ISSN Versión impresa 2218-6425
ISSN Versión Electrónica 1995-1043
Neotropical Helminthology
357
Neotropical Helminthology, 2017, 11(2), jul-dic: 357-375
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
HELMINTH ASSEMBLAGE OF AQUATIC BIRDS (PELECANIFORMES: ARDEIDAE) OF
SOUTHERN RIO GRANDE AND A CHECKLIST OF HELMINTHS OF HERONS OF BRAZIL
ENSAMBLAJE DE HELMINTOS DE AVES ACUÁTICAS (PELECANIFORMES: ARDEIDAE) DEL
SUR DE RIO GRANDE DEL SUR Y UN LISTADO DE HELMINTOS DE GARZAS DE BRASIL
Fabiana Fedatto Bernardon¹,*; Ana Luisa Schifino Valente¹ & Gertrud Müller¹
¹Programa de Pós-graduação em Parasitologia, Departamento de Microbiologia e Parasitologia, Instituto de Biologia,
Universidade Federal de Pelotas. Endereço: Campus Universitário, caixa postal 354 CEP 96010-900, Pelotas, Rio Grande do
Sul, Brazil. Telefone: 55(53) 3275-7635.
*Correspondente author: *fabifedatto@gmail.com
ABSTRACT
We examined 44 bird specimens belonging to nine species of Ardeidae from the most south region of
Brazil, close to Uruguay boundaries. The aim of the study was to report the occurrence of species of
helminths for the aquatic birds, quantify the infections by host species as well as to present a revision of
helminths of Ardeidae of Brazil. The aquatic birds were parasitized by helminths from 18 taxa: five
Nematoda, nine Trematoda, and four Acanthocephala. New records of helminths for Ardeidae in Brazil
have been reported, and Ardea cocoi and Ardea alba stood out by the number of associated species.
Keywords: Acanthocephala – Ardeidae – Brazil – Digenea – Helminths – Nematoda
RESUMEN
Se examinaron 44 ejemplares pertenecientes a las nueve especies de Ardeidae del extremo sur del estado
de Rio Grande do Sul. El objetivo del estudio fue relatar la ocurrencia de las especies de helmintos para las
aves, cuantificar las infecciones por especie hospedadora, además de presentar una revisión de helmintos
de Ardeidae de Brasil. Las aves acuáticas fueron positivas para 18 tasas, cinco Nematoda, nueve
Trematoda y cuatro Acanthocephala. Los nuevos registros de helmintos para Ardeidae en Brasil fueron
reportados. Ardea cocoi y Ardea alba se destacaron por el número de especies asociadas.
Palabras-claves: Acanthocephala – Ardeidae – Brasil – Digenea – Helmintos – Nematoda
Neotropical Helminthology, 2017, 11(2), jul-dic
Fedatto Bernardon et al.
358
INTRODUCTION
Parasitism is considered to be one of the most
successful lifestyles exhibited by living organisms
(Poulin, 2000). The parasites represent a large
proportion of the existing diversity (Price, 1980)
and they can be used as biological markers of the
host's eating habits, the environment in which they
live, and even their migration routes (Amato &
Amato, 2010).
According to Piacentini et al. (2015) the world bird
diversity is estimated in more of 9,021 species.
Brazil has one of the three countries richest
avifauna in the world with 1,919 species, divided
into approximately 33 orders, among them
Pelecaniformes Sharpe, 1891, which include:
Ardeidae Leach, 1820, Pelecanidae Rafinesque,
1815, and Threskiornithidae Poche, 1904.
Ardeidae is composed of more than 60 species, is
one of the largest and most representative families
of birds with characteristics adapted to wet and
flooded areas (Scherer et al., 2006). At South
Brazil, in state of Rio Grande do Sul, 13 species are
recorded: Tigrisoma lineatum (Boddaert, 1783),
Botaurus pinnatus (Wagler, 1829), Ixobrychus
exilis (Gmelin, 1789), Ixobrychus involucres
(Vieillot, 1823), Nycticorax nycticorax
( Linnaeus, 1758 ) , Nyctanassa violacea
(Linnaeus,1758), Butorides striata (Linnaeus,
1758), Bubulcus ibis (Linnaeus, 1758), Ardea
cocoi Linnaeus, 1766, Ardea alba Linnaeus, 1758,
Syrigma sibilatrix (Temminck, 1824), Egretta
thula (Molina, 1782) and Egretta caerulea
(Linnaeus, 1758) (Bencke et al., 2010).
The predominant ecosystem is the Pampa Biome
which integrates part of Argentina, all of Uruguay
and a large part of the territory of the state of Rio
Grande do Sul (62.2%) (Boldrini et al., 2010). The
extreme southern region of Rio Grande do Sul
presents several protected wetlands, such as
“Estação Ecológica do Taim” (ESEC-Taim) and
the “Parque Nacional da Lagoa do Peixe”, natural
areas that shelter a unique diversity of wading birds
that use this environment for rest, reproduction and
feeding. Ardeidae occupy the top of the food chain
and their diet is composed by amphibians, reptiles,
insects and molluscs (Efe, 2001; Belton, 2004),
which may serve as intermediate or paratenic hosts
of helminths species.
Informations on helminths of Ardeidae in Brazil
was carried out by Travassos, (1926), Yamaguti
(1959), Travassos et al. (1969), Vicente et al.
