(
A) Front view from mouth opening. two triangular
lateral lobes and square shape medium lobe. (B) Amphids at the base of the lateral lobe (am), a pair of cephalic pap
papillae (cp) at the base of each pseudolabia and a porous structure (p) at each median lobe. (C) Lateral lobe; denticulated
margin with a central developed teeth (*); porous structure (p). (D) Teeth of diferent shapes and sizes.
Figure 2.
Scanning electron micrographs of
Mastophorus muris
showing ventral view from the posterior end. Male. (A)
Four pairs of pedunculated precloacal papillae (arrows) and a single papilla anterior the cloaca (*). One pair ad-cloacal
papillae (arrowhead) and two pairs pedunculated post-cloacal papillae (arrows). (B) A single papilla anterior the cloaca
(arrowhead) and a pair ad-cloacal papillae (ad). (C) Posterior end female showing the anus.
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Figure 3.
Light microscopy of
Mastophorus muris
(A) Ventral view from the distal end. Tail not ornamented with four
pairs of sessile papillae (arrows) and a pair of phasmid (f). (B) Vulva. (C) Eggs.
Figure 4.
Light microscopy of
Mastophorus muris.
Anterior end of female. (A) Dorsal view. Nerve ring (nr). (B) Excretory
pore (ep). (C) Dorsal view. Stoma (st). (D) Teeth of diferent sizes(arrow). (E, F) Anterior end showing left and right
derids (d).
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DISCUSSION
Te species belonging to the genus
Mastophorus
Diesing,
1853 are found mainly infecting rats belonging to the
families Muridae and Microtidae (Anderson, 2000).
Tis nematode has been reported parasitizing the rats
R.
norvegicus
in
Israel, Portugal and United States of America
(USA) (Firlotte, 1948; Wertheim,1962; Quintal, 2022)
,
R. alexandrinus
Geofroy, 1803 in Israel
(Wertheim,
1962),
R. assimilis
Gould, 1858 in Australia (Smales,
1997),
R. rattus
Linnaeus, 1758 in New Zealand and
Portugal (Charleston & Innes, 1979; Quintal, 2022),
Mus musculus
Linnaeus, 1758 in Lithuania, Serbia and
Germany (Mažeika
et al
., 2003; Vukićević-Radić
et al
.,
2007; Jost
et al
., 2024)
, R. norvegicus
(Syn.
M. decumanus
)
in India (Maplestone & Bhaduri, 1942),
Meriones
persicus
Blanford, 1875 in Iran (Harandi
et al
., 2016),
Myodes glareolus
Schreber, 1780 in Poland and Germany
(Gryzbek, 2014; Jost
et al
., 2024)
, Arvicola amphibius
Linnaeus, 1758 in southern Sweden (Neupane, 2018),
Microtus miurus
Osgood, 1901 in Alaska (Haukisalmi
et al
., 1995),
Graomys griseofavus
Waterhouse, 1837 in
Argentina (Rojas & Digiani, 2003),
Geomys breviceps
Baird, 1855,
Peromyscus leucopus
Rafnesque, 1818
,
Sigmodon hispidus
Say & Ord, 1825 and
Oryzomys
palustris
Harlan, 1837 in USA (Erickson, 1944; Childs
& Cosgrove, 1966) and
Apodemus favicollis
Melchior,
1834 in Germany (Jost
et al
., 2024). In Brazil,
M. muris
was reported infecting
R. norvegicus
and
R. rattus
(Araújo,
1967, Vicente
et al
., 1997). Interestingly, despite this
parasite being found majority in rodent species, this
nematode was also reported in marsupials
Trichosurus
vulpecula
Kerr, 1792 and
Hypsiprymnodon moschatus
Ramsay, 1876 in Australia,
Dactylopsila trivirgata
Gray,
1858 in USA, in mustelid
Meles meles
Linnaeus, 1758 in
Spain and in carnivores
Lynx pardinus
Temmink, 1827 in
Spain,
Vulpes vulpes
Linnaeus, 1758 in Spain and China,
Vulpes ferrilata
Hodgson, 1842
in China and
Canis latrans
Say, 1823 in USA (Johnston & Mawson, 1938;
Smales,
1995; Torres
et al
., 1998; Barbosa
et al
., 2005; Chen,
2022) and
Felis silvestris
Schreber, 1777 in Germany
(Jost
et al
., 2024). Te largest number of rodent species
infected with
M. muris
likely acquire it through their diet.
