ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2018, 12(2), jul-dic:161-178.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
HELMINTHS ASSEMBLAGE OF CHRYSOMUS RUFICAPILLUS (VIEILLOT, 1819)
(PASSERIFORMES: ICTERIDAE) IN SOUTHERN BRAZIL
ENSAMBLAJE DE HELMINTOS DE CHRYSOMUS RUFICAPILLUS (VIEILLOT, 1819)
(PASSERIFORMES: ICTERIDAE) DEL SUR DE BRASIL
¹ Laboratório de Parasitologia de Animais Silvestres (LAPASIL), Departamento de Microbiologia e Parasitologia, Instituto de
Biologia, Universidade Federal de Pelotas. Telefone: +55(53) 3275-7335 Caixa postal 354 CEP 96010-900, Pelotas, Rio
Grande do Sul, Brasil.
² Laboratório de Biologia de Parasitos de Organismos Aquáticos (LABIPOA), Instituto de Ciências Biológicas,
Universidade Federal do Rio Grande. Telefone: +55(53) 3233-6710 Caixa postal 474 CEP 96650-900, Rio Grande,
Rio Grande do Sul, Brasil.
*Corresponding author: E-mail: fabifedatto@gmail.com
Fabiana Fedatto Bernardon¹*; Tatiana Cheuiche Pesenti¹; Renato Zacarias Silva²;
Joaber Pereira Jr² & Gertrud Müller¹
ABSTRACT
Keywords: Acanthocephala – Cestoda – chestnut – Chrysomus ruficapillus – Nematoda – rice fields – Trematoda
Chrysomus ruficapillus (Vieillot, 1819) is an abundant bird of the Pampa Biome, often found associated
with Oryza spp. cultivation. One hundred twenty-two birds were collected in rice fields from southern
Brazil to examine the presence of helminths. One hundred fourteen C. ruficapillus were positive for at
least one parasitic species (P%=93.4). We identified 15 taxa: species of Trematoda (P%=75.4), two
Cestodes (P%=20.5), four Nematodes (P%=57.4) and one acanthocephalan (P%=2.4). Results and
parasitological indexes are new for C. ruficapillus contributing to parasitological knowledge of species
and for the helminthology of Icteridae in South America.
Neotropical Helminthology
161
Volume12,Number2(jul-dec2018)
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
RESUMEN
Palabras clave: turpial de gorro castaño – arrozales – parasitos - Acathocephala Cestoda - Nematoda - Trematoda
Chrysomus ruficapillus (Vieillot, 1819) es una ave abundante en Bioma Pampa frecuentemente asociada a
arrozales. Se examinaron 122 especímenes recolectados en campos de arroz del extremo sur de Brasil para
investigar la presencia de helmintos. Ciento y catorce C. ruficapillus fueron positivos para por lo menos
uma espécie parásita (P% = 93.4) y fueron identificados 15 taxa: ocho pertenecientes a Trematoda (P% =
75.4), dos a Cestoda (P% = 20.5), cuatro a Nematoda (P% = 57,4) y uno a Acanthocephala (P% = 2.4). Los
resultados y índices parasitológicos son inéditos para C. ruficapillus contribuyendo al conocimiento
parasitológico de la espécie y para la helmintología de Icteridae en América del Sur.
Parasites represent a significant part of biological
diversity. According Price (1980), parasitism is one
of most successful lifestyles exhibited by several
organisms. Estimates suggest that there are
between 75,000 and 300,000 species of helminths
parasitizing vertebrates (Dobson et al., 2008),
however, this diversity will only be known when
the hosts are studied (Windsor, 1998).
The southern region of Rio Grande do Sul is
located in the Pampa Biome, which covers part of
Argentina, all of Uruguay and most of the territory
of Rio Grande do Sul (62.2%) (Boldrini et al.,
2010). This biome presents high animal and
vegetal diversity, being the richness of birds in Rio
Grande do Sul composed by 480 species (Develey
et al., 2008).
Chrysomus ruficapillus (Vieillot, 1819)
(Passeriformes: Icteridae) internationally as
known as chestnut-capped blackbird comprises a
characteristic bird of the Pampa Biome. It is
geographically restricted to the South American
continent, occurs in French Guiana, Brazil,
Bolivia, Paraguay, Argentina and Uruguay (IUCN,
2017). In Brazil, C. ruficapillus is distributed
throughout the eastern territory, often found
associated with Oryza spp. (rice fields) and it is
appropriately established at these sites (Belton,
1994; Fallavena, 1988; Dias & Burger, 2005;
Crozariol, 2008).
This species is swampy, has a gregarious habit and
can be found in flocks ranging from a few to
thousands (Belton, 1994). In the state of Rio
Grande do sul it is considered one of the most
abundant bird (Fallavena, 1988; Belton, 1994;
Silva, 2004), however, helminthological
information about C. ruficapillus does not exist, in
this sense, the study identified and quantified the
helminth assemblage associated to C. ruficapillus
in rice fields in southern Brazil.
Collect of host's
One hundred twenty-two hosts were collect in
period of 2013 at 2014 in rice fields of the
propriety “Granjas Quatro Irmãos S. A.” in the city
of Rio Grande, Rio Grande do Sul, Brazil (a.c. 32º
14'37.24” S; 52°29'38.71” W) through the trap (one
cube with sized 2.5 m³ with metal edges, covered
with screen and top opening, which allows the
entry of the birds, but not the exit) was installed
containing potable water and bird food ad libitum.