(1995a), Vicente et al. (1995b), Arruda et al. (2001,
2002), Barros et al. (2002), Pinto & Noronha
(2003), Pinto et al. (2004), Muniz-Pereira et al.
(2004), Pinto et al. (2012), Pinto et al. (2013) and
Fernandes et al. (2015) however, in the state of Rio
Grande do Sul, studies with helminths were not
performed. In this sense, the objective of the
present study was to determine the helminths that
parasitize Ardeidae in this biogeographical area
and to quantify the infections by host species, also a
revision of the helminths is presented.
MATERIAL AND METHODS
Were examined 44 hosts belonging to the Ardeidae:
Ardea alba (n=6), Ardea cocoi (n=5), Butorides
striata (n=4), Bubulcus ibis (n=4), Egrettathula
(n=6), Ixobrychus involucris (n=6), Nycticorax
nycticorax (n=4), Syrigma sibilatrix (n=7) and
Tigrisoma lineatum (n=2) from the natural
environment of extreme southern Rio Grande do
Sul, Brazil. From the municipalities: Arroio do
Padre, Pelotas, Capão do Leão and Rio Grande (-
31º26'34"S -52º25'19"W; -31°46'19"S -
52°20'34"W;-31°45'46"S -52°29'02"W; -32°2'6"S
-52°5'56"W), respectively. The birds were donated
by the “Núcleo de Reabilitação da Fauna Silvestre
and Centro de Triagem de Animais Silvestres from
the Universidade Federal de Pelotas” (NURFS-
CETAS/UFPel), where they died during the period
of 2006 at 2015. Hosts were conditioned
individually, and forwarded at the “Laboratório de
Parasitologia de Animais Silvestres”
(LAPASIL/UFPel) and frozen until processing.
To collect helminths, these birds are necropsied
and their organs ( mouth, esophagus,
proventriculus, gizzard, cecum, small and large
intestines, trachea, lungs, heart, liver, gall bladder,
pancreas, reproductive system, kidneys, cloaca and
air sacs) were separated, opened and washed with
running water through a 150 µm mesh. The
helminths were fixed in AFA for 24 hours and were
stored in accordance with the protocol proposed by
Neotropical Helminthology, 2017, 11(2), jul-dic
359
Amato & Amato (2010). Trematoda and
Acanthocephala were stained with Langeron's
carmine and Nematoda were clarified with Aman's
lactophenol. They were mounted on permanent and
semi-permanent slides.
Morphological identification was performed in
accordance with Travassos et al. (1969), Dubois
(1970), Gibson et al. (2002), Johnson et al. (2004),
Jones et al. (2005), Bray et al. (2008) for
Trematoda (Digenea), Measures (1988), Vicente et
al. (1995b), Anderson (2000), Shamsi et al. (2009),
Gibbons (2010) and Shafey (2012) for Nematoda
and McDonald (1988) for Acanthocephala. The
term assemblage, was utilized according to concept
Fauth et al. (1996). The parameters calculated were
prevalence (P%), mean abundance of infection
(MA) and mean intensity of infection (MI),
according Bush et al. (1997). The voucher
specimens were deposited in the “Coleção do
Instituto Oswaldo Cruz (CHIOC),” from Rio de
Janeiro, Brasil” (numbers 35942-35946 and
37957-37962) and in the “Coleção de Helmintos
do Laboratório de Parasitologia de Animais
Silvestres” from Instituto de Biologia,
U n i v e r s i d a d e F e d e r a l d e P e l o t a s
(CHLAPASIL/UFPel) (numbers 351-471 and 623-
631).
The literature review of Ardeidae for Brazil was
constructed (checklist format) based on the
researches carried out in different places in Brazil
(Travassos, 1926; Yamaguti, 1959; Travassos et
al., 1969; Vicente et al., 1995a; Vicente et al.,
1995b; Arruda et al., 2001, 2002; Barros et al.,
2002; Pinto & Noronha, 2003; Pinto et al., 2004;
Muniz-Pereira et al., 2004; Pinto et al., 2012;
Pinto et al., 2013).
RESULTS AND DISCUSSION
Of the 44 hosts (belong nine species), P% = 97.72
were parasitized by at least one taxon. Were
identified 18 taxa, five Nematoda: Contracaecum
microcephalum (Rudolphi, 1809) (Ascaroidea:
Anisakidae) (P%=63.3; AM=17.6; IM=26.8),
Desportesius invaginatus (Linstow, 1901)
(Acuaroidea: Acuariidae) (P%=36.6; AM= 2.3;
IM=6.3), Desmidocercella ardeae (Nawrotzky,
1914) Yorke & Maspletone,1926 (Aproctoidea:
Desmidocercidae) (P%=20.4; AM=1.1; IM=5.3),
Baruscapillaria sp. (Trichinelloidea: Capillaridae)
(P%=13.6; AM=0.45; IM=3.3) and Eustrongylides
ignotus Jägerskiöld, 1909 (Dioctophymatoidea:
Dioctophymatidae) (P%=9.1; AM=0.9; IM=10.2).
