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Neotropical Helminthology
Neotropical Helminthology, 2023, vol. 17 (2), 265-270
RESEARCH NOTE / NOTA CIENTÍFICA
SUBCUTANEOUS
STRIGEA
SP. (DIPLOSTOMOIDEA: STRIGEIDAE)
METACERCARIAE IN RALLIDAE (GRUIFORMES) FROM THE NEOTROPICAL
REGION
METACERCARIAS DE
STRIGEA
SP. (DIPLOSTOMOIDEA: STRIGEIDAE)
SUBCUTÁNEAS EN RALLIDAE (GRUIFORMES) DE LA REGIÓN
NEOTROPICAL
José Junior dos Santos
1
*, Carolina Silveira Mascarenhas
2
& Gertrud Müller
1
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.24039/rnh20231721694
Volume 17, Number 2 (jul - dec) 2023
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 Programa de Pós-graduação em Microbiologia e Parasitologia, Laboratório de Parasitologia de Animais Silvestres
(LAPASIL), Instituto de Biologia, Departamento de Microbiologia e Parasitologia, Universidade Federal de Pelotas
(UFPel), Campus Universitário S/N, CEP 96160-000, Capão do Leão, RS, Brazil.
² Instituto Federal Sul-rio-grandense (IFSul), Campus Pelotas, Praça Vinte de Setembro, 455, Centro, CEP 96015-360, RS,
Brazil. phrybio@hotmail.com /
gertrudmuller40@gmail.com
* Corresponding author
:
j.therion@unochapeco.edu.br
José Junior dos Santos:
https://orcid.org/0000-0002-3910-0901
Carolina Silveira Mascarenhas:
https://orcid.org/0000-0002-7045-0926
Gertrud Müller:
https://orcid.org/0000-0002-2213-6721
ABSTRACT
T e life cycle of species belonging to
Strigea
remains complex and poorly understood, especially in the Neotropical region,
where information about their intermediate hosts is scarce. Rallidae birds are known for their adaptability to aquatic and
semi-aquatic environments since they exhibit the ability to disperse and adjust to a wide range of ecological conditions.
In this study, we examined seventeen specimens of
Pardirallus maculatus
(Boddaert, 1783) and one of
Pardirallus
sanguinolentus
(Swainson, 1838) collected in southern Brazil in search for
Strigea
sp. metacercariae. Metacercariae
occurred in 11.1% (2/18) of birds with infection intensity of 12 (
Strigea
sp. 2) and 28 (
Strigea
sp. 1) helminths found
in
P. sanguinolentus
and
P. maculatus
, respectively. Metacercariae were found exclusively in the pectoralis muscle region,
beneath subcutaneous tissue. T ese f ndings suggest the potential that Rallidae birds have to act as intermediate hosts of
Strigea
spp. in that region. T ey are reinforced by previous observations of small aquatic birds which were identif ed as
prey of Falconiformes (def nitive hosts). T us, our study provides novel information that may assist further research that
aims at expanding our understanding of the life cycle of
Strigea
spp. and at enhancing our knowledge of biodiversity by
revealing new geographic distribution and intermediate hosts.
Keywords:
Digenea –
Pardirallus maculatus
–
Pardirallus sanguinolentus
– plumbeous rail – spotted rail
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RESUMEN
El ciclo de vida de las especies pertenecientes al género
Strigea
sigue siendo complejo y poco comprendido, especialmente
en la región neotropical, donde la información sobre sus hospederos intermediarios es escasa. Las aves Rallidae son
conocidas por su adaptabilidad en entornos acuáticos y semiacuáticos, demostrando habilidades de dispersión y
capacidad de ajuste a una amplia gama de condiciones ecológicas. En este estudio, examinamos diecisiete especímenes
de
Pardirallus maculatus
(Boddaert, 1783) y uno de
Pardirallus sanguinolentus
(Swainson, 1838) recolectados en el sur
de Brasil en busca de metacercarias de
Strigea
sp. Se encontraron metacercarias en el 11,1% (2/18) de las aves, con
una intensidad de infección de 12 (
Strigea
sp. 2) y 28 (
Strigea
sp. 1) helmintos en
P. sanguinolentus
y
P. maculatus
,
respectivamente. Las metacercarias se encontraron exclusivamente en la región del músculo pectoral, debajo del tejido
subcutáneo. Estos hallazgos sugieren el potencial de las aves Rallidae como hospederos intermediarios de
Strigea
spp. en
la región, respaldado por observaciones previas de aves acuáticas pequeñas identifcadas como presas de Falconiformes
(hospederos defnitivos). Por lo tanto, nuestro estudio aporta nueva información que puede ayudar en investigaciones
futuras destinadas a ampliar nuestra comprensión del ciclo de vida de
Strigea
spp. y mejora nuestro conocimiento de la
biodiversidad al revelar nuevas distribuciones geográfcas y hospederos intermediarios.