The identification of birds was performed
according to Belton (1994). The capture,
euthanasia, and transport of birds have been
licensed by “Instituto Chico Mendes de
Conservação da Biodiversidade” (ICMBio/41095-
3) and approved by “Comissão de Ética e
E x p e r i m e n t a ç ã o A n i m a l – U F P e l ”
(CEEA/UFPel/nº1477). After euthanasia, the hosts
(number 1 at 122) were packed individually in
plastic bags and transported to Instituto de
Biologia, Departamento de Microbiologia e
Parasitologia at “Laboratório de Parasitologia de
Animais Silvestres” (LAPASIL/UFPel), and
frozen until processing.
Collecting, preparing and identification of
helminths
For helminths collection, the birds were
necropsied. Were examined the eyes, mouth,
esophagus, proventriculus, gizzard, small and large
intestine, cecum, trachea, lungs, heart, liver,
gallbladder, kidneys, reproductive system, cloaca
and air sacs. These organs or systems were opened,
washed with current water under sieve 150µm. The
washing resulting well as the cavities and mucous
m e m b r a n e s w e r e e x a m i n e d t u n d e r
®
stereomicroscope (Olympus SZ61). The
helminths were fixed and prepared for the
identification respecting the taxa, according
protocols of Amato & Amato (2010).
The identification was realized according to Faria
(1912), Freitas (1951), Kohn & Fernandes (1972),
Gibson et al. (2002), Jones et al. (2005), Bray et al.
(2008) and Lunaschi et al. (2015) for Trematoda
(Digenea); Saxena & Baugh (1978) and Khalil et
al. (1994) for Cestoda; Vicente et al. (1983) and
Anderson et al. (2009) for Nematoda and Schimidt
& Kuntz (1977) for Acanthocephala. Vouchers
were deposited in “Coleção Helmintológica do
Instituto Oswaldo Cruz – CHIOC” (number
38586,a-b; 39084 at 39095 a-b) from Rio de
Janeiro and “Coleção de Helmintos do Laboratório
162
Neotropical Helminthology, 2018, 12(2), jul-dic
INTRODUCTION
MATERIAL AND METHODS
Fedatto Bernardon et al.
163
de Parasitologia de Animais Silvestres -
CHALAPASIL” (number 644 at 679) in
Departamento de Microbiologia e Parasitologia,
Instituto de Biologia, Universidade Federal de
Pelotas.
Parasitological analysis
The term assemblage was used in this research
according to the concept to Fauth et al. (1996),
because it represents the universe of species
(taxonomic limits) and limits of distribution
(geographic) according to the aim of the study. For
the “assembly” of helminths was estimated:
prevalence (P%), mean abundance of infection
(MA), and mean intensity of infection (MII)
according to Bush et al. (1997), and range of
infection (R) according to Bush et al. (2001).
From the 122 C. ruficapillus examined, one
hundred and fourteen were positive (P%=93.4) for
at least one taxon parasite. Trematoda with
P%=75.4 (n=92), Cestoda with P%= 20.5 (n=25),
Nematoda with P%=57.4 (n=70), and
Acanthocephala with P=2.4% (n=3). The helminth
assemblage was composed by 15 taxa, Trematoda
(Digenea): Tanaisia valida Freitas, 1951
(Eucotylidae: Tanaisiinae) (n=328) (Fig.1-a),
Prosthogonimus ovatus (Rudolphi, 1803)
(Prosthogonimidae) (n=25) (Fig.1-b), Conspicuum
c o n s pi c u u m (G o mes de Fa ri a, 1 912)
(Dicrocoellidae: Leipertrematinae) (n=32) (Fig. 1-
c), Stomylotrema gratiosus Travassos, 1922
(Stomylotrematidae) (n=13) (Fig.1-d),
Eumegacetes sp. (Eumegacetidae) (n=3)
(Figura1-g), Strigea sp. (Strigeidae) (n=2) (Fig.1-
h) e dois Echinostoma spp. (Echinostomatidae)
(n=4/1) (Fig. 1 e/f); Cestoda: Mathevotaenia sp.
(Anoplocephalidae) (n=45) (Fig.2a-d); and
Anonchotaenia sp. (Paruterinidae) (n=1) (Fig. 2 e-
h); Nematoda: Diplotriaena bargusinica Skrjabin,
1917 (Diplotriaenidae) (580 males and 652
females) (n=1,232) (Fig.3a-f), Oxyspirura Drashe
in Stossich, 1897 (Thelaziidae) (two females and
one male) (n=3), one species of Aproctoidea (three
females) and one species of Capillariinae (one
female) (Fig.4a-h) and Acanthochephala:
Mediorhynchus micranthus (Rudolphi, 1819)
(Gigantorhynchidae) (8 males and 11 females)
(n=19) (Fig.5 a-b). Pathological aspects of
infections were not analyzed.
