image/svg+xml
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 Afines (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.
ISSN Versión impresa 2218-6425
ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2022, 16(2), jul-dic:161-172.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
1
Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, Fundação Oswaldo
Cruz, Av. Brasil 4365, 21040-360, Rio de Janeiro, RJ, Brasil.
2
Campus Fiocruz Mata Atlântica, Av. Sampaio Corrêa s/n, Fundação Oswaldo Cruz, 22713-560, Rio de Janeiro, RJ, Brasil.
3
Programa de Pós-Doutorado Júnior, Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brasília, Brasil.
4
Programa de Pós-Doutorado Nota 10 – 2021, Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de
Janeiro, Brasil.
5
Programa de Pós-Graduação em Biodiversidade e Saúde, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Av. Brasil,
4365, 21040-360, Rio de Janeiro, RJ, Brasil.
6
Programa INOVA IOC, Vice-presidência de Pesquisa e Coleções Biológicas,
Fundação Oswaldo Cruz, Av. Brasil 4365, 21040-360, Rio de Janeiro, RJ, Brasil
7
Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro, km 07, BR-465, 23890- 000,
Seropédica, RJ, Brasil.
*Corresponding author: rgentile@ioc.fiocruz.br
Rosana Gentile: https://orcid.org/0000-0001-9160-1204
Sócrates Fraga da Costa Neto: https://orcid.org/0000-0003-2813-525X
Thiago dos Santos Cardoso: https://orcid.org/0000-0003-2724-6038
Raquel Gonzalez Boullosa: https://orcid.org/0000-0002-7560-4277
Carla Elizabeth Macabu: https://orcid.org/0000-0003-2109-0933
Raquel de Oliveira Simões: https://orcid.org/0000-0001-5130-3341
Arnaldo Maldonado Júnior: https://orcid.org/0000-0003-4067-8660
1*2,31,41,5,6
Rosana Gentile; Sócrates Fraga da Costa-Neto; Thiago dos Santos Cardoso; Raquel Gonzalez Boullosa;
17 1
Carla Elizabeth Macabu; Raquel de Oliveira Simões& Arnaldo Maldonado-Júnior
Neotropical Helminthology
161
DOI: http://dx.doi.org/10.24039/rnh20221621451
HELMINTHS OF SMALL MAMMALS IN AN ATLANTIC FOREST BIOLOGICAL STATION IN RIO
DE JANEIRO, BRAZIL
HELMINTOS DE PEQUEÑOS MAMÍFEROS EN UNA ESTACIÓN BIOLÓGICA DEL BOSQUE
ATLÁNTICO EN RÍO DE JANEIRO, BRASIL
HELMINTOS DE PEQUENOS MAMÍFEROS EM UMA ESTAÇÃO BIOLÓGICA DA MATA
ATLÂNTICA NO RIO DE JANEIRO, BRASIL
D
D
D
D
D
D
ABSTRACT
Interface areas between urban and sylvatic environments increase the contact between humans and wild
animals, and may favour the transmission of zoonoses. The aim of this study was to describe the helminth
fauna of a small mammal community in an urban-sylvatic interface area of the Brazilian Atlantic Forest.
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
Twenty helminth species were recovered in six species of small mammals. Parasite sharing was observed
in two helminth species among the marsupials. This study is the first report of a helminth infection for the
marsupial
Monodelphis americana
(Müller, 1776). This is the first report of the nematodes
Aspidodera
raillieti
Travassos, 1913,
Viannaia hamata
Travassos, 1914 and
Trichuris
sp. parasitizing the marsupial
Marmosa paraguayana
(Tate, 1931)
.
None of the helminth species found has been reported to infect
162
Neotropical Helminthology, 2022, 16(2), jul-dic
Keywords:
Marsupials – Prevalence – Rodents – Synanthropic animals – Urbanization – Wild animals
The continuous process of urbanization and
expansion of human activities in forested areas
disrupts natural habitats and may change the
patterns of species diversity and abundance. In
disturbed ecosystems, generalist species, such as
the common opossum
Didelphis aurita
(Wied-
Neuwied, 1826), or opportunistic species, such as
some sigmodontine rodents, are favoured in
relation to specialist species (Gentile
et al.
, 2018).
They may have their densities increased and may
INTRODUCTION
become abundant in rural and peridomicile areas
(D'Andrea
et al
., 2007; Kajin
et al
., 2008). The
occurrence of synanthropic species, such as the
common rat
Rattus norvegicus
Berkenhout, 1769,
and the black rat
Rattus rattus
(Linnaeus, 1758), is
also observed in these areas. Such changes in the
demography and distribution of natural
populations, especially in the areas of the interface
between urban and rural or urban and forest
environments, directly influence the transmission
dynamics of parasites (Kruse
et al.
, 2004). These
interface areas may also harbour invasive species.
