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Gastrointestinal Parasitism in Rescued Wild Birds
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Neotropical Helminthology
Neotropical Helminthology, 2024, vol. 18 (2), 249-258
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
FIRST REGISTER OF
CONTRACAECUM
SP. AND
EUSTRONGYLIDES
SP. (NEMATODA) IN
KINOSTERNON SCORPIOIDES
(LINNAEUS, 1766)
(TESTUDINES: KINOSTERNIDAE) FROM NORTHEASTERN, BRAZIL
PRIMER REGISTRO DE
CONTRACAECUM
SP. Y
EUSTRONGYLIDES
SP.
(NEMATODA) EN
KINOSTERNON SCORPIOIDES
(LINNAEUS, 1766)
(TESTUDINES: KINOSTERNIDAE) DEL NORESTE DE BRASIL
Alana Lislea de Sousa
1
, Almerinda Macieira Medeiros
2
, Júlia Boáis Almeida
2
, Silmara Cristina Silva
de Aquino
1
, Elias Costa Ferreira Junior
1
, Diego Carvalho Viana
3
, Victor Puicón-Niño de Guzmán
4
& Germán Augusto Murrieta-Morey
1,5*
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.62429/rnh20242181853
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.
ABSTRACT
Kinosternon scorpioides
(Linnaeus, 1766) popularly known in Brazil as “Jurará” is a species of chelon that serves as a
food resource and source of income for some families in Northeastern Brazil. In that sense, the present study aimed to
analyze the metazoan endoparasites infecting
K. scorpioides
from the Baixada Maranhense, Brazil. Fifteen adult specimens
1
Universidade Estadual do Maranhão (UEMA). Programa de Pós-graduação em Ciência Animal (PPGCA), Cidade Universitária
Paulo IV, São Luís, 65055-310, Maranhão-Brasil.
2
Universidade Estadual do Maranhão (UEMA). Programa de Pós-graduação em Biotecnologia e Biodiversidade da Amazônia
Legal (Rede Bionorte), Cidade Universitária Paulo IV, São Luis, 65055-310, Maranhão-Brasil.
3
Universidade Estadual da Regiao Tocantina do Maranhão (UEMASUL). Programa de Pós-graduação em Ciência Animal
(PPGCA), Cidade Universitária Paulo IV, São Luís, 65055-310, Maranhão-Brasil.
4
Grupo de Investigación Parasitología Veterinaria y Zoonosis Parasitaria, Laboratorio de Histopatología animal, Facultad de
Medicina Veterinaria, Escuela Profesional de Medicina Veterinaria, Universidad Nacional de San Martín. Tarapoto, Perú.
5
Instituto de Investigaciones de la Amazonia Peruana (IIAP), Laboratorio de Parasitologia y Sanidad Acuicola, Carretera
Iquitos-Nauta, Km 4.5 – San Juan Bautista, Iquitos, 0784, Loreto, Perú.
*
Corresponding author:germantiss1106@gmail.com
Alana Lislea de Sousa:
https://orcid.org/0000-0002-0920-2560
Almerinda Macieira Medeiros:
https://orcid.org/0000-0002-3808-2035
Júlia Boáis Almeida:
https://orcid.org/0009-0000-0230-732X
Silmara Cristina Silva de Aquino:
https://orcid.org/0000-0001-7680-9699
Elias Costa Ferreira Junior:
https://orcid.org/0000-0002-5925-6372
Diego Carvalho Viana:
https://orcid.org/0000-0002-3302-9892
Victor Puicón Niño de Guzmán:
https://orcid.org/0000-0003-2532-2551
Germán Augusto Murrieta Morey:
https://orcid.org/0000-0001-6244-2654
Lislea de Sousa
et al.
250
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
were captured using funnel traps in fooded felds around the Aurá River, close to the city of São Bento-Maranhão.