Nine species of Trematoda ( Digenea):
Amphimerus interruptus (Opisthorchiidae)
(Braun, 1901) Barker, 1911 (P%=2.3; AM=0.06;
IM=3.0), Apharyngostrigea ardearum (Lutz,
1928) Dubois, 1968 (Syn. Apharyngostrigea
brasiliana Szidart, 1929 segundo Labriola &
Suriano 1998 (Strigeidae) (P%=36.6; AM=17.7;
IM=48.9), Ascocotyle sp. (Heterophydae)
(P%=22.7; AM=61.4; IM=270.4), Clinostomum
marginatum (Rodolphi, 1819) (P%=29.54;
AM=1.1; IM=3.6), Ithyclinostomum dimorphum
(Diesing, 1850) Witenberg, 1926 (Clinostomidae)
(P%=4.5; AM=0.1; IM=2.5), Episthmium
proximum Travassos, 1922 (P%=20.4; AM=1.0
IM=4.8), Nephrostomum limai Travassos, 1922
( P % = 1 5 . 9 0 ; A M = 1 . 3 6 ; I M = 8 . 6 )
(Echinostomatidae), Ribeiroia ondatrae (Price,
1931) Price, 1942 (Cathaemasiidae) (P%=11.3;
AM=3.1; IM=27.4) and Stomylotrema sp.
(Stomylotremidae) (P%=11.3; AM=0.27; IM=2.4)
and four Acantocephala: Acanthocephalus sp.
(Echinorhynchidae) (P%=2.3; AM=0.02; IM=1.0),
Andracantha sp. (P%=29.5; AM=11.6; IM=39.5),
Arhythmorhynchus sp. (P%=4.5; AM=0.1;
IM=2.5) and Polymorphus sp. (Plagiorhynchidae)
( P % = 2 5 . 0 ; A M = 5 . 5 ; I M = 2 1 . 9 ) . T h e
parasitological indexes by host specie are
presented in Table 1. Were found pregnant
proglottids of Cestodes of hosts (P% = 29.5), but
not possible identified because scolex were absent.
The literature review of Ardeidae for Brazil is
shown in Table 2.
Contracaecum microcephalum presented the
highest prevalence value (P%=63.3), followed by
the trematode Apharyngostrigea ardearum
(P%=36.6) and the acanthocephalan Andracantha
sp. (P%=29.54). Concerning to mean abundance of
infection, the same helminthes C. microcephalum,
A. ardearum and Andracantha sphad the highest
indexes (AM = 17.6, 17.7 and 11.6, respectively),
however, the highest mean intensity of infection
value was presented by Ascocotyle sp. (IMI =
270.4) (Table 1). Among the species of
Acanthocephala, there was the association
between Andracantha sp. and Polymorphus sp. in
Neotropical Helminthology, 2017, 11(2), jul-dic
Fedatto Bernardon et al.
360
100% of the infected hosts by the species. The
value highest of mean intensity of infection of
Acanthocephala was presented in Ardea cocoi
(IMI=86.6), while the highest number of
Acanthocephala species occurred in Ardea alba
(three species) according (Table 1). Bubulcus ibis
and T. lineatum were no infected for
Acanthocephala.
The nematodes Contracaecum microcephalum and
D. invaginatus parasited eight of nine species of
Ardeidae analyzed; Desmidocercella ardeae, A.
ardearum, Andracantha sp. and Polymorphus sp.
infected seven species of birds (7/9); C.
marginatum six (6/9); Ascocotyle sp. and N. limai
five (5/9); Stomylotrema sp. four (4/9); E.
proximum and R. ondatrae three (3/9);
Baruscapillaria s p . , E . i gnotus a n d
Arhythmorhynchus sp. two (2/9), and only one
species of Ardeidae (1/9) was infected by A.
interruptus, I. dimorphum and Acanthocephalus
sp. (Table 1).
In relation to the Nematoda life cycles identified,
C. microcephalum involves two intermediate
hosts: copepods (Crustacea) as first intermediate
hosts and second intermediate host, young
freshwater fish. The definitive hosts become
infected from consuming fish containing larvae
(Anderson, 2000). Desportesius invaginatus that is
found under the gizzard lining, has as second
intermediate host Discoglossus (Amphibia: Anura)
or fish (Cyprinidae) (Anderson, 2000).
Capillariidae parasite birds, mammals and fishes,
have monoxenous or heteroxenous biological
cycles (Anderson, 2000). Eustrongylides spp. were
found on the wall of proventriculus and gizzard,
form large tunnels on the surface of serosa or still in
the intestine. The infection may cause high
mortality mainly in young birds because due to
high pathogenicity (Spalding et al. 1993; Xiong et
al. 2009). Ingestion of aquatic Oligochaeta
(intermediate hosts) or fish (paratenic hosts) with
infective larvae are responsible for host infection
(Anderson, 2000).
The species of Trematoda have complex cycles of
development, involving one or more intermediate
hosts (Olsen, 1974). Some species identified in the
present study were more specific (A. interruptus
and I. dimorphum) and others species most
generalists, as A. ardearum. Acanthocephala is a
group of parasites obligate utilize Arthropoda as
intermediate hosts and vertebrate as definitive
hosts for complete their life cycle (Near, 2002).
These parasites are strongly linked to the aquatic
environment, and general aquatic birds and marine
mammals are definitive (McDonald 1988; Luque
et al. 2010).