The presence of invasive species and their parasites
Gentile
et al.
Las áreas de interfaz entre ambientes urbanos y selváticos aumentan el contacto entre humanos y animales
salvajes y pueden favorecer la transmisión de zoonosis. El objetivo de este estudio fue describir la
helmintofauna de una comunidad de pequeños mamíferos en un área de interfaz urbano-selvática de la
Mata Atlántica brasileña. Se recuperaron veinte especies de helmintos en seis especies de pequeños
mamíferos. Se observó el intercambio de parásitos en dos especies de helmintos entre los marsupiales.
Este estudio es el primer reporte de una infección por helmintos para el marsupial
Monodelphis americana
(Müller, 1776). Este es el primer reporte de los nematodos
Aspidodera raillieti
Travassos, 1913,
Viannaia
hamata
Travassos, 1914 y
Trichuris
sp. parasitando al marsupial
Marmosa paraguayana
(Tate, 1931). No
se ha informado que ninguna de las especies de helmintos encontradas infecte a los humanos.
RESUMEN
Palabras clave
: Animales sinantrópicos – Animales salvajes – Marsupiales – Prevalencia – Roedores – Urbanización
Áreas de interface entre ambientes urbanos e silvestres aumentam o contato entre os seres humanos e os
animais silvestres, podendo favorecer a transmissão de zoonoses. O objetivo deste estudo foi descrever a
helmintofauna de uma comunidade de pequenos mamíferos em uma área de interface urbano-silvestre da
Mata Atlântica brasileira. Vinte espécies de helmintos foram recuperadas em seis espécies de pequenos
mamíferos. Compartilhamento de parasitos foi observado em duas espécies de helmintos entre os
marsupiais. Este estudo é o primeiro relato de infecção helmíntica pelo marsupial
Monodelphis
americana
(Müller, 1776). Este é o primeiro relato dos nematoides
Aspidodera raillieti
Travassos, 1913,
Viannaia hamata
Travassos, 1914 e
Trichuris
sp. parasitando o marsupial
Marmosa paraguayana
(Tate,
1931). Nenhuma das espécies de helmintos encontrada já foi relatada infectando seres humanos.
RESUMO
Palavras-chave
: animais sinantrópicos – Animais silvestres – marsupiais – prevalência – roedores – urbanização
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
may affect the local communities and the host-
parasite relationships (Lucio
et al.
, 2021).
The occurrence of human infection by helminth
parasites from wild animals has been attributed to
the increase of interface areas between urban or
rural areas with forest fragments or reserves, where
species of reservoir animals occur. Knowledge of
the helminth species that parasitize wild mammals
in these areas is essential for understanding their
role as an etiological and/or zoonotic agent and,
consequently, the potential risk to public and
animal health (Bezerra-Santos
et al
., 2020), due to
the continuous process of urbanization and human
advance on forest areas.
There are several studies of helminth faunas of
small mammals in the Brazilian Atlantic Forest
(Gomes
et al
., 2003; Maldonado
et al
., 2006;
Cardoso
et al
., 2016; Boullosa
et al
., 2020; Lucio
et
al
., 2021). However, there is a large gap concerning
helminth studies in forested reserves close to urban
centres (Costa-Neto
et al
., 2019; Boullosa
et al
.,
2021). The present study is complementary to
Costa-Neto
et al
. (2019), which studied the
structure of the helminth metacommunity of the
common opossum
Didelphis aurita
in three
localities, including the locality of the present
study. The aim of the present study was to describe
the helminth fauna of a small mammal community
and the helminth population parameters in an
urban-sylvatic interface area of the Atlantic Forest
in Brazil.
Study area
This study is part of a comprehensive project on
biodiversity and environmental health aiming to
understand the role of mammals in the
transmission cycles of parasites and zoonotic
agents at the FIOCRUZ Atlantic Forest Biological
Station (EFMA) (Estação Biológica FIOCRUZ
Mata Atlântica) and its surroundings, including
areas of Pedra Branca State Park (PEPB) (Parque
Estadual da Pedra Branca), in the city of Rio de
Janeiro, southeast Brazil. EFMA is located on the
eastern slope of the Pedra Branca massif in the
western zone of the city of Rio de Janeiro, which is
the second most populous city in Brazil. This area
163
MATERIAL AND METHODS
was previously occupied by sugarcane mills and
coffee farms, with the construction of residences
and roads. In 2003, the area was incorporated into
the Fundação Oswaldo Cruz (FIOCRUZ). From
then on, the master plan of the institution delimited
nonedification areas and established a more
effective process of environmental protection and
recovery aiming to mitigate the effects of anthropic
impacts. The area is formed by a mosaic of
landscapes on the border of the forest reserve,
including sites with vegetation in an advanced
stage of ecological succession, transition sites with
intermediate and initial stages of reforestation, and
sites with consolidated urbanization.