Samples were transported to the Postgraduate Multi-User Research Laboratory- Laboratories in Postgraduate Research/
Postgraduate in Animal Science located at the State University of Maranhão- UEMA for parasitological analyses. Te
results revealed the presence of larvae of
Contracaecum
sp. infecting the stomach, intestine, and liver, while
Eustrongylides
sp. was found encysted in the musculature, stomach, intestine, and inside an egg of a gravid female mud turtle. Te
fndings of the present study constitute the frst records of these nematodes parasitizing
K. scorpioides
. Since
K. scorpioides
is consumed as food for some families in the State of Maranhão, Brazil, and the presence of both parasites with hygienic-
sanitary importance, complementary studies should be designed to allow us to understand the relationship between host
parasites and whether they could have zoonotic relevance.
Keywords:
Baixada Maranhense – endoparasites – helminths – Jurará – Nematoda - scorpion mud turtle
RESUMEN
Kinosternon scorpioides
(Linnaeus, 1766), conocido popularmente en Brasil como “Jurará”, es una especie de quelonio
que sirve como recurso alimenticio y fuente de ingresos para algunas familias del Nordeste de Brasil. En ese sentido, el
presente estudio tuvo como objetivo analizar los endoparásitos metazoarios que infectan a
K. scorpioides
de la Baixada
Maranhense, Brasil. Quince especímenes adultos fueron capturados utilizando trampas de embudo en campos inundados
alrededor del río Aurá, cerca de la ciudad de São Bento-Maranhão. Las muestras fueron transportadas al Postgraduate
Multi-User Research Laboratory- Laboratories in Postgraduate Research/Postgraduate in Animal Science ubicado en la
Universidad Estatal de Maranhão - UEMA para análisis parasitológicos. Los resultados revelaron la presencia de larvas de
Contracaecum
sp. infectando el estómago, intestino e hígado, mientras que
Eustrongylides
sp. Se encontró enquistado en
la musculatura, estómago, intestino y en el interior de un huevo de una tortuga de lodo hembra grávida. Los hallazgos
del presente estudio constituyen los primeros registros de estos nematodos parasitando a
K. scorpioides
. Dado que
K.
scorpioides
es consumido como alimento por algunas familias en el Estado de Maranhão, Brasil, y la presencia de ambos
parásitos con importancia higiénico-sanitaria, se deben diseñar estudios complementarios que nos permitan comprender
la relación entre los parásitos hospedadores y si pudieran tener relevancia zoonótica.
Palabras clave:
Baixada Maranhense – endoparásitos – helmintos – Jurará – Nematoda – tortuga de lodo escorpión
RESUMO
Kinosternon scorpioides
(Linnaeus, 1766) popularmente conhecido no Brasil como “Jurará” é uma espécie de quelônio que
serve como recurso alimentar e fonte de renda para algumas famílias no Nordeste do Brasil. Nesse sentido, o presente
estudo teve como objetivo analisar os endoparasitas metazoários que infectam
K. scorpioides
da Baixada Maranhense,
Brasil. Quinze espécimes adultos foram capturados usando armadilhas de funil em campos alagados ao redor do Rio
Aurá, próximo à cidade de São Bento-Maranhão. As amostras foram transportadas para o Laboratório de Pesquisa
Multiusuário de Pós-Graduação - Laboratórios de Pesquisa de Pós-Graduação/Pós-Graduação em Zootecnia localizado na
Universidade Estadual do Maranhão - UEMA para análises parasitológicas. Os resultados revelaram a presença de larvas
de Contracaecum sp. infectando o estômago, intestino e fígado, enquanto
Eustrongylides
sp. foi encontrado encistado na
musculatura, estômago, intestino e dentro de um ovo de uma tartaruga fêmea grávida. Os achados do presente estudo
constituem os primeiros registros desses nematoides parasitando
K. scorpioides
. Como
K. scorpioides
é consumido como
alimento por algumas famílias no estado do Maranhão, Brasil, e a presença de ambos os parasitas com importância
higiênico-sanitária, estudos complementares devem ser delineados para nos permitir entender a relação entre os parasitas
hospedeiros e se eles podem ter relevância zoonótica.