Considering the parasitological diversity presented
in study, Trematoda was the taxa predominant
composed for nine species, followed by five
species of Nematoda and four of Acanthocephala
corroborating with researches with helminths of
Ardeidae realized by Chipev & Kostandinova
(1995) in Bulgaria; Labriola & Suriano (1998) and
Drago & Lunaschi (2011) in Argentina;
Nogueserola et al. (2002) in Spain; Al-Salim & Ali
(2010) in Iraq; Sitko (2012) in Czech republic;
Violante-González et al. (2012) in México; Shafey
(2012) in Egypt and Santoro et al. (2016) in Italy. In
present study, there was difference in the
composition of helminths associated with host
species. Ardea cocoi was parasitized by 14 species
of helminths, A. alba and N. nycticorax by 12
species, E. thula and S. sibilatrix by 10 species, B.
striata by seven species, B. ibis and I. involucris by
six species and T. lineatum by two species of
helminths.
The diversity of helminths and differences in
parasitic loads among Ardeidae may be related to
the variety of items consumed, quantity, behavioral
peculiarities and strategies of dispersion of
parasites. Ardea cocoi and A. alba had the highest
number of associated helminth species, these birds
are the largest Ardeidae occurring in Rio Grande do
Sul and usually share the feeding resources.
Infections are likely to have occurred by ingestion
of intermediate and paratenic hosts such as fish,
amphibians, reptiles, mollusks and insects, as these
constitute the diet of Ardeidae (Efe, 2001; Belton,
2004).
Researches with helminths associated with
Ardeidae in state of Rio Grande do Sul had not been
realized, therefore the work is pioneering in this
sense, being for the first time in the state reported
the taxa: Contracaecum microcephalum,
Desportesius invaginatus, Desmidocercella
ardeae, Baruscapillaria sp., Eustrongylides
ignotus (Nematoda); Amphimerus interruptus,
Neotropical Helminthology, 2017, 11(2), jul-dic
361
Table 1. Parasitological indexes for Ardeidae host's species from the state of Rio Grande do Sul, Brazil.
Ardeidae species
Parasites
P (%)
MA
MI
Ardea alba (n=6)
Nematoda
Contracaecum microcephalum
83.3
28.3
34.0
Desmidocercella ardeae
16.6
2.5
15.0
Desportesius invaginatus
Trematoda
Apharyngostrigea ardearum
33.3
83.3
10.3
31.6
31.0
38.0
Ascocotyle sp.
50.0
12.6
25.3
Clinostomum marginatum
50.0
3.0
6.0
Ephistmium proximum
66.6
3.8
5.75
Nephrostomum limai
16.6
0.3
2.0
Ribeiroia ondratae
Acantocephala
Acantocephalus sp.
50.0
16.6
14.6
0.16
29.3
1.0
Andracantha sp.
50.0
5.3
10.6
Polymorphus sp.
33.3
1.2
3.5
Ardea cocoi (n=5)
Nematoda
Contracaecum microcephalum
100.0
34.0
34.0
Desmidocercella ardea
60.0
3.4
5.6
Desportesius invaginatus
40.0
1.0
2.5
Baruscapillaria sp.
40.0
1.2
3.0
Eustrongylides ignotus
Trematoda
Apharyngostrigea ardearum
60.0
80.0
6.8
42.8
11.3
53.5
Ascocotyle sp.
60.0
111.8
186.3
Clinostomum marginatum
80.0
4.6
5.7
Ephistmium proximum
40.0
0.8
2.0
Ithyoclinostomum dimorphum
40.0
1.0
2.5
Nephrostomum limai
20.0
1.4
7.0
Ribeiroia ondratae
Acanthocephala
Andracantha sp.
20.0
60.0
7.0
52.0
35.0
86.6
Polymorphus sp.
40.0
16.8
42.0
Butorides striata (n=4)
Nematoda
Contracaecum microcephalum
100.0
8.5
8.5
Desmidocercella ardeae
25.0
2.7
11.0
Desportesius invaginatus
Trematoda
Amphimerus interruptus
50.0
25.0
1.2
0.75
2.5
3.0
Clinostomum marginatum
Acanthocephala
Andracantha sp.
50.0
50.0
2.5
42.5
5.0
85.0
Polymorphus sp.
50.0
0.5
2.0
Neotropical Helminthology, 2017, 11(2), jul-dic
Fedatto Bernardon et al.
362
Continuation Table1.
Ardeidae species
Parasites
P (%)
MA
MI
Bubulcus ibis (n=4)
Nematoda
Contracaecum microcephalum
50.0
3.5
7.0
Desportesius invaginatus
Trematoda
Apharyngostrigea ardearum
25.0
50.0
0.2
9.5
1.0
19.0
Ascocotyle sp.
25.0
7.0
28.0
Nephrostomum limai
25.0
2.0
8.0
Stomylotrema sp.
25.0
2.5
10.0
Egretta thula (n=6)
Nematoda
Contracaecum microcephalum
66.6
1.5
2.2
Desmidocercella ardeae
16.6
0.2
1.0
Desportesius invaginatus
50.0
0.6
1.3
Baruscapillaria sp.
Digenea
Apharyngostrigea ardearum
66.6
16.6
2.3
21.1
3.5
127.0
Clinostomum marginatum
16.6
0.3
2.0
Ephistmium proximum
50.0
2.8
5.6
Stomylotrema sp.
Acanthocephala
Andracantha sp.
16.6
16.6
0.2
1.0
1.0
6.0
Polymorphus sp.