Ingestion of intermediate hosts, containing the parasite
larvae, makes them susceptible. Additionally, carnivores
can become infected by accidentally consuming
intermediate or paratenic hosts.
Te life cycle of
M. muris
is indirect with a great
diversity of insects as intermediate hosts (Grybek
et
al
., 2014), likewise, a large number of mammal species
can be defnitive hosts. Te worldwide distribution of
the helminth and diferent host taxa suggests low host
specifcity both defnitive and intermediate. Goldberg &
Bursey (2002) suggest that geckos
Hemidactylus turcicus
Linnaeus, 1758
and
H. mabouia
Moreau de Jonnes,
1818 could be paratenic host
,
since encysted larvae not
yet studied have been found in the skeletal muscles of
these animals in the same place where there was a high
prevalence of the nematode in rodents (Laferty
et al
.,
2010), in fact, further research to elucidate the specifc
roles of various hosts within it is necessary.
In Brazil,
M. muris
infecting murids
was reported as
Protospirura columbiana
Cram, 1926 by Araújo (1967)
and Chief
et al.
(1980) in the city of São Paulo and
as
P. muris
by Brito
et al.
(1969) in the city of Rio de
Janeiro. Indeed, the taxonomic classifcation of the genus
Mastophorus
was historically confused with that of the
genus
Protospirura
Seurat, 1914. Te genus
Mastophorus
was described by Diesing in 1853, however, York &
Maplestone (1926) considered that there was not enough
information to create a new genus and relocated eight
species of
Mastophorus
in the genus
Protospirura.
After,
Chitwood (1938) considered
Mastophorus
a valid genus
that difered from
Protospirura
by the arrangement of
the pseudolabium teeth and, furthermore, subdivided
the species
M. muris
into two varieties:
M. muris
var.
muris
and
M. muris
var.
ascaroides
. Read & Millemann
(1953) disagreed with Chitwood’s (1938) classifcation
arguing that the chosen characteristics were only valid
at the subgenus level. Consequently, they re-established
M. muris
as a distinct species
,
classifying it and removing
it again from the genus
Protospirura
. Examining the
morphology of
M. muris
and
P. muricola
larvae
,
Quentin
(1970) confrmed the distinctness of the two genera in
accordance to Chitwood (1938). Key diferentiating
features include the number of teeth in the pseudolabia,
the shape of the stoma, the morphology and arrangement
of pre- and post-cloacal papillae in males, the length of
the male caudal wing, and the position of the vulva in
females (Chitwood, 1938; Quentin, 1970; Smales
et
al
., 2009). Actually, the synonyms for
M. muris
found
in the literature are:
Protospira labiodentata
Linstow,
1899
, P. gracilis
Cram
,
1924
, P. columbiana
Cram,
1926
, P. ascaroidea
Hall
,
1916
, P. glareoli
Soltys
,
1949
,
P. marsupialis
Baylis
,
1934
and
P. bestiarum
Kreis
,
1953
.
Te species of the present study is
M. muris
by the following
characteristics: fve to nine teeth in each pseudolabia,
long stoma, long tail and pedunculated papillae in males
and a pre-equatorial vulva in females in accordance to
Chitwood (1938) and Quentin (1970). Inconsistent
descriptions of the anterior region, particularly regarding
the highly variable tooth shapes, and inaccurate posterior
region descriptions on the arrangement of pedunculated
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and sessile papillae, hindered the accurate classifcation
of
Mastophorus
and
Protospirura
species (Jost
et al
.,
2024). Recently, Jost
et al
. (2024) investigated the
morphological and molecular variation within
M. muris
,
emphasizing the importance of dentition analysis for
parasite taxonomy. Te study proposed tooth pattern
formulas to diferentiate
M. muris
specimens based on
their hosts.