Pedra Branca State Park, adjacent to EFMA, is the
largest urban forest in the Americas and one of the
largest remnants of the Atlantic Forest biome in the
state of Rio de Janeiro. It covers an area of 12,492
ha, and the predominant phytophysiognomy is
ombrophilous dense Atlantic Forest vegetation.
The region's climate is humid mesothermic, with
hot, rainy summers and mild winters.
The samplings were made in different types of
habitat representing preserved forest areas
(22°56'45"S, 43°25'00"W), transition areas
between urban and forested environments,
including reforestation areas (22°56'29"S,
43°24'25”W), and peridomicile areas (22°56'18”S,
43°24'11”W). See Gentile
et al
. (2018) for a more
detailed description of the study area. The areas of
preserved forest were located distant from human
dwellings and, for the most part, above 100 m
elevation. These areas have canopy heights ranging
from 10 to 30 m and irregular slopes, ranging from
flat to steep. The transition areas were located
between the peridomicile areas and the preserved
forest, with a canopy height ranging from 6 to 20 m
and a flat slope. The peridomicile areas were
located in the backyards of the houses, with a lower
canopy ranging from 6 to 10 m, predominance of
shrubs and small trees, presence of flooded areas
and slope varying from flat to moderate.
Small mammal sampling
Small mammal captures were carried out from July
2012 to April 2014 every four months and in July,
October and November 2017 for five consecutive
nights in the three types of habitat. Mammals were
collected using Tomahawk® (16 × 5 × 5 inches)
and Sherman® (3 × 3.75 × 12 inches) live-traps.
Neotropical Helminthology, 2022, 16(2), jul-dic
Helminths of small mammals in Rio de Janeiro
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
164
Two transects of twenty points were established in
each habitat. On each transect, two traps were
placed on the ground at each point. All traps were
baited with a mixture of peanut butter, banana,
oatmeal and bacon. The total trapping effort was
9,120 trap-nights. The animals were anesthetized
and submitted to euthanasia for helminth search.
The mammals were identified by external
morphology, cranial morphology and cytogenetic
analyses, when necessary. The mammalian
specimens were submitted to taxidermy and
deposited in the mammalian collection of the
National Museum of the Federal University of Rio
de Janeiro voucher: 83156 - 83163; 83167 - 83172.
Collection and identification of helminths
Viscera, thoracic and abdominal cavities, and
musculature were examined for helminths. The
organs were separated in Petri dishes with saline
solution (0.85% NaCl) and dissected using a
stereoscopic microscope. The nematodes were
fixed in AFA solution (93 parts 70% ethanol, 5 parts
0.4% formol, and 2 parts 100% acetic acid) and
heated to 65°C. Some specimens were stored in
70% ethanol for further molecular analysis.
Trematodes were fixed in the same solution under
compression, and the cestodes and
acanthocephalans were kept in distilled water for
relaxation of the musculature (Amato
et al.
, 1991).
Nematodes were diaphanized with lactophenol or
glycerinated alcohol. Trematodes, cestodes and
acanthocephalans were stained with Langeron's
carmine or Delafield's hematoxylin, differentiated
with 0.5% hydrochloric acid, dehydrated in a
crescent alcoholic series, diaphanized in methyl
salicylate and mounted in Canada balsam for
permanent preparation (Amato
et al.
, 1991). The
specimens were analysed under a light microscope
(Axio Scope A1 light microscope – Zeiss,
Göttingen, Germany) coupled to an Axio Cam
MRc digital camera.
The specific morphological aspects used to
identify the specimens were according to Anderson
et al.
(2009), Gibbons (2010), Gibson
et al.
(2002),
Jones
et al.
(2005), Khalil
et al.
(1994), Travassos
(1937), Vicente
et al.
(1997) and Yamaguti (1961).
The specimens were deposited in the scientific
collection of helminths at the Laboratory of
Biology and Parasitology of Wild Mammal
Reservoirs - IOC/FIOCRUZ-RJ using the same
deposit numbers of their respective hosts.
Helminth population parameters
Population parameters were calculated for each
helminth species in each host species according to
Bush
et al.
(1997). The average abundance was
considered as the total number of helminths
divided by the number of host individuals
analysed. Mean intensity was calculated as the total
number of helminths divided by the number of
animals infected. Prevalence was considered to be
the ratio between the number of infected animals
and the total number of animals analysed. These
three parameters were calculated for each helminth
species considering each host species. Mean
helminth species richness was calculated as the
average of the helminth species richness found in
each infracommunity (community harboured by a
single host) for each host species.
A bipartite network plot to illustrate host-parasite
interactions between species (Poulin, 2010) was
carried out between the small mammals and the
helminth species. This plot was built based on a
matrix of the presence/absence of each helminth
species in each host species using the bipartite
package (Dormann
et al.