Palabras clave
: Digenea –
Pardirallus maculatus
–
Pardirallus sanguinolentus
– riel moteado – riel plomizo
INTRODUCTION
Strigeidae Railliet 1919 (Digenea) is composed of species
with a cup-shaped forebody and holdfast organ in the
form of two lobes, which commonly parasitize birds
(defnitive hosts) (Niewiadomska, 2002). Metacercariae
are transmitted trophically through ingestion of
intermediate hosts (Niewiadomska & Pojmańska,
2011).
Strigea
Abildgaard, 1790 comprises 45 known
species which develop into their adult forms in birds of
prey (Lunaschi & Drago, 2013). Unlike other strigeids,
species in this genus have four hosts in their life cycle,
i. e., mollusks (frst-order intermediate hosts), anurans
and snakes (second-order intermediate hosts), in which
mesocercariae develop, and amphibians, fsh, snakes,
birds and mammals (third-order intermediate hosts), in
which ‘tetracotyle’ metacercariae develop (Lutz, 1933;
Niewiadomska, 2002).
Tetracotyles (metacercariae) are mainly found
encapsulated and encysted in subcutaneous tissue,
intercostal muscles, inner thighs and the neck region,
but also in bird pectoralis (intermediate hosts), with no
records in the body cavity (Pearson, 1959; Awad & Al-
Tameemi 2014). A metacercaria is composed of a fbrous
capsule with a viscous fuid separating the capsule from
the cyst (Wittrock
et al
., 1991).
Rallidae birds have representatives in all habitable
continents. Tey are both aquatic and semi-aquatic
birds with remarkable ability to disperse and adapt
to a wide range of ecological conditions (García
et al
.,
2014).
Pardirallus maculatus
(Boddaert, 1783) is typically
associated with areas of aquatic vegetation in wetlands,
since it depends on this ecological structure for foraging
and nesting (Navas, 1991). Te species is recorded from
North America to the southern continent (De La Peña
& Rumboll, 1998). Its diet consists mainly of insects but
may also include mollusks and small vertebrates, such
as tadpoles and fsh, as food resources (Navas, 1991).
Pardirallus sanguinolentus
(Swainson, 1838) is a small-
sized species found in the Americas; it inhabits all types
of wetlands with vegetation that provides shelter, nesting
resources and foraging opportunities (Clements
et al
.,
2023). Te species is insectivorous but also consumes
mollusks, crustaceans and plants (Goodal
et al
., 1951;
Taylor & Bonan, 1996).
Even though there are records of birds which are as
hosts of metacercariae of the species
Strigea
, there is
scarce information on their life cycle. Metacercariae
(tetracotyles) have been described in Brazil parasitizing
Sterna
sp. (Laridae) (Lutz, 1933). In Germany and Iraq,
they have been associated with
Buteo buteo
(Linnaeus,
1758) (Accipitridae) (Krone & Streich, 2000) and
Ardeola ralloides
(Scopoli, 1769) (Ardeidae) (Awad & Al-
Tameemi, 2014), respectively. In the Neotropical region,
there are no records of other birds that participate in the
cycle as intermediate hosts, in addition to the previously
described defnitive hosts (Lunaschi & Drago, 2013).
Terefore, this study aims at recording
P. maculatus
and
P. sanguinolentus
as intermediate hosts of
Strigea
spp. and
at providing morphometric information on cysts and
metacercariae.
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Strigea
Metacercariae in Rallidae birds.
Neotropical Helminthology (Lima). Vol. 17, N
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MATERIAL AND METHODS
Seventeen specimens of
P. maculatus
and one specimen
of
P. sanguinolentus
collected in Pelotas (31°44’45.6”S -
52°21’43.3”W), Rio Grande do Sul (RS), Brazil, were
examined. Te birds were donated by the Núcleo de
Reabilitação da Fauna Silvestre and Centro de Triagem
de Animais Silvestres which belongs to the Universidade
Federal de Pelotas (NURFS/CETAS/UFPel) where the
animals died during the rehabilitation process. Te hosts
were individually frozen and subsequently necropsied.