Mus
hosts were identifed by the formula 1–
(2 + n)–1–(2 + n)–1, where “n” represents the variable
number of smaller denticles. Specimens from non-
Mus
hosts (as
Myodes
,
Rattus
, and
Felis
) shared the formula
1–(2 + n)–1, with a large central tooth and a variable
number of smaller denticles. Finally,
Graomys
specimens
exhibited a unique formula of 1–3–1–3–1, characterized
by three smaller denticles between larger ones in the
margin of each lobe as described by Rojas & Digiani
(2003). Diferently, Wertheim (1962) considered that the
denticles would be serrated projections of the thin and
fexible membrane covering the pseudolabium noting a
high variability in both the number and shape of teeth
within the lobes with no dental pattern. In most cases,
was observed a centrally placed large tooth and a variable
number of teeth, often bifd, juxtaposed to the large
central tooth as in specimens of
R. assimilis
from Israel.
Our fndings are in agreement with Wertheim (1962)
that the tooth arrangement on the margin of each lobe
is asymmetrical. Notably, a central tooth is consistently
present in each lobe, smaller teeth with pointed ends
that can be either bifd (divided into two) or trifurcated
(divided into three) and pointed teeth of varying sizes can
be observed.
Wertheim (1962), Roja & Digiani (2003) and Jost
et al
.
(2024) described four pairs of pre-anal and two post-anal
pedunculated papillae along with a variable number of
sessile papillae (1 to 7 pairs) at the end of the tail and a
single papilla just anterior to the edge of the cloaca. Our
observations confrm the presence of previously reported
papillae, while we additionally identifed a pair of ad-
cloacal papillae not documented before.
M. muris
exhibits
signifcant morphological and morphometric variation
among isolates from diferent host species. Furthermore,
genetic diferences have also been identifed between
isolates, as evidenced by Jost
et al
. (2024). Despite our
eforts, genetic material extraction from the samples
proved unsuccessful. Tis limits our ability to contribute
valuable insights into the genus’ complexity. Tis study
underscores the need for further investigation to clarify
host-genus relationships and explore the possibility of
reclassifying the parasite into distinct species or even a
new genus identity.
Te pathogenicity of
M. muris
in defnitive hosts have
been evaluated as mild pathology mainly related to low
parasite burdens. Tis efect is likely due to the nematodes’
consumption of gastric contents, leading to a decline in
body condition (Laferty
et al
., 2010). However, high
parasite loads could result in regurgitation, signs of
gastritis, obstruction of the gastrointestinal tract, and
severe weight loss (Grzybek
et al.
, 2014).
Te nematode
M. muris
is worldwide distributed and
found in Eurasia, America, and Oceania (Rausch, 1951;
Neupane
et al.
, 2018). Study of the prevalence of
M.
muris
in
R. rattus
in an island with extensive vegetation
cover and coconut trees Palmyra Atoll in the central
Pacifc Line Islands from North America showed a
high prevalence with 59% (97/165) of hosts infected
(Laferty
et al
., 2010). In contrast, a low prevalence of
3.7% (21/567) was observed in
Mus musculus
collected
in Germany (Jost
et al
., 2024). In Brazil, the prevalence
of this stomach spirurid in studies of the helminth fauna
of synanthropic rodents is very low with 2% (4/205)
(Chief
et al
., 1980) or non-observed in some areas
(Simões
et al
., 2016; Carvalho-Pereira
et al
., 2018). In
fact, a low prevalence of 0.5% (1/173) was also observed
in the present study. Probably, due to the low prevalence
of this nematode in Brazil, it is difcult to fnd infected
defnitive hosts, moreover, anthropic changes could
modify the natural habitats of the intermediate hosts
leading to disappearance of parasites. Reinforcing the
infuence of habitat, Roberts
et al
. (1992) demonstrated
a strong correlation between helminth infections and
specifc environments. Teir study on
Rattus exulans
Peale, 1848 in forests, pastures, and farms found the
highest infection rates of the trematode
Brachylaima
sp
.
Dujardin, 1843 and the nematode
Calodium hepaticum
Bancroft, 1893 (syn.
Capillaria hepatica
), and
M. muris
in
forested areas. Tis suggests that the greater abundance
of arthropods, particularly those that create favorable
microhabitats for intermediate host survival and
reproduction, contributes to higher infection levels in
these environments. Te prevalence of
M. muris
infection
in rodents can be infuenced by several factors, such as
age, sex, and reproductive status (e.g., adult rodents,
mature or lactating females), can play a role (Laferty
et
al
., 2010; Grzybek
et al
., 2014). Additionally, extrinsic
factors like season, local temperature, feeding habits,
and food availability in the host’s environment can also
infuence infection rates (Laferty
et al
., 2010; Burlet
et
al
. 2011).