Palavras-chave:
Baixada Maranhense – endoparasitas – helmintos – Jurará – Nematoda – tartaruga-escorpião
Contracaecum
sp. and
Eustrongylides
sp. in
Kinosternon scorpioides
251
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INTRODUCTION
Maranhão is a State that encompasses three of the main
Brazilian morphoclimatic domains: Amazon, Caatinga,
and Cerrado. Te State represents an ecotone zone
between these biomes, with 14 distinct vegetation types
(IBGE, 2004), refecting the transition between humid
forests and semi-arid habitats (Da Silva, 2011).
Te Baixada Maranhense region, placed in Maranhão, is
located on the easternmost limit of the Amazon biome,
forming part of the Brazilian Legal Amazon. Tis region
is characterized by a landscape made up of lakes, felds,
foodplains, igapós, landflls, river-marine systems, and dry
land. Te foodable natural felds of Baixada Maranhense
are extremely complex environments from an ecological
point of view, with very diverse structures and functioning
(Costa-Neto
et al
., 2002; Pinheiro, 2013).
Due to the recognized importance of the region’s foodable
natural felds, the Government of the State of Maranhão
established the Baixada Maranhense Environmental
Protection Area (APA) with Decree No. 11,900 of June 11,
1991 (State of Maranhão, 1991). In 2000 it was designated
by the National Wetlands Committee (CNZU) as a Ramsar
Site: regions that provide fundamental ecological services -
meeting water and food needs - for species of fauna and
fora and human populations, rural and urban. In addition
to regulating the water regime of vast regions, they function
as a source of biodiversity at all levels. It has the largest set
of lake basins in the Northeast, which contribute to high
fshing productivity, the main basis of food and income
support for its population (Costa-Neto
et al
., 2002).
Chelonians are animals that perform important ecosystem
functions and are intrinsically linked in many traditional
cultures, from the consumption and seed dispersal of various
tree species to the important social role of communities
that use river systems as a means of subsistence (Alves
et
al
., 2008; Rhodin et al., 2018).
Kinosternon scorpioides
(Linnaeus, 1766) popularly known as the scorpion mud
turtle and commonly named in Brazil as “Jurará” is a species
of chelon widely distributed in the Neotropical region,
occurring from Panama, along the Caribbean mountain
range to Brazil, covering the entire Amazon forest, eastern
mountain ranges of Colombia, Ecuador, and Peru.
Historically, many species of chelonians in diferent
parts of the world have great nutritional, economic, and
cultural importance, with their eggs, meat, viscera, fat, and
shell being used intensively by humans (Van Dijk
et al
.,
2014). In Baixada Maranhense, species such as
Phrynops
geofroanus
(Schweigger, 1812) and mainly
Kinosternon
scorpioides
serve as a food resource and source of income for
some families, being captured illegally, in adult and sub-
adult form alive and hanging, and sold mainly from May
to August, when females appear ovate. Wild populations
are used for consumption as a regional delicacy, both
for subsistence and recreational consumption (Machado
Júnior
et al
., 2006; Medeiros, 2016).
According to Giari
et al.
(2022) in aquatic environments
there exist metazoan parasites with zoonotic potential
that can cause strong negative impacts on the safety and
quality of the meat. Tese parasites can be of public health
interest and can compromise the health of the consumers.
Humans can be infected accidentally with zoonotic
parasites by the ingestion of raw or poorly cooked meat
(Giari
et al
., 2022).
Due to the consumption of
K. scorpioides
meat by the
Brazilian population and the presence of parasites with
zoonotic potential in aquatic organisms, the present study
aimed to analyze the metazoan endoparasites infecting
K.
scorpioides
from the Baixada Maranhense, Brazil.
MATERIAL AND METHODS
Te study was carried out around the Aurá River, located
in the Baixada Maranhense Environmental Protection
Area (APA), in the Northeast of Brazil, on the eastern edge
of the Amazon (Figure 1). Tis area represents a wetland of
international importance (Ramsar Site), bringing together
a set of river basins and fooded felds, and seasonal periods
with great contrasts in temperature, humidity, and rainfall
(Costa-Neto
et al
., 2002; Mendes, 2018).
Te collections were carried out in fooded felds around
the Aurá River, city of São Bento-Maranhão (2°42’08,1”S,
44°51’40,3”W and 2°40’60,0”S, 44°49’00,0”W) (Fig.1).