Helminths assemblage of C. ruficapillus, infection
site and parasitological indexes (P%, MA, MII e R)
are presented in Table 1. According to P%, T.
valida, D. bargusinica and Mathevotaenia sp.
were the taxa the showed highlighted values. T.
valida the taxon with highlight in the P% and D.
bargusinica the species with highlight in MA, MII
and R (Table 1).
Helminths of C. ruficapillus were not recorded
until the present study, although there are
occurrences of parasites for other Icteridae in
Brazil. Species of Tanaisia (Digenea) parasite
renal tubules and kidneys of birds (Gibson et al.,
2002). Tanaisia valida was described by Freitas,
1951 parasitizing kidneys of Himantopus
melanurus Vieillot, 1817 (Charadriiformes:
Recurvirostridae) in the state of Rio de Janeiro,
Brazil. It resembles Tanaisia fedtschenkoi
Skrjabin, 1924, differentiating them by the size
(length and width) of the eggs, which are slightly
larger than those of T. valida, in addition to the
geographical distribution, as T. fedtschenkoi occurs
in Asia and Europe, reported in Charadriiformes
(Scolopacidae, Recurvirostridae, Charadriidae,
Laridae) (Freitas, 1951).
The specimens of T. valida found in C. ruficapillus
presented small variations in the morphology of the
testis lobes, possibly related to the maturation of
the trematodes, also verified by Freitas (1951). It
was possible to observe the insertions of the spines
in the integument in most of the digenetics,
whereas spines were visualized only in parasites of
two hosts. These birds did not undergo the freezing
process after euthanasia, a fact that may explain the
conservation of the spines, corroborating Monteiro
et al. (2007) and Mascarenhas et al. (2016) that
attributed the absence of spines in Trematoda
(Digenea) due to the freezing or the state of
conservation of the hosts (P. ovatus of aquatic birds
and Telorchis spp. Of freshwater turtles,
RESULTS
DISCUSSION
Helminths assemblage of Chrysomus rucapillus
Neotropical Helminthology, 2018, 12(2), jul-dic
Table 1. Assemblage of helminths of Chrysomus ruficapillus (Vieillot, 1819) (Passeriformes: Icteridae) from
southern Brazil. Infection sites (IS), number of infected birds (NIB) and parasitological indexes: prevalence (P%),
mean abundance of infection (MA), mean intensity of infection (MII) and range of infection (R).
Helminths
IS
P% (NIB)
MA
MII
R
Trematoda (Digenea)
Tanaisia valida
kidney ducts
58.2 (71)
2.7
4.62
1-12
Prosthogonimus ovatus
cloaca
14.75 (18)
0.2
1.38
1-5
Conspicuum conspicuum
small bladder
8.20 (10)
0.26
3.2
1-7
Stomylotrema
gratiosus
cloaca
7.37 (9)
0.1
1.4
1-3
Echinostoma
morphotype 1
small intestine
2.45 (3)
0.024
1
1
Echinostoma
morphotype 2
small intestine
0.82 (1)
0.0082
1
1
Eumegacetes sp.
cloaca
0.82 (1)
0.02
3
3
Strigea
sp.
small intestine
1.64 (2)
0.01
1
1
Cestoda
Mathevotaenia
sp.
small intestine
19.67 (24)
0.36
1.87
1-5
Anonchotaenia
sp.
small intestine
0.82 (1)
0.008
1 1
Nematoda
Diplotriaena bargusinica
air sacs
53.30 (65)
10.9
19.1
1-106
Oxyspirura
sp.
washing of external
surface of the body
1.64 (2)
0.016
1
1
Aproctoidea
cavity washing
1.64 (2)
0.024
1.5
1-2
abdominal
Capillariinae
cavity washing
0.82 (1)
0.008
1
1
abdominal
Acanthocephala
Mediorhynchus micracanthus small intestine 2.46 (3) 0.15 6.33 1-9
Total number of infected birds 114
respectively). In this way, it is evident that the
freezing, state of conservation of the hosts as well
as the preparation of the specimens influences the
quality of the digenetics for taxonomic
identification.
In Brazil for Icteridae were registered Tanaisia
inopina Freitas, 1951 in Icterus chrysocephalus
(Linnaeus, 1766), T. oviaspera in Icterus
pyrrhopterus (Vieillot, 1819) (Freitas, 1951) and T.
valida in Molothrus bonariensis (Gmelin, 1789)
(Passeriformes: Icteridae) (n=5) (P%=40, MA=4.0
and MII=10) in the state of Rio Grande do Sul
(Bernardon et al., 2016). The values of the T. valida
indexes in C. ruficapillus (Table 1) were higher
than those presented by Bernardon et al. (2016).
The life cycle of T. valida is unknown, however,
according to Lunaschi et al. (2015) the biology of
Tanaisiinae involves the ingestion of molluscs
containing metacercariae (intermediate hosts).
Pathological aspects caused by T. valida are not
known, however, researches with wild birds and
mainly with breeding birds parasitized by T. bragai
were realized in state of Rio de Janeiro, Brazil
(Menezes et al., 2001; Pinto et al., 2004; Gomes et
Neotropical Helminthology, 2018, 12(2), jul-dic Fedatto Bernardon et al.
164
165
Figure 1. Trematoda (Digenea) of Chrysomus ruficapillus (Vieillot, 1819) (Passeriformes: Icteridae) from southern Brazil. a.