Tis study provided a detailed morphological analysis
adding new taxonomic features as a pair of adcloacal
papillae and details of pseudolabia teeth for
M. muris
194
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Rapozo Dias
et al.
from
R. norvegicus
in Nova Iguaçu municipality, Rio
de Janeiro state. Additionally, contributing with a new
geographical distribution to
M. muris.
Tis refned
characterization may contribute to future identifcations
and improve our understanding of the species. To gain
a deeper understanding of diversity within the genus
Mastophorus
, integrating molecular characterization
analysis would be highly suggested.
Author contributions: CRediT (Contributor Roles
Taxonomy)
AJRD =
Ana Júlia Rapozo Dias
BEAS =
Beatriz Elise de Andrade Silva
TCBB =
Teresa Cristina Bergamo do Bomfm
AMJ =
Arnaldo Maldonado Júnior
ROS =
Raquel de Oliveira Simões
Conceptualization:
AJRD, TCBB, ROS
Data curation:
AJRD, TCBB, ROS
Formal Analysis:
AJRD, BEAS, AMJ
Funding acquisition:
ROS
Investigation:
AJRD, BEAS, TCBB, AMJ, ROS
Methodology:
AJRD, BEAS, TCBB, ROS
Project administration:
AJRD, TCBB, ROS
Resources:
AJRD, BEAS, TCBB, AMJ, ROS
Software:
AJRD, BEAS, TCBB, AMJ, ROS
Supervision:
BEAS, AMJ, ROS
Validation:
AJRD, BEAS, TCBB, AMJ, ROS
Visualization:
AJRD, BEAS, ROS
Writing – original draft:
AJRD, BEAS, ROS
Writing – review & editing:
AJRD, BEAS, TCBB,
AMJ, ROS
BIBLIOGRAPHIC REFERENCES
Anderson, R. C. (2000). Nematode parasites of vertebrates: their development and transmission. 2
nd
ed.
CABI digital
Library.
Araujo, P. (1967)
.
Helmintos de
Rattus norvegicus
(Berkenhout, 1769) da cidade de São Paulo.
Revista de Farmácia e
Bioquimica, 5,
141-159.
Bain, O., Mutafchiev, Y., & Junker, K. (2014). Order Spirurida. pp. 661–732
in
Schmidt-Rhaesa, A (
Ed
.)
Handbook of
zoology: Gastrotricha, Cycloneuralia and Gnathifera
. Volume 2. Nematoda. De Gruyter.
Barbosa, A.M., Segovia, J.M., Vargas, J.M., Torres, J., Real, R., & Miquel, J. (2005). Predictors of red fox (
Vulpes vulpes
)
helminth parasite diversity in the provinces of Spain.
Wildlife Biology in Practice, 1
, 3–14.
Bomfm, T., & Lopes, C.W.G. (1999). Species of the genus
Eimeria
(Apicompexa: Eimeriidae) parasites of
Rattus
norvergicus
in Rio de Janeiro, Brasil.
Revista Universidade Rural Ciências da Vida, 21
, 11-23.
Burlet, P., Deplazes, P. & Hegglin, D. (2011). Age, season and spatio-temporal factors afecting the prevalence of
Echinococcus multilocularis
and
Taenia taeniaformis
in
Arvicola terrestris
.
Parasites and Vectors
,
4
, 1-9.
Calhoun, J. B. (1962). Te ecology and sociology of Norway rat. United States Government.
Print Of, 210.
Carvalho-Pereira, T., Souza, F., Santos, L., Walker, R., Pertile, A., de Oliveira, D., Pedra, G., Minter, A., Rodrigues, M.,
Bahiense, T., Reis, M., Diggle, P., Ko, A., Childs, J., da Silva, E., Begon, M., & Costa, F. (2018). Te helminth
community of a population of
Rattus norvegicus
from an urban Brazilian slum and the threat of zoonotic diseases.
Parasitology
,
145
, 797-806.
