image/svg+xml
Reports of filarial nematodes in wild birds are scarce in South America, particularly in the Amazon region.
We analyzed the organs in the thoracic and abdominal cavities of 34 wild birds belonging to 12 different
species of the order Passeriformes in the Periurban areas of Para State. Adult filariae was observed in 3/34
(9%) birds, located in the abdominal cavity of hosts. The morphological and morphometric characteristics
of the filarial nematodes were consistent with the taxonomic classification of
Aproctella stoddardi
Cram,
1931, making this the first report of this species in the Amazon region in northern Brazil. Due to the
observed migration of other genera of filariae,
Aproctella
Cram, 1931 may have the ability to infection at
other sites, such as the liver, heart, lung, and brain. In addition, it is necessary to expand the records of the
presence of filariae in birds of the region to elucidate the factors that influence this infection.
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:199-204.
RESEARCH NOTE / NOTA CIENTÏFICA
1
Laboratório de Patologia Animal (LABOPAT), Instituto da Saúde e Produção Animal (ISPA), Universidade Federal Rural
da Amazônia (UFRA), Av. Presidente Tancredo Neves n. 2501. CEP 66077-901 Bele
́m, PA, Brazil.
2
Museu de Zoologia, Instituto da Saúde e Produção Animal (ISPA), Universidade Federal Rural da Amazônia (UFRA), Av.
Presidente Tancredo Neves n. 2501. CEP 66077-901 Belém, PA, Brazil.
3
Programa de Pós-Graduação em Saúde e Produção Animal na Amazônia, Universidade Federal Rural da Amazônia (UFRA),
Av. Presidente Tancredo Neves 2501, Terra Firme, 66077-830, Belém-Pará, Brazil.
*Corresponding author:
E-mail: daket17@hotmail.com.
Adriane M. P. Rabelo: https://orcid.org/0000-0001-5469-8393
Jane D.F. Correa: https://orcid.org/0000-0002-0416-2184
Andréa M. Bezerra: https://orcid.org/0000-0002-7656-1109
Washington L.A. Pereira: https://orcid.org/0000-0001-7140-8124
David M.F. Conga: https://orcid.org/0000-0003-2891-6531
11 21, 3
Adriane M. P. Rabelo; Jane D. F. Corrêa; Andréa M. Bezerra; Washington L. A. Pereira & David M. F.
1,3*
Conga
Neotropical Helminthology
199
DOI: http://dx.doi.org/10.24039/rnh20221621464
FILARIAL INFECTION BY
APROCTELLA STODDARDI
CRAM, 1931 (NEMATODA:
ONCHOCERCIDAE) IN PASSERIFORMES FROM PERIURBAN AREAS, PARÁ STATE, BRAZIL
INFECCION FILARIAL DE
APROCTELLA STODDARDI
CRAM, 1931 (NEMATODA:
ONCHOCERCIDAE) EN PASSERIFORMES DE AREAS PERIURBANAS, ESTADO DE PARÁ. BRASIL
D
ABSTRACT
Key words:
Brazilian Amazon – Filarial – Onchocercidae – Wild Birds
D
D
D
D
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
Birds of the order Passeriformes have a worldwide
distribution, with greater diversities in tropical and
subtropical regions. They function as plant
pollinators, seed dispersers, and pest controllers,
contributing to the ecological balance (Almeida
et
al
., 2018). Passeriformes are hosts for various
parasitic agents (Berto
et al
., 2011; Magalhães-
Matos
et al
., 2016; Santos
et al
., 2020), within
which helminths are the most frequent in free-
living birds, including nematodes
Capillaria
Zeder, 1800,
Dispharynx
Rudolphi, 1819 and
acanthocephalan
Mediorhynchus
Van Cleave,
1916
,
the genera of helminths predominantly found
in the gastrointestinal tract (Mascarenhas
et al
.,
2009; Souza
et al
., 2019).
Within the Onchocercidae family, 16 genera are
observed infecting the lungs, joints, and abdominal
and thoracic cavities of wild birds, including
Andersonfilaria
Bartlett & Bain, 1987,
Aproctella
Cram, 1931,
Aproctiana
Skrjain, 1934
,
Cardiofilaria
Ström 1937
, Chandlerella
Yorke &
Maplestone, 1926,
Dessetfilaria
Bartlett & Bain,
1987,
Eufilaria
Seurat, 1921,
Eulimdana
Founikoff, 1934,
Lemdana
Seurat, 1917,
Paronchocerca
Peters, 1936
Pelecitus
Railliet &
Henry, 1910,
Pseudlemdana
Sonin & Shumilo,
1964
Sarconema
Wehr, 1939,
Splendidofilaria
Skrjabin, 1923,
Striatofilaria
Lubimov, 1927, and
Struthiofilaria
Noda & Nagata, 1976, some of
which, such as
Splendidofilaria caperata
Hibler,
1964, are associated with severe lung damage in
American crows and by microfilariae in boreal
Reportes de nematodos filarias en aves silvestres son escasos en América del Sur, principalmente en la
región amazónica. Fueron analizados los órganos de las cavidades torácica y abdominal de 34 aves
silvestres pertenecientes a 12 especies diferentes de aves Passeriformes en áreas periurbanas del Estado de
Pará. Filarias adultas fueron observadas en 3/34 (9%) aves, localizadas en la cavidad abdominal de los
huéspedes Las características morfológicas y morfométricas de los nematodos fueron compatibles con la
clasificación taxonómica de
Aproctella stoddardi
Cram, 1931, siendo este el primer relato de esta especie
en la amazónica en el norte de Brasil. Debido a la migración observada de otros géneros de filarias,
Aproctella
Cram, 1931
puede tener la capacidad de infección en otros sitios, como hígado, corazón,
pulmón y cerebro. Además, es necesario ampliar los registros de filarias en aves de la región para elucidar
los factores que influencian esta infección.