16.6
0.6
4.0
Ixobrychus involucris (n=6)
Nematoda
Contracaecum microcephalum
83.3
42.6
51.2
Desmidocercella ardeae
16.6
0.16
1.0
Desportesius invaginatus
Trematoda
Clinostomum marginatum
33.3
16.6
2.0
0.3
6.0
2.0
Acanthocephala
Andracantha sp.
16.6
0.2
1.0
Polymorphus sp.
33.3
0.2
0.5
Apharyngostrigea ardearum, Ascocotyle sp.,
Clinostomum marginatum, Ithyclinostomum
d i m o r p h u m , E p i s t h m i u m p ro x i m u m ,
Nephrostomum limai, Ribeiroia ondatrae,
Stomylotrema sp. (Trematoda); Acanthocephalus
sp., Andracantha sp., Arhythmorhynchus sp. and
Polymorphus sp. (Acanthocephala) and their
indexes parasitological.
New records of Nematoda to Ardeidae hosts in
Brazil were: C. microcephalum in A. cocoi, B. ibis,
I. involucris, N. nycticorax and S. sibilatrix;
Desportesius invaginatus in A. alba, A. cocoi, B.
ibis, B. striata, I. involucris, N. nycticorax and S.
sibilatrix; Desmidocercella ardeae in B. striata, E.
thula, I. involucris, S. sibilatrix and T. lineatum;
Baruscapillaria sp. in A. cocoi and E. thula. For the
Trematoda the new records were: Ascocotyle sp. in
A. alba, A. cocoi, B. ibis, N. nycticorax, and S.
sibilatrix; Apharyngostrigea ardearum in A. alba,
A. cocoi, B. ibis, E. thula, N. nycticorax, S.
sibilatrix and T. lineatum; Clinostomum
marginatum in E. thula and I. involucris;
Episthmium proximum in A. alba and E. thula;
Neotropical Helminthology, 2017, 11(2), jul-dic
363
Continuation Table 1.
Ardeidae species Parasites P (%)
MA
MI
Nycticorax nycticorax (n=4) Nematoda
Contracaecum microcephalum 50.0
30.5
61.0
Desportesius invaginatus 25.0
0.2
1.0
Eustrongylides ignotus 25.0
1.7
7.0
Trematoda
Apharyngostrigea ardearum 25.0
9.25
37.0
Ascocotyle sp. 50.0
448.7
897.5
Clinostomum marginatum 75.0
2.7
3.6
Nephrostomum limai 50.0
10.0
20.0
Ribeiroia ondratae 25.0
3.5
14.0
Stomylotrema sp. 25.0
0.2
1.0
Acanthocephala
Andracantha sp. 50.0
10.2
20.5
Arhytmorhynchus sp. 25.0
0.2
1.0
Polymorphus sp. 50.0
4.0
8.0
Syrigma sibilatrix (n=7)
Nematoda
Contracaecum microcephalum
28.5
0.3
1.0
Desmidocercella ardeae
14.3
0.3
2.0
Desportesius invaginatus
Trematoda
Apharyngostrigea ardearum
42.8
28.5
1.6
24.4
3.6
85.5
Ascocotyle sp.
14.3
35.1
246.0
Nephrostomum limai
28.6
0.4
1.5
Stomylotrema sp.
Acanthocephala
Andracantha sp.
28.6
14.3
0.4
0.43
1.5
3.0
Arhytmorhynchus sp.
14.3
0.6
4.0
Polymorphus sp.
14.3
18.1
127.0
Tigrisoma lineatum (n=2)
Nematoda
Desmidocercella ardeae
50.0
0.5
1.0
Trematoda
Apharyngostrigea ardearum
50.0
2.5
5.0
Nephrostomum limai in A. alba, A. cocoi, B. ibis
and N. nycticorax; Ribeiroia ondatrae in A. alba, A.
cocoi and N. nycticorax; Stomylotrema sp. in B.
ibis, E. thula and N. nycticorax. For to
Acanthocephala: Acanthocephalus sp. in A. alba;
Arhythmorhynchus sp. in N. nycticorax and S.
sibilatrix; Andracantha sp. in A. alba, A. cocoi, B.
striata, E. thula, I. involucris, N. nycticorax and S.
sibilatrix; Polymorphus sp. in A. alba, A. cocoi, B.
striata, E. thula, I. involucris, N. nycticorax and S.
sibilatrix.
The records, and indexes as well as the presentation
of the Ardeidae helminth checklist aim to
contribute to existing knowledge in Brazil.
Neotropical Helminthology, 2017, 11(2), jul-dic
Fedatto Bernardon et al.
364
Table 2. Checklist from helminths from Ardeidae (Aves: Pelecaniformes) in Brazil.