Tanaisia valida Freitas, 1951 (Eucotylidae) BAR=410µm; b. Prosthogonimus ovatus (Rudolphi, 1803) (Lühe, 1899)
(Prosthogonimidae) BAR=580µm; c. Conspicuum conspicuum (Gomes de Faria, 1912) (Dicrocoellidae) BAR=460µm; d.
Stomylotrema gratiosus Travassos, 1922 (Stomylotrematidae) BAR=430µm; e. Echinostoma morphotype 1 BAR=600µm; f.
Echinostoma morphotype 2 BAR= 560µm (Echinostomatidae) g. Eumegacetes Looss, 1900 (Eumegacetidae) BAR=320µm; h.
Strigeidae BAR=175µm. OS=oral sucker; P= pharynx; C=cecum; VS=ventral sucker; O=ovary; T=testes; CS=cirrus sac; U-
EG=uterus with eggs.
Helminths assemblage of Chrysomus rucapillus
Neotropical Helminthology, 2018, 12(2), jul-dic
166
Figure 2. Cestoda of Chrysomus ruficapillus (Vieillot, 1819) (Passeriformes: Icteridae) from
southern Brazil. a-d. Mathevotaenia sp. (Anoplocephalidae); a. scolex BAR=190µm; b. mature
proglottides BAR=625µm; c. gravid proglottides BAR=750µm; d. gravid proglottides with cirrus
sac and cirrus BAR=150µm; e-h. Anonchotaenia sp. (Paruterinidae); e. scolex BAR=250µm; f.
mature proglottides BAR=92µm; g. mature proglottides in highlight BAR=340µm; h. gravid
proglottides and paruterine organ with eggs BAR=42µm. S=suckers; IP= immature proglottides;
CB=cirrus bag; O=ovary; C=cirrus; T=testes; PO= paruterine organ; LCE=longitudinal excretory
canal.
Neotropical Helminthology, 2018, 12(2), jul-dic Fedatto Bernardon et al.
167
Figure 3. Diplotriaena bargusinica Skrjabin, 1917 (Nematoda: Diplotriaenidae) of Chrysomus ruficapillus
(Vieillot, 1819) (Passeriformes: Icteridae) from southern Brazil. a. Body cavity of the bird, arrow head
indicates the nematodes in air sacs BAR=1000µm; b. Nematodes inside air sacs BAR= 1000µm; c. Anterior
extremity of nematode, arrow head indicates the smooth trident with tapered apex BAR= 30µm; d. arrow head
indicates the genital pore of female BAR=100µm; e. Posterior region of female rounded BAR=400µm; f.
Posterior region of male, right and left spicules arrow head pointing the papillae BAR=350µm. LI=lips;
E=esophagus AS=air sacs; N=nematode; TR=trident; PRF=posterior region of female; LS=left spicule;
RIS=right spicule.
Helminths assemblage of Chrysomus rucapillus
Neotropical Helminthology, 2018, 12(2), jul-dic
168
Figure 4. Nematode of Chrysomus ruficapillus (Vieillot, 1819) (Passeriformes: Icteridae) from southern Brazil.
a-e. Oxyspirura sp. (Thelaziidae); a. anterior region, arrow head indicates the papillae BAR=62µm; b. medium
region of female BAR =45µm; c. posterior region of female BAR =77µm; d. posterior region of male BAR
=157µm; e. spicules of male, arrow head indicates the papillae BAR=157µm; f. Capilariinae eggs BAR=65µm;
g. anterior region BAR =6µm; g-h. Aproctoidea g. anterior region BAR =6µm h. posterior region of female BAR
=6µm. OC=oral capsule; E= esophagus; S= spicules; RIS= right spicule; LS=left spicule. EG= eggs.
Neotropical Helminthology, 2018, 12(2), jul-dic Fedatto Bernardon et al.
169
Figure 5. Mediorhynchus micracanthus (Rudolphi, 1819) (Acanthocephala: Gigantorhynchidae) of Chrysomus ruficapillus
(Vieillot, 1819) (Passeriformes: Icteridae) from southern Brazil. a. female BAR=600µm. b. male BAR=950µm. PRO=proboscis;
LE= lemniscus; EG=eggs; T=testes; CG=cement gland; CB=copulatory bursa.
al., 2005; Silva et al., 2005; Costa et al., 2015).
Although T. bragai is considered to be poorly
pathogenic to birds, it can cause clinical
complications such as apathy, weight loss, diarrhea
and death in high parasite loads (Costa et al., 2015).
Microscopic lesions such as dilatation of the
collecting ducts, nephritis, fibrosis, destruction,
and calcification points have been reported
(Menezes et al., 2001; Pinto et al., 2004).
Prosthogonimus spp. are found in the oviduct,
Fabricius bursa, cloaca and accidentally in the
intestine and eggs (Olsen, 1974), distribution is
cosmopolitan (Bray et al., 2008). Prosthogonimus
ovatus has a low parasitic specificity, recorded in
Brazil for the first time in Gallus gallus (Linnaeus,
1758) (Galliformes: Phasianidae) (n=17)
(P%=17.6), however, the authors did not cite origin
and MII (Travassos, 1928; Travassos et al., 1969).