In the necropsy process, skin was detached from muscles.
All organs were removed and individually separated
(esophagus, trachea, proventriculus, gizzard, heart, lungs,
stomach, small and large intestines, ceca, kidneys, liver
and cloaca). Ten, they were washed through a 150µm
mesh sieve. Metacercariae were counted and isolated
from host tissues and removed from cysts by preparation
needles. Metacercariae were fxed in cold AFA (70ºGL
ethanol, 37% formalin and glacial acetic acid) for 48
hours and preserved in 70ºGL ethanol. Specimens were
stained with Langeron’s carmine and mounted in Canada
balsam. Helminth identifcation followed Niewiadomska
(2002) and Hamann
et al
. (2023). Voucher specimens
were deposited in the Helminthological Collection at the
Instituto Oswaldo Cruz (CHIOC) Rio de Janeiro, Brazil
(CHIOC 39648, 39649, 40269a-j, 40285a-f).
Measurements are expressed as micrometers (µm) and
minimum and maximum values are shown between
parentheses. Parasitological indices of prevalence and
mean abundance of infection were estimated in agreement
with Bush
et al
. (1997). Illustrations were created in ink
and assembled by the GIMP 2.10 software program.
Ethic aspects
: For this study, formal consent is not
required.
RESULTS
Two (11.1% - one of each species) out of eighteen birds
under investigation were parasitized by
Strigea
spp.
metacercariae. Infection intensities were 28 metacercariae
– with mean abundance of 1.64 and prevalence of 5.8% –
in
P. maculatus
and 12 metacercariae in
P. sanguinolentus
.
Metacercariae were found only in chest muscle region
beneath subcutaneous tissue (Fig. 1). Two morphotypes
were identifed, i. e., one in each host species.
Strigea
spp.
1 occurred in
P. maculatus
while
Strigea
sp. 2 was found
in
P. sanguinolentus
.
Figure 1 -
Cysts in the pectoral muscle region in
Pardirallus maculatus
(Boddaert, 1783)
(Rallidae) from southern Brazil.
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et al
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Strigea
sp. 1
(Fig. 2 A - B)
Total length of the metacercariae (tetracotyle) (Fig. 2A) is
410±25 (390 – 450) and its width is 278±16 (260 – 300).
Oral sucker is 50±4 (45 – 55) long and 60±4 (55 – 65)
wide. Ventral sucker is 72±8 (65 – 85) long and 110±8
(100 – 120) wide. Left pseudosucker is 100±16 (80 –
120)long and 80±8 (70 – 90) wide. Right pseudosucker
is 80±8 (70 – 90) long and 100±16 (80 – 120) wide.
Round cysts (Fig. 2B) consist of three layers; both outer
layers are thicker than the inner one. Te frst outer layer
is fbrous and originates from the host’s immune response
while the third layer, near the metacercariae, is hyaline
and fragile. Total length of the cyst is 574±52 µm (560 –
640)and its width is 453±52 (400 – 515). Te frst outer
layer is 60±9 (50 – 75) thick while the second layer is
70±7 (60 – 80) thick and the hyaline layer closer to the
metacercariae is 69±5 (60 – 75) thick.
Strigea
sp. 2
(Fig. 2 C - D)
Total length of the metacercariae (tetracotyle) (Fig. 2C)
is 458±28 (430 – 500) and its width is 208±13 (200 –
230). Oral sucker is 80±2 (78 – 84) long and 70±4 (65
–75) wide. Ventral sucker is 80±4 (75 – 85) long and
97±4 (90 – 100) wide. Left pseudosucker is 90±6 (80 –
95)long and 77±4 (70 – 80) wide. Right pseudosucker is
77±4 (70 – 80) long and 90±6 (80 – 95) wide.
Oval cysts (Fig. 2 D) are composed of two layers; the
outer layer is thicker than the inner one, which is near the
metacercariae and is hyaline and fragile. Te metacercariae
occupies most of the cyst. Total length is 510±25 (490 –
550)and width is 315±17 (290 – 330). Te outer layer
is 37±2 (35 – 40) thick while the inner layer is 37±2 (35
–40) at the most distant ends of metacercariae.