Charleston, W., & Innes, J. (1979). Seasonal trends in the prevalence and intensity of spiruroid nematode infections of
Rattus rattus
.
New Zealand Journal of Zoology
,
7
, 141–145.
Chen, Q., Wang, X., Li, C., Wu, W., Zhang, K., Deng, X., Xie, Y., & Guan, Y. (2022). Investigation of parasitic
nematodes detected in the feces of wild carnivores in the eastern Qinghai-Tibet Plateau, China.
Pathogens
,
11
,
1520.
195
Mastophorus muris parasite of the
Rattus norvegicus
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Chief, P., Grispino, D., Mangini, A., Dias, R., Villanova, A., Guidugli, N. & de Souza, A. (1980). Helmintos parasitas
do aparelho digestivo de murídeos capturados no município de São Paulo, S.P., Brazil. Prevalência, intensidade
de parasitismo e importância em saúde pública.
Revista do Instituto Adolfo Lutz
,
401
, 35-41.
Childs, H. & Cosgrove, G. (1966). A study of pathological conditions in wild rodents in radioative areas.
Te American
Midland Naturalist
,
76
, 309–324.
Chitwood, B.G. (1938). Te status of
Protospirura
vs.
Mastophorus
with a consideration of the species of these genera.
Livro Jubilar do Professor Lauro Travassos
, 115–118.
Erickson, A. (1944). Helminths of Minnesota Canidae in relation to food habits, and a host list and key to the species
reported from North America.
Te American Midland Naturalist, 32
, 358–372.
FIBGE. (1985). Censo Agropecuário Rio de Janeiro, IBGE.
20,
370.
Firlotte, W. (1948). Parasites of the Norway rat.
Canadian journal of comparative medicine and veterinary Science
,
12
,
187-191.
Gmelin, J.F. (1791). Caroli a Linné. Systema naturae.
Tom. I. Pars VI
, 3021-3910.
Goldberg, S.R., & Bursey, C.R. (2002). Gastrointestinal helminths of seven Gekkonid Lizard species (Sauria:
Gekkonidae) from Oceania.
Journal of Natural History 18
, 2249–2264.
Grzybek, M., Bajer, A., Behnke-Borowczyk, J., Al-Sarraf, M., & Behnke, J. (2014). Female host sex-biased parasitism
with the rodent stomach nematode
Mastophorus muris
in wild Bank Voles (
Myodes glareolus
).
Parasitology Research
,
114
, 523-533.
Harandi, M.F., Madjdzadeh, S.M., & Ahmadinejad, M. (2016). Helminth parasites of small mammals in Kerman
province, southeastern Iran.
Journal of Parasitic Diseases,
40
, 106-9.
Haukisalmi, V., Henttonen, H., & Batzli, G. (1995). Helminth parasitism in the voles
Microtus oeconomus
and
M.
miurus
on the North Slope of Alaska: host specifcity and the efects of host sex, age and breeding status.
Annales
Zoologici Fennici
,
32
, 193-201.
Johnston, T.H. & Mawson, P.M. (1938). Some nematodes from Australian marsupials.
Records of the South Australian
Museum
,
6
, 187–198.
Jost, J., Hirzmann, J., Ďureje, L., Maaz, D., Martin, P., Stach, T., Heitlinger, E., & Jarquín-Díaz, V.H. (2024).
Parasitology
Research
,
123
, 237.
Laferty, K., Hathaway, S., Wegamann, A.S, Shipley, F., Backlin, A.R., Helm, J., & Fisher, R. (2010). Stomach nematodes
(
Mastophorus muris
) in rats (
Rattus rattus
) are associated with coconut (
Cocos nucifera
) habitat at Palmyra Atoll.
Journal of Parasitology
,
96
, 16-20.
Mafra, A.C., & Lanfredi, R.M. (1998). Reevaluation of
Physaloptera bispiculata
(Nematoda: Spiruroidea) by light and
scanning electron microscopy.
Journal of Parasitology
,
84
, 582-588.
Maplestone, P., & Bhaduri, N. (1942). Helminth parasites of certain rats in India.
Records of Te Indian Museum
,
44
,
201-206.
Mažeika, V., Algimantas-Paulauskas, A., & Balčiauskas, L. (2003). New data on the helminth fauna of rodents of
Lithuania.