According to Kohn & Fernandes (1972), after
examining 84 P. ovatus specimens 22 hosts of 10
orders, verified that the digenetic presents
significant intraspecific morphological variations
(=phenotypic plasticity), and these variations may
be greater in the specimens of the same host than
Helminths assemblage of Chrysomus rucapillus
Neotropical Helminthology, 2018, 12(2), jul-dic
170
when observed in parasites of zoologically far
away hosts (Kohn & Fernandes, 1972; Monteiro et
al., 2007). According to Boddeke (1960a) apud
Monteiro et al. (2007) differences in morphology
may be linked to different sites of infection and low
specificity. However, P. ovatus of C. ruficapillus
did not present relevant morphological differences
between the specimens and all specimens were
found in the cloaca of the hosts.
Boddeke (1960b) elucidated the biological cycle of
P. ovatus in Europe (Holland) presented a
participation of Bithynia tentaculata (Linnaeus,
1758) (Mollusca: Gastropoda) as primary host and
adults or young adults of Odonata Cordulia aenea
(Linnaeus, 1758) (Corduliidae), Orthetrum
cancellatus Linnaeus, 1758 (Libellulidae),
Leucorrhinia caudalis (Charpentier, 1840)
(Libellulidae) and Aeshna cyanea (Muller, 1764)
(Aeshnidae) as secondary host of trematode. The
author comments that the primary intermediate
host and larval stages of the parasite were not
identified for the Americas. It is evident the lack of
work in relation to the biology of P. ovatus in
Brazil. The effects of Prosthogonimus parasitism
on egg-laying birds, affecting egg production,
causing decline or non-formation (economic losses
in domestic poultry) (Olsen, 1974).
Prosthogonimus ovatus was recorded in Icteridae
in Sturnella superciliaris (Bonaparte, 1850) in the
state of Minas Gerais (Kohn & Fernandes, 1972)
without indexes, and in M. bonariensis (n=5) in the
state of Rio Grande do Sul (P%=20; MA=1;
MII=5) (Bernardon et al., 2016). The P% value of
P. ovatus in M. bonariensis was higher than in C.
ruficapillus (Table 1), however, it is necessary to
consider that the sample number of hosts in the
present study was high to that presented by
Bernardon et al. (2016).
Conspicuum spp. (Leipertrematinae) parasite the
gallbladder of birds, rarely mammals. Its
distribution comprises Europe, Asia, Africa, North
America, Central America and South America
(Bray et al., 2008). Conspicuum conspicuum was
described as Dicrocoelium conspicuum by Faria
(1912), from three specimens collected from
Mimus gilvus (Passeriformes: Mimidae) (n = 1) in
the state of Rio de Janeiro, Brazil. For Icteridae, C.
conspicuum was recorded in Cacicus haemorrhous
(Linnaeus, 1766) no recorded origin, number of
birds sampled and parasitological indexes
(Travassos et al., 1969; Fernandes et al., 2015).
Biology of C. conspicuum is not known, Patten
(1952) elucidated the cycle of Conspicuum
icteridorum Denton & Byrd, 1951 and identified
Zonitoides arboreus (Say, 1816) (Gastropoda:
Mollusca) as the primary intermediate host and
Armandillidium quadrifrons Stoller, 1902
(Isopoda: Armadillidiidae) as secondary. Menezes
et al. (2001), identified C. conspicuum in Numida
meleagris Linnaeus, 1764 (Galliformes:
Numididae) (n=36) (P%=2.8; MII=1), in the state
of Rio de Janeiro, birds were raised in the air free
and had no clinical signs. However, macroscopic
and microscopic lesions were observed: enlarged
liver lobes (hepatomegaly) and yellowish
(jaundice), and hepatic degenerative process
(hepatolysis). These is the first record of C.
conspicuum in C. ruficapillus in Brazil.
Species of Stomylotrema Looss, 1900 are found in
the posterior alimentary tract, especially in the
cecum, rectum, Fabricius Bursa or cloaca of birds,
with cosmopolitan distribution (Bray et al., 2008).
Brenes et al. (1966) elaborated the identification
key for Stomylotrema spp. from Costa Rica. In this
study the authors described Stomylotrema
ucremium from two specimens collected from
Icterus galbula Linnaeus, 1758 (Passeriformes:
Icteridae), differentiated from S. gratiosus due
differences in genital pore position, shape and
extent of vitellaria fields, and egg size. According
to Pinto et al. (2015) these differences may be the
result of intraspecific variation or preparation of
specimens, suggesting that S. ucremium is S.
gratiosus synonym. That the low number of
specimens and possibly the preparation of the
specimens compromised the description of Brenes
et al. (1966).
About life cycle of S. gratiosus, Pinto et al. (2015)
identified Pomacea maculata Perry, 1810
(Gastropoda) naturally infected in the state of
Maranhão, Brazil. Studies on the pathology caused
by S. gratiosus don't exist, although Stomylotrema
spp. have been recorded in several species of birds
in Brazil (Travassos et al., 1969). This is the first
report in Icteridae showing the parasitological
indexes (Tab. 1).
Species of Echinostomatidae Looss, 1899 are
Neotropical Helminthology, 2018, 12(2), jul-dic Fedatto Bernardon et al.