Figure 2.
Metacercaria (A, C) and cyst (B, D) of
Strigea
spp. associated with Rallidae birds from southern Brazil.
A – B.
Strigea
sp. 1 found in
Pardirallus maculatus
(Boddaert, 1783).
C – D.
Strigea
sp. 2 found in
Pardirallus sanguinolentus
(Swainson, 1838).
Figure 2.
Metacercaria(A, C) and cyst
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DISCUSSION
Te life cycle of
Strigea
species is poorly understood and
complex, especially in the Neotropical region, where
there are few reports about their hosts (Lunaschi
et al
.,
2007). Parasitic relations between intermediate hosts and
Strigea
spp. are infuenced by the diversity and structure
of the environment in which they are found (Lutz 1933;
Pearson, 1959). Furthermore, complexity of the life cycle
depends on three intermediate hosts for metacercariae to
develop and complete their cycle in defnitive hosts (Lutz,
1933).
Findings of encysted metacercariae in subcutaneous
tissue of Rallidae birds from southern Brazil corroborate
information reported by Krone & Streich (2000) and
Awad & Al-Tameemi (2014). A study carried out by
Krone & Streich (2000) examined 77 birds (
B. Buteo
)
from three locations in Germany and found prevalence
ranging from 10% to 58% and infection intensity from 2
to 76 metacercariae found in the neck connective tissue.
Awad & Al-Tameemi (2014) do not mention the number
of metacercariae found in each host. Infection indices
in Rallidae birds were higher than the ones found in
A.
ralloides
(8.6%)(Awad & Al-Tameemi, 2014) and lower
than the ones found in
B. buteo
(41%) (Krone & Streich,
2000). Although encysted metacercariae have been found
in
B. buteo
(Krone & Streich, 2000) which is normally
considered a defnitive host (Lunaschi 2013), Krone
& Streich (2000) pointed out that, in this record, the
falconiform would be acting as a third-order intermediate
host.
Te authors suggested that high prevalence of
metacercariae in
B. buteo
may be linked to abundance of
fooded areas, which results in high availability of second-
order intermediate hosts (Krone & Streich, 2000). In
contrast, fndings of this study suggest that Rallidae
birds may potentially play the role of intermediate hosts
of
Strigea
spp. in the region. It is based on the previous
observation that small aquatic birds have been identifed
as part of the diet of falconiforms in the Neotropical
region (Silva, 1997; Bó
et al
., 2007). Tis pattern may be
explained by the active hunting behavior of birds of prey
in open areas, as reported by Bó
et al
. (2007).
Tis study is the frst record of
Strigea
metacercariae in
Rallidae birds and increases our understanding of the
diversity of helminths associated with them and the life
cycle of strigeids in the Neotropical region. Need for
further studies to comprehend the role of these birds
in the transmission dynamics of digeneans is evident.
Furthermore, it is essential to consider the signifcance
of parasitic diversity in ecosystems, especially because
human activities have altered trophic dynamics and,
consequently, have afected parasitic biodiversity (Gómez
& Nichols, 2013; Strona, 2015). Tus, documentation of
new trophic interactions plays a crucial role in supporting
conservation strategies.
A
CKNOWLEDGEMENTS
Special thanks to the Núcleo de Reabilitação da Fauna
Silvestre and the Centro de Triagem de Animais Silvestres
(NURFS/CETAS/UFPel) for donating the birds and to
André Mota Alves for the illustration work. Tis study
was funded by the Coordenação de Aperfeiçoamento do
Pessoal de Nível Superior (CAPES) (process no. 32/2010)
and by the doctoral fellowship granted to JJS in the Post-
graduate Program in Microbiology and Parasitology
(PPGMPar) at UFPel in Pelotas, RS, Brazil.
Author contributions: CRediT (Contributor Roles
Taxonomy)
JJS
= José Junior dos Santos
CSM
= Carolina Silveira Mascarenhas
GM
= Gertrud Müller
Conceptualization
: JJS, CSM
Data curation
: JJS
Formal Analysis
: JJS, CSM, GM
Funding acquisition
: GM
Investigation
: JJS
Methodology
: JJS, CSM, GM
Project administration
: JJS
Resources
: JJS, CSM, GM
Software
: JJS, CSM
Writing – review & editing
: JJS, CSM, GM
A
T
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.
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