200
Neotropical Helminthology, 2022, 16(2), jul-dic
RESUMEN
Palabras clave:
Amazonia brasileña – Aves silvestres – Filarias – Onchocercidae
INTRODUCTION
owls (Bartlett & Anderson, 1981; Atkinson
et al
.,
2009; Larrat
et al
., 2012). Despite the knowledge
about the great number and diversity of birds in the
Amazon region, the records of filarial nematodes in
these hosts are scarce. Therefore, we report the
occurrence of filarial nematodes in free-living
Passeriformes in the periurban areas of Pará State,
Brazil.
During the period from January 2018 to August
2019, 34 wild birds of the Order Passeriformes
originating from free living and collected for
wildlife monitoring belonging to the species were
analyzed:
Ammodramus humeralis
Bosc, 1792
(n=2),
Turdus leucomelas
Vieillot, 1818
(n=7),
Myiothlypis flaveola
Baird, 1865
(n=1),
Dendrocinela fuliginosa
Vieillot, 1818
(n=3),
Sporophila nigricollis
Vieillot, 1823
(n=2),
Sporophila castaneiventris
Cabanis,1849
(n=1),
Zonotrichia capensis
Statius Müller, 1776
(n=2),
Saltator maximus
Statius Müller,1776
(n=1),
Ramphocelus carbo
Pallas,1764
(n=5),
Schistochlanys melanopis
Latham, 1790
(n=1),
Pitangus sulphuratus
Linnaeus, 1766
(n=2),
Tachyphonus rufus
Boddaert,1783
(n=1) and six
specimens that, due to their poor state of
conservation, could not be identified. The birds
were necropsied at the Animal Pathology
Laboratory of the Federal Rural University of the
Amazon (LABOPAT-UFRA) and were deposited
in the Zoology Collection of the Federal Rural
University of the Amazon - MZUFRA (deposit
MATERIAL AND METHODS
Rabelo
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
201
codes: MZUFRA birds-037), 1 bird from the
Zoobotanic Park Mangal das Garças (S 1°
27'49.082 ", W 48°30'19.552"), 18 birds from
UFRA - Campus Belém (S 1°27'21.380 "S, W
48°26'15.893" ) and 15 birds from the Serra Leste
Fauna Monitoring Program in Curionópolis-Pará
(S5°58'12.886 ", W49°37'43.115").
To obtain the helminths, the thoracic-abdominal
cavity and the gastrointestinal organs:
proventriculus, ventriculus, duodenum and
jejunum ileum, cecum and liver, were analyzed and
the adult specimens were removed and preserved in
70ºGL ethanol. Subsequently, the specimens were
clarified with Amann's Lactophenol for the
observation of internal structures according to the
nematode protocol by Amato & Amato (2010) and
identified according to the taxonomic keys of
Anderson & Chabaud (1959). For the measurement
and obtaining of the photos of the helminths found,
a Moticam10 camera coupled to the Zeiss Primo
Star light microscope was used.
Ethic aspects:
The study was approved by the
Ethics Committee on the Use of Animals of Federal
Rural University of the Amazon (CEUA-UFRA)
under protocol nº 034/2014 (CEUA) - 23084-
022512 / 2014-2018. The authors assert that all
procedures contributing to this study was
conducted in accordance with bioethical
requirements at the Universidade Federal Rural da
Amazônia.
Of the 34 birds analyzed, adult filariae were
observed in three (9%). One male specimen was
found in the final portion of the large intestine of
the host
D. fuliginosa
; two specimens (one male
and one female) were found in the initial portion of
the small intestine within the abdominal cavity in
the host
T. leucomelas
and one female specimen
was found in the liver capsule of the host
T. rufus
(Fig. 1A). In general, the average intensity of
infection was 1.6 specimens/host. Two infected
birds came from the Curionópolis region, while
one from the Universidade Federal Rural da
Amazonia, Belém, State of Pará, Brazil.
The nematodes morphologically presented as
small, fine, whitish worms. The morphometric
description, which was based on two male and two
female specimens (Fig. 1), showed a small, circular
oral aperture with a slight projection from the oral
opening (Fig. 1C) and four pairs of small cephalic
papillae around the oral aperture. Males had
7.5–8.3 mm long and 108–123 µm wide. The short
esophagus apparently without division was
370–400 µm. The nerve ring was located 110–130
µm from the anterior end (Fig. 1B). Short, robust,
slightly, curved spicules, left 99–104 µm and right
90–99 µm length (Fig. 1H). The tail was 63–72 µm
long, with a cloacal opening located at the posterior
end, and caudal papillae were absent (Fig. 1G).