Ardeidae species Taxon Reference
Cestoda
Ardeidae sp. Jardugia sp. Arruda et al. (2001)
Trematoda
Ardea sp. Clinostomum marginatum (Rudolphi, 1819) Travassos et al. (1969)
Parastrigea cincta (Brandes, 1888) Travassos et al. (1969)
Trematoda
Agami agami (Gmelin, 1789) Posthodiplostomum grande (Diesing, 1850) Travassos et al. (1969)
Posthodiplostomum microsicya Dubois, 1936 Travassos et al. (1969)
Sphincterodiplostomum musculosum Dubois, 1936 Travassos et al. (1969)
Ardea alba Linnaeus, 1758
Trematoda
Apharyngostrigea ardearum (Lutz, 1928) present study
Ascocotyle sp. present study
Clinostomum detruncatum Braun, 1899 Travassos et al. (1969)
Clinostomum marginatum (Rudolphi, 1819) Travassos et al. (1969); Pinto et al. (2004)
Clinostomum marginatum (Rudolphi, 1819) present study
Ephishmium proximum Travassos, 1922 present study
Ignavia venusta Freitas, 1948 Travassos et al. (1969)
Ithyoclinostomum dimorphum (Diesing, 1850) Pinto et al. (2004)
Nephrostomum limai Travassos, 1922 present study
Opisthorchis sp. Travassos et al. (1969)
Philophtalmus lacrymosus Braun, 1902 Travassos et al. (1969)
Posthodiplostomum grande (Diesing, 1850) Travassos et al. (1969)
Ribeiroia insignis Travassos, 1939 Travassos et al. (1969)
Ribeiroia ondatrae (Price, 1931) Price, 1942 present study
Nematoda
Spiruroidea Arruda et al. (2001)
Contracaecum sp. Vicente et al. (1995b)
Contracaecum microcephalum (Rudolphi, 1819) Vicente et al. (1995b)
Contracaecum microcephalum (Rudolphi, 1819) present study
Contracaecum multipapillatum (Drasche, 1882) Pinto et al. (2004)
Desmidocercella ardeae (Nawrotzki, 1914) Pinto et al. (2004)
Desmidocercella ardeae (Nawrotzki, 1914) present study
Desportesius invaginatus (Linstow, 1901) present study
Eustrongylides sp. Vicente et al. (1995b)
Eustrongylides perpapillatus Jägerskiöld, 1909 Vicente et al. (1995b)
Eustrongylides ignotus Jagerskiold, 1909 Pinto et al. (2004)
Porrocaecum reticulatum (Linstow, 1899) Vicente et al. (1995b)
Neotropical Helminthology, 2017, 11(2), jul-dic
365
Continuation Table 2
Ardeidae species Taxon Reference
Ardea alba Linnaeus, 1758
Ardea cinerea Linnaeus, 1758
Cestoda
Deudrouterina pilherodiae Mahon, 1956 Arruda et al. (2001)
Valipora mutabilis Linston, 1927 Pinto et al. (2004)
Acanthocephala
Acanthocephalus sp. present study
Andracantha sp. present study
Centrorhynchus spinosus (Kaiser, 1893) Travassos (1926)
Polymorphus sp. present study
Polymorphus mutabilis (Rudolphi, 1819) Travassos (1926)
Polymorphus striatus (Goeze, 1782) Travassos (1926)
Acanthocephala
Polymorphus striatus (Goeze, 1782) Travassos (1926)
Trematoda
Ardea cocoi Linnaeus, 1766 Amphimerus interruptus (Braun, 1909) Arruda et al. (2001)
Apharyngostrigea ardearum (Lutz, 1928) present study
Ascocotyle sp. present study
Ascocotyle (Phagicola) longa Ransom, 1920 Barros et al. (2002); Pinto et al. (2004)
Cladocystis trifolium (Braun, 1901) Travassos et al. (1969)
Clinostomatopsis sorbens (Braun,1899) Travassos et al. (1969)
Clinostomum detruncatum Braun, 1899 Travassos et al. (1969)
Clinostomum marginatum Rudolphi, 1819 Travassos et al. (1969); Pinto et al. (2004)
Clinostomum marginatum (Rudolphi, 1819) present study
Clinostomum heluans Braun, 1899 Travassos et al. (1969)
Episthmium oscari Travassos, 1922 Travassos et al. (1969)
Episthmium proximum Travassos, 1922 Travassos et al. (1969)
Episthmium proximum Travassos, 1922 present study
Ithyoclinostomum dimorphum (Diesing, 1850) Travassos et al. (1969); Pinto et al. (2004)
Ithyoclinostomum dimorphum (Diesing, 1850) present study
Nephrostomum limai Travassos, 1922 present study
Phagicola angrense (Travassos, 1916) Arruda et al. (2001)
Proctobium proctobium (Travassos, 1918) Arruda et al. (2001)
Prorrocaecum reticulatus (Linstow, 1899) Vicente et al. (1995b)
Ribeiroia ondatrae (Price, 1931) Price, 1942 present study
Nematoda
Baruscapillaria sp. present study
Contracaecum sp. Vicente et al. (1995b)
Contracaecum multipapillatum (Drasche, 1882) Vicente et al. (1995b); Pinto et al. (2004)
Contracaecum microcephalum (Rudolphi, 1819) present study
Neotropical Helminthology, 2017, 11(2), jul-dic
Fedatto Bernardon et al.