Te animals were captured using funnel traps (Secco
et al
.,
2013; Balestra
et al
., 2016).
Captured animals presented 13,73 cm. mean carapace
length, 9,17 cm. mean carapace width, 12,60 cm.
mean plaston length, 7,97 cm. mean plaston width,
4,87 cm. mean height and 342,40 g. mean weight.
Samples were transported at the Postgraduate Multi-User
Research Laboratory- Postgraduate Multi-User Research
Laboratory- Laboratories in Postgraduate Research/
Postgraduate in Animal Science located at the State
University of Maranhão- UEMA Campus Paulo VI. Te
samples were collected in the region of the Municipality
of São Bento-MA, belonging to the APA of Baixada
Maranhense, Sítio Ramsar.
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Te musculature was analyzed and carefully observed.
Internal organs were analyzed using a stereoscope Leica
EZ4. Organs were placed in Petri dishes with distilled
water, and with the aid of tweezers and needles, the tissue
was examined by making fne cuts that allowed to observe
inside them. In the presence of any parasites, these were
removed with tweezers and preserved in ethanol 70% for
posterior taxonomic identifcation.
For taxonomic identifcation, cysts with nematodes were
placed in Petri dishes, and then, with the aid of needles,
the cysts were broken, liberating the larvae, and then
preserved in 70% ethanol for posterior analyses. For the
identifcation of nematodes, they were placed into glass
slides with Lactic Acid, which is used for the clarifcation
of parasite tissue and consequent visualization of external
structures and internal organs. All parasites mounted in
slides were observed under an optical microscope Leica
DM750. Based on the morphological characteristics
of the parasites, the identifcation was made using the
information of Moraveck (1998) and Morey
et al.
(2022).
Parasitological indices were calculated according to Bush
et al.
(1997).
Figure 1
. Study area. Identifcation of collection points distributed along the Aurá River (blue) A-Forest areas; B- Flooded
felds; C- Water areas (River). Source: IBGE (2018); ZEE (2019); MapBiomas (2021).
Ethic aspects
: Te collection of samples was carried
out under the permissions granted by the Biodiversity
Authorization and Information System (SISBIO),
number 85805-1.
RESULTS
Te nematodes
Contracaecum
sp. and
Eustrongylides
sp.
were found parasitizing
K. scorpioides
.
Contracaecum
sp.
was found in the stomach, intestine, and liver (Fig. 2, while
Eustrongylides
sp. was found encysted in the musculature
(Fig. 3) stomach, intestine and inside the egg of a gravid
female
K. scorpioides
(Fig. 4). Both parasites were found
encysted, being necessary to break the cyst to liberate the
larvae. Parasitological indices are presented in Table 1.
Contracaecum
sp. medium-sized nematodes, opaque-white
when alive. Transversely striated cuticles present and more
distinct at the extremities of the body, with the anterior
region interrupted by a short, lateral line. Te cephalic
extremity is rounded with a small, ventral cuticular tooth.
Te oesophageal muscle is narrow, the ventricle is small
and rounded, and the ventricular appendix is a short, long
intestinal caecum, extending anteriorly to the nerve ring.
Tail conical without mucron (Fig. 5A-C).
Contracaecum
sp. and
Eustrongylides
sp. in
Kinosternon scorpioides
253
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dec 2024
Figure 2
. A. Encysted
Contracaecum
sp. in internal organs of
Kinosternon scorpioides
. Black circles present the cyst of the
parasites. Scale bar: 2 cm.
Figure 3
. A.
Eustrongylides
sp. in the musculature of
Kinosternon scorpioides
. B. Cyst. C.
Eustrongylides
sp. being released
from a cyst. D. Free
Eustrongylides
sp. Scale bar: A, B = 2 cm. C-E = 0.5 cm
Lislea de Sousa
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Neotropical Helminthology (Lima). Vol. 18, N
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Eustrongylides
sp. presented a cephalic extremity with a
small oral cavity surrounded by 12 cephalic papillae of
similar size arranged in two concentric rings, and genital
primordia in the posterior part of the body (Fig. 5D-F).