171
hematophagous, parasitize birds, mammals, fish
and reptiles and have cosmopolitan distribution
(Lutz, 1924; Jones et al., 2005). The taxonomy is
complex, characterized by the presence of an
uninterrupted cephalic collar armed with one or
two crowns of thorns. The family belongs to 10
subfamilies, among them, Echinostomatinae
Looss, 1899 with 19 genera including Echinostoma
Rudolphi, 1809 (Jones et al., 2005). About the
biological cycle of Echinostoma, in Brazil, Lutz
(1924) observed molluscs, tadpoles and fish as
intermediate hosts. According to Esteban &
Muñoz-Antoli (2009) apud Pinto & Melo (2012)
biology involves three hosts (Gastropoda and
Mollusca). Pinto & Melo (2012) identified Physa
marmorata Guilding, 1828 (Mollusca: Physidae)
as a natural intermediate host of E. exile Lutz, 1924
in the state of Minas Gerais. It is known that E.
revolutum causes slimming and catarrhal enteritis,
which may lead to the death of young Anseriformes
(Yousuf et al., 2009 apud Saijuntha et al., 2013).
In Brazil, Echinostoma spp. were recorded for
several birds, including Icteridae: E. discinctum
Dietz, 1909 in Procacicus solitarius (Vieillot,
1816) and E. revolutum in M. bonariensis
(Travassos et al., 1969; Fernandes et al., 2015).
Parasitism in humans has been reported especially
in South Asia, since some species of
Echinostomatidae have zoonotic potential (Sohn et
al., 2011a, 2011b; Chai et al., 2012). This is the first
record of Echinostoma spp. for C. ruficapillus
including parasitological indexes. In C.
ruficapillus there was a low P% (Table 1), however,
two morphologically distinct species were
identified (Fig. 1 e-f). It is important to emphasize
that due to the current complexity and taxonomy, a
revision of Echinostomatidae from Brazil is
necessary, besides studies involving the biological
cycle and pathology of the species.
Eumegacetes spp. (Eumegacetidae) has a
cosmopolitan distribution and they are parasites of
the intestinal tract, especially the rectum, cloaca
and renal system of birds (Bray et al., 2008).
Although species are widely distributed, there are
few records of Eumegacetes spp. in Brazil,
constituted by a single species E. medioximus
Braun, 1901. In the state of Rio de Janeiro, Brasil &
Amato (1992) reported E. medioximus on two P.
domesticus (Passeriformes: Passeridae) (n=142)
(P%=0.13 and MII=0.013) and in state of Rio
Grande do Sul, Callegaro-Marques & Amato
(2010) identified Eumegacetes sp. (n=1) in P.
domesticus (n=160) (P%=0.6 MA=0.01, MII=1
and R=1). The low values of parasitological
indexes in C. ruficapillus (Table 1) corroborate the
previously mentioned authors. And for the first
time, Eumegacetes sp. was recorded for Icteridae in
Brazil.
The biological cycle of Eumegacetes Looss, 1900
involves dragonflies (Odonata) (Bray et al., 2008).
In Brazil, Pinto & Melo (2012) identified and
characterized morphologically metacercariae of E.
medioximus in Orthemis discolor (Burmeister,
1839) and Perithemis mooma Kirby, 1889
(Odonata: Libellulidae) in the state of Minas
Gerais. However, the primary intermediate host of
E. medioximus remains unknown as well as
information about the pathology in the definitive
host´s.
Strigeidae Railliet, 1919 are parasites of birds
characterized by the anterior cup-shaped region
and the presence of holdfast, composed of
Duboisiellinae Baer, 1938 and Strigeinae Railliet,
1919. Strigeinae Railliet, 1919 houses 12 genera
among them, Strigea Abildgaard, 1790, which has
vitellarias distributed evenly throughout the body
and presence of pharynx (Gigson et al., 2002). In
Brazil, according to Travassos et al. (1969) Strigea
spp. were recorded in several birds, for Icteridae
Strigea sphaerocephala (Westrumb, 1823) in
Psarocolius decumanus (Pallas, 1769). For the first
time, Strigea sp. is recorded in C. ruficapillus as
well as parasitological indexes (Table 1).
Paruterinidae Fuhrmann, 1907 are cestodes that
present the paruterine organ (= structure in which
the eggs are surrounded by layers of membranes)
that gives name to the family (Georgiev &
Kornyushin, 1994). Paruterinidae is composed by
21 genera, including Anonchotaenia Cohn, 1900
with cosmopolitan distribution (PHILLIPS et al.,
2014). According to Phillips et al. (2012) when
reviewing the family in South America, eight
species of Anonchotaenia Cohn, 1900 were
recorded for Passeriformes and Apodiformes. In
Icteridae, A. brasiliensis Fuhrmann, 1908 was
reported in Cacicus haemorrhous (Linnaeus, 1766)
(Passeriformes: Icteridae) in Brazil. The
intermediate hosts of Paruterinidae are unknown as
well as the pathological aspects; however, Phillips
Helminths assemblage of Chrysomus rucapillus
Neotropical Helminthology, 2018, 12(2), jul-dic
172
et al. (2014) suggest the involvement of terrestrial
insects in the cycle.