366
Continuation Table 2
Ardeidae species Taxon Reference
Nematoda
Ardea cocoi Linnaeus, 1766
Desmidocercella ardeae (Nawrotzki, 1914) Vicente et al. (1995b)
Desmidocercella ardeae (Nawrotzki, 1914) present study
Desportesius invaginatus (Linstow, 1901) present study
Eustrongylides ignotus Jagerskiold, 1909 Vicente et al. (1995b); Pinto et al. (2004)
Prorrocaecum sp. Vicente et al. (1995b)
Cestoda
Anomotaenia sp. Arruda et al. (2001)
Deudrouterina sp. Arruda et al. (2001)
Drepanidotaenia sp. Arruda et al. (2001)
Acanthocephala
Andracantha sp. present study
Polymorphus sp. present study
Nematoda
Ardea herodias Linnaeus, 1758 Contracaecum perpapillatus Jagerskiold, 1909 Vicente et al. (1995b)
Acanthocephala
Polymorphus obtusus Van Cleave, 1918 Travassos (1926)
Nematoda
Ardea leuca Eustrongylides multipapillatus Jagerskiold, 1909 Vicente et al. (1995b)
Acanthocephala
Ardea purpurea Linnaeus, 1766 Arhythmorhynchus macrourus Bremser, 1821 Travassos (1926)
Trematoda
Butorides sp. Phagicola angrense (Travassos, 1916) Arruda et al. (2001)
Cestoda
Drepanidotaenia sp. Arruda et al. (2001)
Trematoda
Botaurus pinnatus (Wagler, 1829) Posthodiplostomum microsicya Dubois, 1936 Travassos et al. (1969)
Nematoda
Eustrongylides ignotus Jagerskiold, 1909 Vicente et al. (1995b)
Acanthocephala
Botaurus lentigiosus (Rackett, 1813) Arhythmorhynchus pumidirostris Cleave, 1916 Travassos (1926)
Polymorphus breves Cleave, 1916 Travassos (1926)
Acanthocephala
Botaurus stellaris (Linnaeus, 1758) Polymorphus striatus (Goeze, 1782) Travassos (1926)
Prosthorhynchus spiralis (Rudolphi, 1809) Travassos (1926)
Trematoda
Butorides striata Linnaeus, 1758 Ascocotyle (Phagicola) angrense (Travassos, 1916) Pinto et al. (2013)
Ascocotyle (Phagicola) pindoramensis (Travassos, 1928)
Pinto et al. (2013)
Amphimerus interruptus Braun,1901 Travassos et al. (1969)
Neotropical Helminthology, 2017, 11(2), jul-dic
367
Continuation Table 2
Ardeidae species Taxon Reference
Trematoda
Butorides striata Linnaeus, 1728
Amphimerus interruptus Braun,1901 present study
Apharyngostrigea brasiliana (Szidat, 1929) Arruda et al. (2001)
Centrocestus formosanus (Nishigori, 1924) Pinto et al. (2013)
Clinostomum marginatum (Rudolphi, 1819) present study
Clinostomum marginatum Rudolphi, 1819 Travassos et al. (1969); Pinto et al. (2013)
Clinostomum heluans Braun, 1899 Pinto et al. (2013)
Diplostomum sp. Arruda et al. (2001)
Echinostoma sp. Travassos et al. (1969)
Episthmium oscari Travassos, 1922 Travassos et al. (1969)
Gynaecotyla adunca (Linton, 1905)
Arruda et al. (2001); Muniz-Pereira et al. (2004)
Maritrema sp. Arruda et al. (2001)
Mesostephanus infecundus Lutz, 1935 Arruda et al. (2001)
Phagicola angrense (Travassos, 1916) Travassos et al. (1969)
Posthodiplostomum nanum Dubois, 1937 Travassos et al. (1969); Pinto et al. (2013)
Prosthogonimus ovatus (Rudolphi, 1803) Pinto et al. (2013)
Nematoda
Contracaecum sp. Vicente et al. (1995b)
Contracaecum multipapillatum (Drasche, 1882) Pinto et al. (2004)
Contracaecum microcephalum(Rudolphi, 1809) Vicente et al. (1995b)
Contracaecum microcephalum (Rudolphi, 1819) present study
Desmidocercella ardeae (Nawrotzki, 1914) present study
Desportesius invaginatus (Linstow, 1901) present study
Pelecitus sp. Pinto & Noronha (2003)
Thelazia aquilina Baylis, 1934 Vicente et al. (1995b)
Cestoda
Diploposthe bifaria Siebold, 1946 Arruda et al. (2001)
Drepanidotaenia sp. Arruda et al. (2001)
Valipora minuta (Coil, 1950) Pinto et al. (2012)
Acanthocephala
Butorides striata Linnaeus, 1758 Andracantha sp. present study
Polymorphus sp. present study
Polymorphus mutabilis (Rudolphi, 1819) Travassos (1926)
Butorides virescens (Linnaeus, 1758)
Cestoda
Raillietina macroscolecina (Fuhrmann, 1908) Yamaguti (1959)
Acanthocephala
Polymorphus mutabilis (Rudolphi, 1819) Travassos (1926)
Trematoda
Bubulcus ibis (Linnaeus, 1758) Apharyngostrigea ardearum (Lutz, 1928) present study
Neotropical Helminthology, 2017, 11(2), jul-dic
Fedatto Bernardon et al.
368
Continuation Table 2
Ardeidae species Taxon Reference
Trematoda
Bubulcusibis Linnaeus, 1758
Ascocotyle sp. present study
Nephrostomum limai Travassos, 1922 present study
Stomylotrema sp. present study
Nematoda
Contracaecum microcephalum (Rudolphi, 1819) present study
Desportesius invaginatus (Linstow, 1901) present study
Nematoda
Cochlearius cochlearius Contracaecum multipapillatum (Drasche, 1882) Vicente et al. (1995b); Pinto et al. (2004)
(Linnaeus, 1766)
Contracaecum sp.