, 2008).
Ethic aspects
Animals were captured under authorization of the
Brazilian Government's Chico Mendes Institute for
Biodiversity and Conservation (ICMBIO, licence
number 13373) and the Environmental Institute of
Rio de Janeiro State (INEA, licence number
020/2011). All procedures followed the guidelines
for the capture, handling, and care of animals of the
Ethical Committee on Animal Use of the Oswaldo
Cruz Foundation (CEUA, licence numbers
LW81/12, and LW-39/14). Biosafety procedures
and personal safety equipment were used during all
procedures involving animal handling and
biological sampling.
Seven species of small mammals were captured,
four of which were marsupials,
Didelphis aurita
(Wied Neuwied, 1826) (45),
Metachirus myosurus
(Temminck, 1924) (1),
Marmosa paraguayana
Tate, 1931 (5) and
Monodelphis americana
(Müller, 1776) (9) (Didelphimorphia,
Didelphidae), and three were rodents,
Akodon
RESULTS
Neotropical Helminthology, 2022, 16(2), jul-dic
Gentile
et al.
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
165
Table 1.
Mean abundance, intensity (± SD), prevalence (95% CI) and site of infection of the helminths of marsupials at FIOCRUZ Atlantic Forest Biological
Reserve, Rio de Janeiro, Brazil. (-) indicates absence of the parasite species.
Neotropical Helminthology, 2022, 16(2), jul-dic
Helminths of small mammals in Rio de Janeiro
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
Table 2.
Mean abundance, intensity (± SD), prevalence (95% CI) and site of infection of the helminths of rodents at FIOCRUZ Atlantic Forest Biological
Reserve, Rio de Janeiro, Brazil. (-) indicates absence of the parasite species.
166
Neotropical Helminthology, 2022, 16(2), jul-dic
Gentile
et al.
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
167
cursor
(Winge, 1887) (7),
Oligoryzomys nigripes
(Olfers, 1818) (9) (Rodentia, Sigmodontinae), and
the sinantropic rodent
Rattus rattus
(Linnaeus,
1758) (7) (Rodentia, Muridae). Twenty species of
helminths were collected from the small mammal
community. Thirteen species were collected from
D. aurita
, three from
M. paraguayana
, one from
M.
americana
, two from
A. cursor
, two from
O.
nigripes
and two from
R. rattus
(Table 1). No
helminth was found in the marsupial
M. myosurus
.
Forty-five individuals of
D. aurita
were analysed,
and all were infected by at least one helminth
species. The mean species richness was 5.4 and
varied from 1 to 9 among the infracommunities.
The highest abundances and intensities were
observed for the nematodes
Viannaia hamata
Travassos, 1914 (Nematoda: Viannaiidae Durette-
Desset & Chabaud, 1981), followed by
Cruzia
tentaculata
(Rudolphi, 1819) Travassos (1917)
(Nematoda: Kathlaniidae Travassos, 1918) and
Travassostrongylus orloffi
Travassos, 1935
(Nematoda: Viannaiidae Durette-Desset &
Chabaud, 1981) (Table 1). The highest prevalence
was recorded for
C. tentaculata
,
T. orloffi
and
Turgida turgida
(Rudolphi, 1819) Travassos, 1919
(Nematoda: Physalopteridae Leiper, 1908) (Table
1).
M. paraguayana
had two specimens infected
among the five analysed. The helminth species
found were
Aspidodera raillieti
Travassos, 1913
(Nematoda: Aspidoderidae (Freitas, 1956),
Trichuris
sp. 1, and
V. hamata
, the latter showing
the highest prevalence and abundance in this host
(Table 1). The mean species richness was 1. Only
two specimens among nine
M. americana
were
infected by a single helminth species,
V. hamata
(Table 1).
Considering rodents, seven individuals of
A.
cursor
were analysed, and two of them were
infected by helminths, the cestode
Rodentolepis
akodontis
Rêgo, 1967 (Platyhelminthes,
Hymenolepididae) and the nematode
Trichuris
sp.
2 (Table 2). All helminths presented low
abundances and intensities. The mean species
richness was 0.43. Four individuals among nine
O.
nigripes
analysed were infected. The helminth
species found were
Guerrerostrongylus zetta
(Travassos, 1937), Sutton & Durette-Desset, 1991
(Nematoda, Heligmonellidae) and
Stilestrongylus
lanfrediae
Souza
et al.
, 2008 (Nematoda,
Heligmonellidae), both with low abundance and
intensity (Table 2). The mean species richness was
0.55. Seven individuals of the synanthropic rodent
R. rattus
were analysed, and two were infected.