The females were 14.7–15.1 mm long and 119–141
µm wide. The esophagus was 360–392 µm long.
The nerve ring was 145–150 µm long from the
anterior end (Fig. 1D). The vulvar aperture
posterior to the esophagus was 0.77–1.42 mm long
from the anterior end (Fig. 1E). The anal aperture
was located at the posterior end of the body. The tail
with a rounded tip measured 110.5–160 µm in
length (Fig. 1F). The filarid specimens were
classified as
Aproctella stoddardi
Cram, 1931
(Nematoda: Onchocercidae) owing to the post-
esophageal position of the vulvar aperture,
presence of an esophageal tooth in the oral
aperture, and absence of caudal papillae in the male
specimen, consistent with studies by Anderson &
Chabaud (1959), Sonin & Barus (1968), and Bain
et al
. (1981).
Filarial species of the genus
Aproctella
are non-
specific to their definitive hosts, including various
taxonomic orders of birds. Currently, four species
of
Aproctella
are registered in the Americas for
parasitizing the peritoneal cavity:
A. carinii
Pereira
& Vaz, 1933, reported in Passeriformes and
Pelecaniformes in southern Brazil (Mascarenhas
et
al
., 2009; Scheer
et al
., 2019);
A. alessandroi
,
Bain, Petit, Kozek & Chabaud, 1981 registered as
Passeriformes
Thraupis episcopus
Linnaeus, 1766
in Colombia;
A. golvani
Bain, Petit, Kozek &
Chabaud, 1981 in Passeriformes
Quiscalus
lugubris
Swainson, 1838 and
Loxigilla noctis
Linnaeus, 1766 in Petit-Bourg, Central America
(Bain
et al
., 1981); and
A. stoddardi
, initially
reported in Galliformes, Coraciformes, and
Passeriformes in the United States and Canada
(Anderson, 1957; Anderson, 1961; Boyd, 1966)
and later observed in 14 species of birds
Neotropical Helminthology, 2022, 16(2), jul-dic
RESULTS AND DISCUSSION
Filarial infection in Passeriformes
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
202
Strigiformes, Psittaciformes, Piciformes, and
Passeriformes in the island of Cuba (Sonin &
Barus, 1968) and
Thraupis sayaca
Linnaeus,1766
in southern Brazil (Pinto
et al
., 1991).
Studies on the complex life cycle of the genera
Aproctella
are scarce. Bain
et al
. (1981)
experimentally described the development of
A.
alessandroi
microfilariae using Diptera
Aedes
togoi
Theobald, 1907 as an intermediate host that
reached its infective stage on day 13. According to
studies by Pandey
et al
. (2015), Gomez-Puerta &
Mayor (2017), and Mondal
et al
. (2017), filarid
specimens of other genera are dynamic at the
infection sites, and it is likely that in birds, the
filariae can also reach the vital organs, such as the
liver, heart, lung, reproductive organs, and brain. In
the present study, we extended the distribution to
the Amazon region of
A. stoddardi
in the hosts
Dendrocincla fuliginosa
Vieillot, 1818,
Turdus
leucomelas
Vieillot, 1818, and
Tachyphonus rufus
Boddaert, 1783 at different infection sites with
images of the morphology under light microscopy.
It is necessary to expand the records of the presence
of filarid nematodes in birds in the region to
elucidate the ecological factors that influence this
infection.
Neotropical Helminthology, 2022, 16(2), jul-dic
Figure 1
. Specimens de
Aproctella stoddardi
.
A
: macroscopic view of the adult female specimen (arrow) in the capsule hepatic
(scale bar=0.5 cm).
B
: Anterior end of the male showing the nerve ring (n) and the final esophagus portion and beginning of the
intestine (e) (scale bar =100µm)
C:
Anterior end of the female showing the projection of the esophageal tooth in the oral aperture
(t) (scale bar =40µm).
D
: Anterior end of the female showing the nerve ring (n) and the final esophagus portion and beginning of
the intestine (e) (scale bar =100µm).
E
: anterior end portion of the female showing the vulvar aperture (v) (scale bar =100µm).
F:
Posterior end of female showing tail shape and anal aperture (a) (scale bar=100µm).
G
: Posterior end of male showing cloacal
aperture (c) and tail shape (scale bar =100µm).
H:
Final portion tail of the male showing the shape of the spicules (s) (scale bar
=20µm).
Rabelo
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
The authors would like to thank the Mangal das
Garças Zoobotanic Park and the Battalion of the
Environmental Police of the State of Pará-Brazil
for donating the studied specimens. This study is
part of the conclusion work of the undergraduate
course of A.M.P. Rabelo. This work was supported
by Coordenação de Aperfeiçoamento de Pessoal de
Nível Superior, Programa Nacional de Pós-
doutorado (CAPES-PNPD) for the postdoctoral
scholarship granted to the author D. F. Conga.
203
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Received August 31, 2022.
Accepted November 6, 2022.
Rabelo
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