Acta Zoologica Lituanica
,
13
, 41-47.
Neupane, B., Miller, A.L., Evans, A.L., Olsson, G., & Hoglund, J. (2018). Seasonal variation of
Mastophorus muris
(Nematoda: Spirurida) in the water vole
Arvicola amphibious
from Southern Sweden.
Journal of Helminthology
,
94,
1-4.
Quentin, J.C. (1970) Morphogénèse larvaire du Spiruride
Mastophorus muris
(Gmelin, 1790).
Annales de Parasitologie
Humaine et Comparée
,
45
, 839–855.
196
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Rapozo Dias
et al.
Quintal, L.T.F. (2022).
Helmintofauna gastrointestinal de Rattus rattus e Rattus norvegicus nas áreas portuárias de Lisboa e
Ponta Delgada.
(Dissertação de Mestrado Integrado em Medicina Veterinária). Universidade de Lisboa.
Rausch, R. (1951). Distribution and specifcity of helminths in Microtine rodents: Evolutionary Implications.
Evolution
,
11
, 361-368.
Read, C.P., & Milleman, R.E. (1953). Helminth parasites in Kangaroo rats.
University of California Publications in
Zoology
,
59
, 61-80.
Roberts, M., Rodrigo, A., Mcardle, B., & Charleston, W. (1992). Te efect of habitat on the helminth parasites an
Island population of the Polynesian rat (
Rattus exulans
).
Journal of Zoology
,
227
, 109-125.
Rojas, M., & Digiani, Mc. (2003). First Record of
Mastophorus muris
(Gmelin, 1790) (Nematoda: Spiruroidea) from a
wild host in South America.
Parasite
,
10
, 375-378.
Seurat, L.G. (1914). Sur um noveau Spiroptera du Chat gante.
Comptes Rendus de la Sociéte
́
de
Biologie
,
77
, 344-347.
Simões, R.O., Luque, J.L., Gentile, R., Rosa, M.C.S., Costa-Neto, S., & Maldonado, A. (2016). Biotic and abiotic
efects on the intestinal helminth community of the brown rat
Rattus norvegicus
from Rio de Janeiro, Brazil.
Journal of Helminthology
,
90
, 21-27,
Smales, L. (1995).
Mastophorus muris
(Nematoda: Spirocercidae) from the musky rat-kangaroo,
Hypsiprymnodon
moschatus
.
Transactions of the Royal Society of South
Australia,
119, 95–96.
Smales, L. (1997). A Review of the helminth parasites of Australian rodents.
Australian Journal of Zoology
,
45
, 505-521.
Smales, L.R., Harris, P.D. & Behnke, J.M. (2009). A redescription of
Protospirura muricola
Gedoelst, 1916 (Nematoda:
Spiruridae), a parasite of murid rodents.
Systematic Parasitology
,
72,
15–26.
Souza, A. (1980). Helmintos parasitas do aparelho digestivo de murídeos capturados no município de São Paulo:
prevalência, intensidade de parasitismo e importância em Saúde Pública.
Revista do Instituto Adolfo Lutz
,
1
, 35-41.
Torres, J., Garcia-Perea, R., Gisbert, J., & Feliu, C. (1998). Helminth fauna of the
Iberian lynx
,
Lynx pardinus
.
Journal
of Helminthology
,
72
, 221–226.
Vicente, J., Rodrigues, H., Gomes, D., & Pinto, R. (1997). Nematóides do Brasil. Parte V: Nematóides de Mamíferos.
Revista Brasileira de Zoologia
,
14,
1-452.
Vukićević-Radić, O., Kataranovski, D., & Kataranovski, M. (2007). First record of
Mastophorus muris
(Gmelin, 1790)
(Nematoda: Spiruroidea) in
Mus musculus
from the suburban area of Belgrade, Serbia.
Archives of Biological
Sciences
,
59
, 1-2.
Wertheim, G. (1962). A study of
Mastophorus muris
(Gmelin, 1790) (Nematoda: Spiruridae).
Transactions of the American
Microscopical Society
,
81
, 274-279.
Yorke, W., & Maplestone, P. A. (1926).
Te nematode parasites of vertebrates
. P. Blakiston. 536 p.
Received September 2, 2024.
Accepted October 11, 2024.