Mathevotaenia Akhunyan, 1946 belongs to the
Anoplocephalidae: Anoplocephalinae. It includes
28 parasitic species of mammals (rodents,
marsupials, primates, mustelids, edentados,
lemurs) and birds (Yamaguti, 1959; Schmidt,
1986). According to Spasskii (1951) apud
Lunaschi et al. (2012) the life cycle of
Mathevotaenia spp. involves Blattaria and
Lepidoptera as intermediate hosts. Pathological
aspects not known for definitive hosts. Saxena &
Baugh (1978) report that the occurrence of
Mathevotaenia spp. is rarer in birds than in
mammals. This authors hey described
Mathevotaenia ornithis Saxena & Baugh (1978)
(P%=100, MII =2) parasitizing P. domesticus (n=1)
in India (Saxena & Baugh, 1978). In Brazil,
Mathevotaenia is first recorded for Icteridae,
presenting the parasitological indexes (Table 1).
Diplotriaenoidea Anderson, 1958 (Nematoda) are
respiratory tract parasites of reptiles and birds
(Anderson, 2000). Diplotriaenidae (Anderson,
1962) includes 27 valid species with cosmopolitan
distribution (Atkinson et al., 2009). Diplotriaena
Railliet & Henry, 1909 is a nematode from the air
bags of brids, reflecting its specificity for this host
group, moreover this parasite group shows wide
geograpgic distribution (Vicente et al., 1983;
Atkinson et al., 2009).
Diplotriaena bargusinica was registered in
different regions in Brazil in a several
Passeriformes (Vicente et al., 1983; Pinto et
al.,1997; Carvalho et al., 2007). For Icteridae in: C.
cela (Linnaeus, 1758), C. haemorrhous (Linnaeus,
1766), Gnorimopsar chopi (Vieillot, 1819), Icterus
croconotus (Wagler, 1829), Icterus sp. Brisson,
1760, Psarocolius decumanus maculosus
(Chapman, 1920), Molothrus bonariensis
(Gmelin, 1789) in the states of Mato Grosso do Sul,
São Paulo and Pará (Vicente et al., 1983). In P.
bifasciatus (Spix, 1824) (n=3) from Manaus, state
of Amazonas, without presenting indexes
(Gonçalves et al., 2002). In M. bonariensis (n=5)
(P%=60; MA=7.4; MII=12.3; A=1-18) in the state
of Rio Grande do Sul (Bernardon et al., 2016). The
value of P% in C. ruficapillus was lower than that
reported by Bernardon et al. (2016), although the
sample number is higher in the present study
(n=122), with emphasis on the R value (Table 1).
The biological cycle of D. bargusinica was detailed
by Anderson in 1962 through experimental
infection with wild birds (Turdidae and Icteridae).
It is heteroxenous, involving grasshoppers
(Orthoptera) as intermediate hosts (Anderson,
1962, 2000). The common clinical signs in
parasitized birds are: lethargy, difficult respiration
due to the presence of nematodes in the respiratory
tract that causes inflammatory reaction with airway
congestion in high infections (Atkinson et al.,
2009).
According to Anderson (2000) Aproctoidea, 1945
Skrjabin & Shikhobalova includes nematodes of
bird found in air sacs, nasal cavity, nictitating
membranes, subcutaneous tissue of the head and
neck. To the superfamily belong Aproctidae
Skrjabin & Shikhobalova, 1945 that occur in
terrestrial birds and Desmidocercidae Cram, 1927
in piscivorous birds. Knowledge about the
transmission of these nematodes is scarce, for
Aprocta Linstow, 1883 eggs containing the first-
stage larvae are known to be eliminated by birds
and ingested by arthropods (intermediate hosts)
(Anderson, 2009). According to Anderson (2009),
for morphological identification male specimens
are required, however, in C. ruficapillus only
females were found, making it impossible to
identify at lower taxonomic level. For the first time,
it is recorded Aproctoidea in Icteridae in Brazil.
Thelaziidae Skrjabin, 1915 (Nematoda) composed
by Thelaziinae Skrjabin, 1915 and Oxyspirurinae
Skrjabin, 1916 has cosmopolitan distribution.
Oxyspirura Drasche in Stossich, 1897 belongs to
Oxyspirurinae, a parasite found under the
nictitating membranes of eyes of domestic and
wild and occasionally in mammalian (Anderson et
al., 2009). Eighty-four species have been reported
in birds for at least 43 host's families (Anderson,
2000). In Brazil were registered O. spp. for a
several birds, for Icteridae: O. cassici Rodrigues,
1963 in C. haemorrhous (Linnaeus, 1766); O.
cephaloptera (Molin, 1860) Stossich, 1897 in I.
croconotus (Wagler, 1825); O. matogrossensis
Rodrigues, 1963 in: P. decumanus (Pallas, 1769), I.
croconotus and G. chopi chopi (Vieillot, 1819).
Oxyspirura sp. in P. decumanus (Vicente et al.,
1995). According to Table 1, Oxyspirura and
Aproctoidea occurred only in two C. ruficapillus.
Neotropical Helminthology, 2018, 12(2), jul-dic Fedatto Bernardon et al.