According to the results of the present study, it can be
assumed that in the life cycle of
Eustrongylides
sp. and
Contracaecum
sp., diferent organisms are involved:
invertebrates play the role of intermediate hosts, while
fsh and
K. scorpioides
act as paratenic hosts. Finally,
given that
K. scorpioides
are preyed upon by Amazonian
alligators, it can be inferred that they act as fnal hosts for
these nematodes in territories of the Baixada Maranhense,
Maranhão, Brazil (Fig. 6).
DISCUSSION
Studies focusing on South American turtles are still
recent and scarce (Bursey & Brooks, 2011; Mascarenhas
et al
., 2013). Few studies have examined the nematodes
parasites of
K. scorpioides
in Brazil:
Serpinema magathi
from specimens collected in Pará (Alho, 1965); Freitas and
Dobbin Jr. (1971) from Pernambuco;
S. monospiculatus
from specimens collected in a semiarid region in the
Northeast (Pereira
et al
., 2018):
S. pelliculatus
was found
from the gastrointestinal tract of specimens collected in
Baía do Capim (municipality of Abaetetuba) and Ilha do
Marajó (municipality of Soure), Pará, Brazil (Silva
et al
.,
2023). Tese parasites are commonly found in freshwater
turtles worldwide (Hidalgo-Vila
et al
., 2009; Bursey &
Brooks, 2011; Moraga
et al
., 2012; Mascarenhas
et al
.,
2013; Mascarenhas & Muller, 2015).
Figure 4.
A.
Eustrongylides
sp. in an egg of
Kinosternon scorpioides
. Te black arrow indicates the egg with the parasite. B.
Broken egg showing the nematode inside. Scale bar: 2 cm.
Table 1
. Parasitological indices of endoparasites reported in Kinosternon scorpioides. AS = Analyzed specimen. PS =
Parasitized specimen. P% = prevalence. TNP = total number of parasites. mI = mean intensity of infection. mA = mean
abundance of infection.
ParasiteASPSP%TNPmImA
Contracaecum
sp.151173.33191.720.73
Eustrongylides
sp.151280322.662.13
Contracaecum
sp. and
Eustrongylides
sp. in
Kinosternon scorpioides
255
Neotropical Helminthology (Lima). Vol. 18, N
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Figure 5.
A. Microphotography of the anterior part of
Contracaecum
sp. Dark circle showing intestinal cecum. B.
Microphotography of larval tooth (dark circle). C. Microphotography of the tail of
Contracaecum
sp. D. Encysted
Eustrongylides
sp. E. Microphotography of the anterior part of
Eustrongylides
sp. F. Microphotography of the tail of
Figu re 6
. T e life cycle of Nematoda larvae of
Eustrongylides
sp. and
Contracaecum
sp. 1. Nematoda eggs are liberated from
the alligator. 2. Eggs with infective L1 larvae. 3. Eggs are consumed by an annelid (for
Eustrongylides
sp.) or for a copepod
(for
Contracaecum
sp.). Nematoda larvae develop inside the invertebrates from L1 into L2 and L3. Invertebrates act as
intermediate hosts. 4. Fish consume the invertebrates with Nematoda larvae. Fish are paratenic hosts. 5. Fish are consumed
by
Kinosternum scorpioides.
T e mud turtle acts as a paratenic host. 6.
Kinosternon scorpioides
are consumed by an alligator.
T e alligator acts as the f nal host of Nematoda larvae of
Eustrongylides
sp. and
Contracaecum
sp.
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For northeastern Brazil, the nematodes
Serpinema magathi
and Spiroxys fgueiredoi
have been found in the digestive
tract of
K. scorpioides
(Viana
et al
., 2016). In the present
study, none of these nematodes were found on specimens
captured in the municipality of São Bento, Maranhão,
Brazil. In the present study, the fndings of
Contracaecum
sp.
and
Eustrongylides
sp. are the frst records of
K. scorpioides
.
Since
K. scorpioides
is an omnivorous species that feeds
on algae, plants, seeds, and a variety of insects, mollusks,
fsh, and small amphibians (Berry & Ivwerson, 2001;
Berry & Iverson, 2011), its feeding habits facilitate the
infection of this freshwater turtle by diferent parasitic
nematode larvae present in aquatic environments, such as
Contracaecum
spp. and
Eustrongylides
spp.