Two helminth species were found:
Nippostrongylus brasiliensis
(Travassos, 1914)
(Nematoda, Heligmonellidae) in a single host and
Syphacia muris
(Yamaguti, 1935) (Nematoda,
Oxyuridae) in two hosts, the latter with the largest
abundance and intensity found among rodent hosts
(Table 2). The mean species richness was 0.43.
The bipartite network plot between small
mammals and helminths showed little parasite
sharing among host species (Fig. 1). The nematode
V. hamata
was shared between the marsupials
D.
aurita
,
M. paraguayana
and
M. americana
(Fig. 1).
D. aurita
and
M. paraguayana
shared the
nematode
A. raillieti
(Figure 1). No other helminth
species sharing was observed (Figure 1).
The marsupial
D. aurita
had the highest helminth
species richness when compared to the other host
species. This fact can be due to the generalist habit
of this species, to its vagility (Cáceres & Monteiro-
Filho, 2001), which may have contributed to a
greater acquisition of parasites in different
environments, to its larger body size in relation to
the other mammals and to the larger number of
specimens captured and analysed. The low
helminth species richness found for all the other
host species may be due to the high disturbance of
the local environment, resulting in helminth
species whose eggs may be more resistant in the
soil or species less sensitive to environmental
alterations. Other studies found that habitat
fragmentation and disturbances could negatively
affect the life cycles of some species of parasites,
limiting the occurrence of some species '(Lafferty
& Kuris, 1999; Cardoso
et al
., 2016). However, we
cannot discard the low sample sizes of these
mammals.
This study is the first report of a helminth infection
for the marsupial
M. americana
, which was
infected by
V. hamata.
Furthermore, this is the first
report of the nematodes
A. raillieti
,
V. hamata
and
Trichuris
sp. parasitizing
M. paraguayana
,
DISCUSSION
Neotropical Helminthology, 2022, 16(2), jul-dic
Helminths of small mammals in Rio de Janeiro
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
168
increasing its helminth fauna to six species and
adding this mammal as a new host for these
helminths. Little is known about the helminth
fauna of
M. paraguayana
(Santos-Rondon
et al.
,
2012). In Brazil, only two nematode species have
been reported in this host, the oxyurid
Gracilioxyuris agilisis
Feijó, Torres, Maldonado Jr
& Lanfredi, 2008 in the Cerrado (Neotropical
savannah), state of São Paulo (Santos-Rondon
et
al
., 2012), and the filariid
Litomosoides barretti
Muller, 1980 in the state of Bahia (Muller, 1980).
The cestode
Mathevotaenia bivittata
(Janicki,
1904) has also been reported in this host in
Argentina (Campbell
et al.
, 2003). The helminths
of
D. aurita
are discussed in detail in Costa-Neto
et
al
. (2019).
Regarding the sigmodontine rodent
A. cursor
,
which occurs only in the Brazilian Atlantic Forest
up to 1,170 m high (Geise, 2012), the cestode
R.
akodontis
had been previously reported in this host
Simões
et al.
(2011), as well as a nematode of the
genus
Trichuris
(
T. navonae
) by Lucio
et al
. (2021).
The helminth species richness reported in the
present study was very low compared to previous
reports of the helminth fauna of this rodent in the
Figure 1
. A bipartite network plot indicating the small mammal – helminth associations at FIOCRUZ Atlantic Forest Biological
Reserve, Rio de Janeiro, Brazil.
Neotropical Helminthology, 2022, 16(2), jul-dic
Gentile
et al.
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
169
Atlantic Forest. Simões
et al
. (2011) found nine
species in forest fragments, and Lucio
et al
. (2021)
found eight species in open matrix areas, both in the
state of Rio de Janeiro.
The two nematodes found in
O. nigripes
are
commonly reported in other studies of the helminth
fauna of this sigmodontine rodent (Pinto
et al.
,
1982; Gomes
et al.
, 2003; Simões
et al.
, 2011;
Werk
et al.
, 2016; Panisse
et al.
, 2017; Boullosa
et
al
., 2020; Cardoso
et al.
, 2020). Likewise, the two
nematodes recovered from the synanthropic rodent
R. rattus
have also been reported for this host in
other studies (Gómez-Muñoz
et al.
, 2018; Panti-
May
et al.
, 2020). In Argentina, Muñoz
et al
.
(2018) found higher values of abundance and
prevalence of
N. brasiliensis
in
R. rattus
than in this
study. Panti-May
et al
. (2019) found low values of
intensity, abundance and prevalence for this
helminth in a region of Mexico. These authors also
found high prevalence of
S. muris
positively
associated with the abundance of
R. rattus.
The helminth species were shared only within a
single taxonomic group (Tribe Didelphini), with no
record of parasite sharing between rodents and
marsupials. The two helminths (
V. hamata
and
A.
raillieti
) shared by the marsupial species can be
considered core species in the present study, with
high prevalence and abundances.