173
In the biological cycle of O. mansoni (Cobbold,
1879) the adult nematodes located in the
membrane of the eyes deposit the eggs, which
together with lacrimal secretions follow the tear
ducts to the mouth where they are swallowed and
eliminated by the feces. These eggs are ingested by
roaches such as Pycnoselus surinamensis
(Linnaeus, 1758) (Blattodea) that act as
intermediate hosts (Anderson, 2000). In definitive
hosts clinical sings of this parasitosis depend on
parasite load, being common, eye irritation,
conjunctivitis and loss of vision. As a consequence,
there is the compromise of foraging, loss of
appetite and decrease in weight and death (Dunham
et al., 2016).
According to Anderson (2000) the classification of
the Capillarinae is one of the most difficult in the
Nematoda. Were identified approximately 300
species of Capillaria (Zeder, 1800) parasitizing a
wide range of fish and mammals. The life cycle of
Capillarinae can be monoxenous or heteroxenous,
eggs are released to the environment through feces,
urine or predation, depending on the location of the
parasite in the host (Anderson, 2000). In relation to
pathology, they cause weight loss and diarrhea
(Weher, 1939). This study records for the first time
in Brazil Capillariinae in Icteridae, parasitizing C.
ruficapillus.
Giganthorhynchidea Southwell & Mache, 1925
(Acanthocephala) are bird parasites composed of
five families, among them Giganthorhynchidae
Hamann, 1892 with five genera: Gigantorhynchus
Hamann, 1892, Empodisma Travassos, 1916,
Heteracanthorhynchus Lundström, 1942 and
Mediorhynchus Van Cleave, 1916 (Yamaguti,
1963).
In South America, Petrochenko (1971) reported M.
vaginatus (Diesing, 1851) in Dolichonyx
oryzivorus (Linnaeus, 1758) and M. emberizae
(Rudolphi, 1819) in C. haemorrhous (Linnaeus,
1766), M. bonarienses and P. decumanus (Pallas,
1769) in Icteridae. In Brazil, Machado Filho (1941)
recorded M. micracanthus (Rudolphi, 1819) in
Pro ca ci cu s s ol it ar iu s (Vieillot, 1816)
(Passeriformes: Icteridae) in the state of Mato
Grosso. The biological cycle of Mediorhynchus
involves Blattodea, Orthoptera and Coleoptera as
intermediate hosts (Nickol, 1977). Pathological
aspects were addressed by Nickol (1977),
commenting that the deep penetration of the
proboscis produces nodules (granulomas) in the
intestine of the host. For the first time M.
micracanthus is reported in C. ruficapillus with
parasitological indexes.
According to the literature, the complex life cycles
of the parasites provide information on trophic
ecology, food webs, food preferences and host
foraging mode (Marcogliese & Cone, 1997;
Overstreet, 1997; Marcogliese, 2003). Thus,
suggesting the diet of C. ruficapillus composed of
arthropods (larvae and adults) (Coleoptera,
Hemiptera, Odonata, Collembola and Diptera)
(Fallavena, 1988, Belton, 2004, Silva, 2004) is
relating to the observed infections. It was
evidenced of parasite infections with heteroxenous
life cycles: Trematoda (P% = 75.4), Nematoda (P%
= 57.4) and Cestoda (P% = 20.5), C. ruficapillus is
the definitive host of T. valida, D. bargusinica and
Mathevotaenia sp..
In Brazil, were realized other studies with
helminths with Icteridae (Freitas, 1951; Travassos
et al., 1969; Kohn & Fernandes, 1972; Vicente et
al., 1995; Bernardon et al., 2016), however, the
small sample size, the absence of host numbers and
information on the locality of the birds in the
publications, made it difficult to compare the
populations of Icteridae helminths. Nevertheless, it
was possible to observe similarity in the
composition of helmintofauna between M.
bonariensis (Bernardon et al., 2016) and C.
ruficapillus, since both icterids share the
environment and food items. It can be noticed, after
the research with C. ru ficapillu s and
bibliographical review, that efforts beyond the
taxonomy of parasites are necessary, mainly in
relation to the biology and pathology of helminth
species.
The t a x a S . g r a t i o s u s , E u m e g a c e t e s ,
Mathevotaenia, Aproctoidea and Capillariinae
were reported for the first time for Icteridae in
Brazil. Tanaisia valida, Conspicuum conspicuum,
Prosthogonimus ovatus, Stomylotrema gratiosus,
Eumegacetes sp., Strigea sp., two species of
Echinostoma (Trematoda); Mathevotaenia sp. and
Anonchotaenia sp. (Cestoda); Diplotriaena
bargusinica, Oxyspirura sp., one species of
Aproctoidea and to Capillariinae (Nematoda), and
Mediorhynchus micranthus (Acanthocephala) are
Helminths assemblage of Chrysomus rucapillus
Neotropical Helminthology, 2018, 12(2), jul-dic
174
unprecedent for Chrysomus ruficapillus in South
America.
We thank the “Instituto Chico Mendes de
Conservação da Biodiversidade” (ICMBio) for
authorizing the collection of hosts and especially to
“Granjas 4 Irmãos S.A.” for their assistance
throughout the project. To “Coordenação de
Aperfeiçoamento do Pessoal de Nível Superior”
(CAPES) for scholarship support of the doctoral
studies of the first author and for the financial
support provided through edict 2010/032/CAPES.
ACKNOWLEDGMENTS
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