Contracaecum
larvae show low specifcity, are often found
in abnormal hosts, and do not develop into adults in turtles
(Shubber
et al
., 2020). In this sense, it can be assumed
that
K. scorpioides
acquired the nematodes by feeding on
fshes in their ecosystems, a fact that was supported by a
personal observation made in the feld during the capture
of the animals in this study.
In the life cycle of
Eustrongylides
spp. freshwater
oligochaetes act as intermediate hosts; fsh as paratenic
hosts and birds as fn7al hosts (Spalding, 2008).
Eustrongylides
spp. can infect poikilothermous hosts, as
was demonstrated by experimental infections with piscine,
amphibians, and reptilian hosts (Cooper
et al
., 1978). Te
presence of nematode larvae in
K. scorpioides
indicates
that this turtle acts as the paratenic host of
Contracaecum
sp. and
Eustrongylides
sp. Natural predators of this mud
turtle are documented as jaguars (Savage, 2002), owls
(Pereira
et al
., 2007), vultures, green iguanas (Acuña-
Mesén, 1998), and alligators (Savage, 2002). Te presence
of
Eustrongylides
sp. inside the egg of a gravid female
K.
scorpioides
can be assumed as a strategy of the parasite to
reach easily the fnal host, since eggs deposited by females
are more vulnerable to predators, being predated by birds,
terrestrial mammals, and reptiles, facilitating the contact
of the nematode with the fnal host.
In that way, due to the feeding habitat of this chelonian,
it is assumed that invertebrates are the intermediate hosts,
fsh, and
K. scorpioides
paratenic hosts, and alligators are
the fnal hosts.
Kinosternum scorpioides
from the Baixada Maranhense
are parasitized by the nematodes
Contracaecum
sp. and
Eustrongylides
sp. Since
K. scorpioides
is consumed as
food for some families in the State of Maranhão, Brazil,
and the presence of both parasites with hygienic-sanitary
importance, complementary studies should be designed
to allow us to understand the relationship between host
parasites and whether they could have zoonotic relevance.
Author contributions: CRediT (Contributor Roles
Taxonomy)
ALS
= Alana Lislea de Sousa
AMM
= Almerinda Macieira Medeiros
JBA
= Júlia Boáis Almeida
SCSDA
= Silmara Cristina Silva de Aquino
ECFJ
= Elias Costa Ferreira Junior
DCV
= Diego Carvalho Viana
VPN
= Victor Puicón N.
GAMM
= Germán Augusto Murrieta Morey
Conceptualization
: ALS, AMM, JBA, ECF, DCV, ECF,
DCV, GAMM
Data curation
: ALS, GAMM
Formal Analysis
: ALS, GAMM
Funding acquisition
: AMM, JBA, SCSDA, GAMM
Investigation
: SCSDA, ECF, DCV, VPN, GAMM
Methodology
: ALS, AMM, JBA, SCSDA, ECF, DCV,
VPN, GAMM
Project administration
: ALS, AMM, JBA, GAMM
Resources
: AMM, JBA, ECF, DCV, GAMM
Software
: SCSDA, GAMM
Supervision
: AMM, JBA, GAMM
Va
lidation
: ALS, AMM, JBA, SCSDA, ECF, DCV,
GAMM
Visualization
: ALS, AMM, JBA, SCSDA, ECF, DCV,
VPN, GAMM
Writing – original draft
: ALS, AMM, JBA, SCSDA,
ECF, DCV, VPN, GAMM
Writing – review & editing
: ALS, AMM, JBA, SCSDA,
ECF, DCV, VPN, GAMM
ACKNOWLEDGMENTS
We wish to thank the Maranhão State Foundation for
Research Development (FAPEMA) for the fellowship
granted to SCSDA (002832/2023) and to GAMM
(000448/2023).
Contracaecum
sp. and
Eustrongylides
sp. in
Kinosternon scorpioides
257
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2, jul - dec 2024
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