Indeed,
A.
raillieti
and
V. hamata
presented prevalence
greater than 50% in
D. aurita
. This indicates that
the three didelphids,
D. aurita, M. paraguayana
and
M. americana
, which share the environment,
also share some helminth species. Jiménez
et al
.
(2011), studying helminth component
communities of didelphid marsupials from several
localities, suggested that sympatric species of
marsupials shared more species of parasites than
parasite communities occurring in conspecific
marsupials from different localities. Our results
corroborate that study with regard to the local
scale.
The results indicated little sharing of parasite
species in these small mammal-helminth
associations. Although these mammals have been
reported as reservoirs of zoonotic pathogens in the
study area
(Berbigier
et al.
, 2021), and some of
them may harbour helminths with zoonotic
potential (Bezerra-Santos
et al
., 2020; Meerburg
et al
., 2009; Araújo
et al
., 2014), none of the
identified helminth species are known to infect
humans.
We would like to thank the staff and students of
Laboratório de Biologia e Parasitologia de
Mamíferos Silvestres Reservatórios, Laboratório
de Hantaviroses e Rickettsioses, Laboratório de
Biologia de Tripanossomatíedeos and Laboratório
de Pesquisa Clínica em Dermatozoonose from
FIOCRUZ who helped in the field work; the
coordinator of FIOCRUZ Atlantic Forest Campus,
Gilson Antunes, for providing local facilities and
supporting the general project; the equip of
FIOCRUZ Atlantic Forest Campus, especially to
Ricardo Moratelli, Marta L. Brandão and José L.P.
Cordeiro for local facilities and help in the field
work; to Marcelo F. Freitas for helping in the field
work in all campaigns; to Cibele R. Bonvicino for
rodent identification, Fabiana P. Caramaschi for
marsupial identification and Daniela Dias for the
curator of the collected animals. This project was
financially supported by Conselho Nacional de
Desenvolvimento Científico e Tecnológico-CNPq
(AMJ, grant number 306352/2014-1), (RG,
researcher fellowship number 304355/2018-6),
Fundação Carlos Chagas Filho de Amparo à
Pesquisa do Estado do Rio de Janeiro-FAPERJ
(RG grant number E-26/111.296/2014 and E-
26/010.001597/2019), and Instituto Oswaldo Cruz
(FIOCRUZ), Fundação Oswaldo Cruz (RGB, PhD
scholarship), (TSC postdoctoral fellowship).
ACKNOWLEDGEMENTS
Amato, JFR, Boeger, W & Amato, SBB, 1991.
Protocolos para laboratório: coleta e
processamento de parasitos de pescado.
Imprensa Universitária, UFRRJ, Rio de
Janeiro.
Anderson, RC, Chabaud, AG & Willmott, S. 2009.
Keys to the nematode parasites of
vertebrates
. CABI International,
Wallingford.
Araújo EO, Mendes, MM, Langone, PQ & Müller,
BIBLIOGRAPHIC REFERENCES
Neotropical Helminthology, 2022, 16(2), jul-dic
Helminths of small mammals in Rio de Janeiro
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
170
G. 2014.
The helminth parasites of
Rattus
rattus
(Linnaeus, 1758) of urban,
intermediate and rural environments in
southern brazil
. Neotropical
Helminthology, vol. 8, pp. 19-22.
Berbigier, AP, Barros, JHS, Pontes, ES, Lisboa,
CV., Gentile, R, Xavier, SCC, Jansen, AM
& Roque, ALR. 2021.
Trypanosomatid
richness in wild and synanthropic small
mammals from a biological station in Rio de
Janeiro, Brazil.
Pathogens, vol. 10, 1442.
Bezerra-Santos MA, Fontes CS, Nogueira BCF,
Yamatogi RS, Ramos RAN, Galhardo JA,
Furtado LFV, Rabelo EML, Araújo JV &
Campos AK. 2020.
Gastrointestinal
parasites in the opossum
Didelphis aurita
:
are they a potential threat to human health?
Journal of Parasitic Diseases, vol. 44, pp.
355–363.
Boullosa, RG, Cardoso, TS, Costa-Neto, SF,
Teixeira, BR, Freitas, TPT, Maldonado-
Júnior, A & Gentile, R. 2020.
Helminth
community structure of three sigmodontine
rodents in the Atlantic Forest, southern
Brazil
. Oecologia Australis, vol. 24, pp.
577–589.
Boullosa, RG, Costa-Neto, SF, Morgado, L,
Maldonado Jr, A & Gentile, R. 2021.
A
longitudinal survey of gastrointestinal
parasites of the black-eared opossum
Didelphis aurita
at an urban-sylvatic
interface area in Southeast Brazil: a
morphological and ecological
characterization based on helminth eggs.
Parasitology Research, vol.120,
pp.3815–3825.
Bush, AO, Lafferty, KD, Lotz, JM & Shostak, AW.
1997.
Parasitology meets ecology on its
own terms: Margolis et al. revisited
. Journal
of Parasitology, vol. 83, pp. 575–583.
Cáceres, NC & Monteiro-Filho, ELA. 2001.
Food
habits, home range and activity of
Didelphis
aurita
(Mammalia, Marsupialia) in a forest
fragment of Southern Brazil
. Studies on
Neotropical Fauna & Environment, vol. 36,
pp. 85–92.
Campbell, ML, Gardner, SL, & Navone, GT. 2003.
A new species of
Mathevotaenia
(Cestoda:
Anoplocephalidae) and other tapeworms
from marsupials in Argentina
. Journal of
Parasitology, vol. 89, pp. 1181–1185.
Cardoso, TS, Costa-Neto, SF, Braga, C, Weksler,
M, Simões, RO, Maldonado, A, Luque, JL
& Gentile, R. 2020.
Helminth
metacommunity of small mammals in a
Brazilian reserve: the contribution of
environmental variables, host attributes
and spatial variables in parasite species
abundance
. Community Ecology, vol. 21,
pp. 159–170.
Cardoso, TS, Simões, RO, Luque, JLF,
Maldonado, A & Gentile, R., 2016.
The
influence of habitat fragmentation on
helminth communities in rodent
populations from a Brazilian Mountain
Atlantic Forest. Journal of Helminthology,
vol. 90, pp. 460–468.
Costa-Neto, SF, Cardoso, TS, Boullosa, RG,
Maldonado, A & Gentile, R. 2019.
Metacommunity structure of the helminths
of the black-eared opossum
Didelphis aurita
in peri-urban, sylvatic and rural
environments in south-eastern Brazil.
Journal of Helminthology, vol. 93, pp.
720–731.
D'Andrea, PS, Gentile, R, Maroja, LS, Fernandes,
FA, Coura, R & Cerqueira, R. 2007.
Small
mammal populations of an agroecosystem
in the Atlantic Forest domain, southeastern
Brazil.
Brazilian Journal of Biology, vol. 67,
pp. 179-186.
Dormann, CF, Gruber, B & Fruend, J. 2008.
Introducing the bipartite Package:
analysing ecological networks
. R News,
vol. 8, pp. 8–11.
Geise, L. 2012.
Akodon cursor
(Rodentia:
Cricetidae).
Mammalian Species, vol. 44,
pp. 33–43.
Gentile, R, Cardoso, TS, Costa-Neto, SF, Teixeira,
BR & D'Andrea, PS. 2018.
Community
structure and population dynamics of small
mammals in an urban-sylvatic interface
area in Rio de Janeiro, Brazil.
Zoologia,
vol. 35, pp. 1–12.
Gibbons, LM. 2010.
Keys to the Nematoda
parasites of vertebrates: supplementary
volume
. CABI Publishing, London.
Gibson, DI, Jones, A & Bray, RA. 2002.
Keys to the
Trematoda
. CABI Publishing and the
Natural History Museum, London, UK.
Gomes, DC, Cruz, RP, Vicente, JJ & Pinto, RM.
2003.
Nematode parasites of marsupials
and small rodents from the Brazilian
Atlantic Forest in the State of Rio de
Neotropical Helminthology, 2022, 16(2), jul-dic
Gentile
et al.
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
171
Janeiro, Brazil
. Revista Brasileira de
Zoologia, vol. 20, pp. 699–707.
Gómez-Muñoz, MA, Robles, MR, Milano, AMF &
Navone, GT. 2018
.
Helminth infection
levels on
Rattus rattus
(Rodentia: Muridae)
from Corrientes city, Argentina
.
Mastozoología Neotropical, vol. 25, pp.
221–227.
Jiménez, FA, Catzeflis, F & Gardner, SL. 2011.
Structure of parasite component
communities of Didelphid marsupials:
insights from a comparative study
. Journal
of Parasitology, vol. 97, pp. 779-786.
Jones, A, Bray, RA & Gibson, DII. 2005.
Keys to
the Trematoda
. CABI Publishing, U.K.
Kajin, M, Cerqueira, R, Vieira, MV, Gentile, R.
2008.
Nine-year demography of the black-
eared opossum
Didelphis aurita
(Didelphimorphia: Didelphidae) using life
tables
. Revista Brasileira de Zoologia, vol.
25, pp. 206-213.
Khalil, LF, Jones, A & Bray, RAA. 1994.
Keys
to
the cestode parasites of vertebrates
. CAB
International, Wallingford, Oxon.
Kruse, H, Kirkemo, AM & Handeland, K. 2004.
Wildlife as source of zoonotic infections
.
Emerging Infectious Diseases, vol. 10, pp.
2067- 2072.
Lafferty, KD & Kuris, AM. 1999.
How
environmental stress affects the impacts of
parasites
. Limnology & Oceanography,
vol. 44, pp. 925–931.
Lucio, CS, Gentile, R, Cardoso, TS, Oliveira-
Santos, F, Teixeira, BR, Maldonado Jr., A &
D'Andrea, PS. 2021.
Composition and
structure of the helminth community of
rodents in matrix habitat areas of the
Atlantic forest of southeastern Brazil
.
International Journal for Parasitology:
Parasites & Wildlife, vol. 15, pp. 278–289.
Maldonado, A, Gentile, R, Fernandes-Moraes, CC,
D'Andrea, PS, Lanfredi, RM & Rey, L.
2006.
Helminth communities of
Nectomys
squamipes
naturally infected by the exotic
trematode
Schistosoma mansoni
in
southeastern Brazil
. Journal of
Helminthology, vol. 80, pp. 369–375.
Meerburg, BG, Singleton, GR & Kijlstra, A. 2009.
Rodent-borne diseases and their risks for
public health.
Critical Reviews in
Microbiology, vol. 35, pp. 221-270.
Munõz, MAG, Robles, MDR, Milano, AMF &
Navone, GT. 2018.
Helminth infection
levels on
Rattus rattus
(Rodentia: Muridae)
from Corrientes city, Argentina
.
Mastozoología Neotropical, vol. 25, pp.
221-227.
Panisse, G, Robles, MDR, Digiani, MC,
Notarnicola, J, Galliari, C & Navone, GT.
2017.
Description of the helminth
communities of sympatric rodents
(Muroidea: Cricetidae) from the Atlantic
Forest in northeastern Argentina
. Zootaxa,
vol. 4337, pp. 243–262.
Panti-May, JA, Palomo-Arjona, EE, Gurubel-
González, YM, Barrientos-Medina, RC,
Digiani, MC, Robles, MR, Hernández-
Betancourt, SF & Machain-Williams, C.
2020.
Patterns of helminth infections in
Rattus rattus
and
Mus musculus
from two
Mayan communities in Mexico
. Journal of
Helminthology, vol. 94, e30.
Pinto, RM, Kohn, A, Fernandes, BMM & Mello,
DA. 1982.
Nematodes of rodents in Brazil,
with description of
Aspidodera vicentei
n.sp
. Systematic Parasitology, vol. 4, pp.
263-267.
Poulin, R. 2010.
Network analysis shining light on
parasite ecology and diversity
. Trends in
Parasitology, vol. 26, pp. 492–498.
Santos-Rondon, MVS, Pires, MM, Reis, SF &
Ueta, MT. 2012.
Marmosa paraguayana
(Marsupialia: Didelphidae) as a new host
for
Gracilioxyuris agilisis
(Nematoda:
Oxyuridae) in Brazil.
Journal of
Parasitology, vol. 98, pp. 170–174.
Simões, RO, Souza, JGR, Maldonado, A & Luque,
JL. 2011.
Variation in the helminth
community structure of three sympatric
sigmodontine rodents from the coastal
Atlantic Forest of Rio de Janeiro, Brazil.
Journal of Helminthology, vol. 85, pp.
171–178.
Travassos, L. 1937.
Revisão da família
Trichostrongylidea Leiper 1912
. Memórias
do Instituto Oswaldo Cruz, vol. 1, pp.
1–512.
Vicente, JJ, Rodrigues, HO, Gomes, DC & Pinto,
RM. 1997.
Nematóides do Brasil. Parte V:
nematóides de mamíferos.
Revista
Brasileira de Zoologia, vol. 14, pp. 1–452.
Werk, DF, Gallas, M, Silveira, EF & Périco, E.
2016.
New locality records for
Guerrerostrongylus zetta
(Travassos, 1937)
Neotropical Helminthology, 2022, 16(2), jul-dic
Helminths of small mammals in Rio de Janeiro
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134
image/svg+xml
172
Sutton & Durette-Desset, 1991 (Nematoda:
Heligmonellidae) parasitizing
Oligoryzomys nigripes (Olfers, 1818)
(Rodentia: Sigmodontinae) from southern
Brazil
. Check List, vol. 12, 1861.
Yamaguti, S. 1961.
Systema Helminthum
.
Interscience Publishers, New York.
Received August 26, 2022.
Accepted November 4, 2022.
Neotropical Helminthology, 2022, 16(2), jul-dic
Gentile
et al.
art. 1=10-24
art. 2=26-41
Art 3 =42-51
art. 4=52-59
art. 5=60-65
art 6=66-79
art. 7=80-91
art 8 =92-100
art 9=102-111
nota 1=112-116
nota 2=118-123
rev =124-134