Prorrocaecum sp.
Vicente et al. (1995b)
Vicente et al. (1995b)
Egretta thula (Molina, 1782)
Trematoda
Apharyngostrigea ardearum (Lutz, 1928)
present study
Ascocotyle felippei Travassos,1928
Travassos et al. (1969)
Clinostomum sp.
Travassos et al. (1969)
Clinostomum marginatum (Rudolphi, 1819)
present study
Episthmium proximum Travassos, 1922
present study
Ignavia venusta Freitas, 1948
Travassos et al. (1969)
Opisthorchis sp.
Travassos et al. (1969)
Proctobium proctobium (Travassos, 1918)
Arruda et al. (2001)
Stomylotrema sp.
present study
Nematoda
Baruscapillaria sp.
present study
Contracaecum sp.
Vicente et al. (1995b)
Contracaecum microcephalum (Rudolphi, 1819)
Vicente et al. (1995b)
Contracaecum microcephalum (Rudolphi, 1819)
present study
Desmidocercella ardeae (Nawrotzki, 1914)
present study
Desportesius invaginatus (Linstow, 1901)
Vicente et al. (1995b)
Desportesius invaginatus (Linstow, 1901)
present study
Porrocaecum sp.
Vicente et al. (1995b)
Porrocaecum reticulatum (Linstow, 1899)
Vicente et al. (1995b)
Cestoda
Anomotaenia aurita (Rudolphi, 1819)
Yamaguti (1959)
Dilepis fuhrmanni Railliet & Henry, 1909
Arruda et al. (2001)
Acanthocephala
Andracantha sp.
present study
Polymorphus sp.
present study
Polymorphus mutabilis (Rudolphi, 1819)
Travassos (1926)
Trematoda
Neotropical Helminthology, 2017, 11(2), jul-dic
369
2002
Continuation Table 2
Ardeidae species Taxon Reference
Trematoda
Egretta caerulea (Linnaeus, 1758) Ascocotyle felippei Travassos, 1928 Travassos et al. (1969)
Clinostomum heluans Braun, 1899 Travassos et al. (1969)
Gynaecotyla adunca (Linton, 1905)
Arruda et al. (2001); Muniz-Pereira et al. (2004)
Maritrema nicolli Travassos, 1920 Arruda et al. (2001)
Cestoda
Dilepis papillifera Fuhrmann, 1908 Yamaguti (1959)
Acanthocephala
Polymorphus corynosoma Travassos, 1915 Travassos (1926)
Trematoda
Ixobrychus exilis erythromelas Ascocotyle felippei Travassos, 1929 Travassos et al. (1969)
Vieilliot, 1817 Phagicola angeloi (Travassos, 1929) Travassos et al. (1969)
Phagicola angrense (Travassos, 1916) Travassos et al. (1969)
Pygidiopsis pindoramensis Travassos, 1929 Travassos et al. (1969)
Nematoda
Porrocaecum sp. Vicente et al. (1995b)
Trematoda
Ixobrychus exilis (Gmelin, 1789) Ascocotyle (Phagicola) rara Arruda, Muniz-Pereira & Pinto,
Cestoda
Arruda et al. (2002)
Drepanidotaenia sp. Arruda et al. (2001)
Trematoda
Ixobrychus involucris (Vieillot, 1823)Clinostomum marginatum (Rudolphi, 1819) present study
Nematoda
Contracaecum microcephalum (Rud., 1819) present study
Desmidocercella ardeae (Nawrotzki, 1914) present study
Desportesius invaginatus (Linstow, 1901) present study
Acanthocephala
Andracantha sp. present study
Polymorphus sp. present study
Acanthocephala
Ixobrychus minutus (Linnaeus, 1766) Polymorphus striatus (Goeze, 1782) Travassos (1926)
Prosthorhynchus spiralis (Rudolphi, 1809)
Travassos (1926)
Trematoda
Nycticorax Forster, 1817 Ithyoclinostomum dimorphum (Diesing, 1850) Arruda et al. (2001)
Acanthocephala
Polymorphus corynosoma Travassos, 1915 Travassos (1926)
Trematoda
Nycticorax nycticorax Amphimerus interruptus (Braun, 1909) Arruda et al. (2001)
(Linnaeus, 1758) Apharyngostrigea ardearum (Lutz, 1928) present study
Neotropical Helminthology, 2017, 11(2), jul-dic
Fedatto Bernardon et al.
370
Continuation Table 2
Ardeidae species Taxon Reference
Nycticorax nycticorax
(Linnaeus, 1758)
Trematoda
Ascocotyle sp. present study
Clinostomum marginatum Rudolphi, 1819 Travassos et al. (1969); Pinto et al. (2004)
Clinostomum marginatum (Rudolphi, 1819) present study
Episthmium proximum Travassos, 1922 Travassos et al. (1969)
Ithyoclinostomum dimorphum (Diesing, 1850) Pinto et al. (2004)
Levinseniella sp. Arruda et al. (2001)
Nephrostomum limai Travassos, 1922 present study
Trematoda
Nycticorax nycticorax Pygidiopsis pindoramensis Travassos, 1929 Arruda et al. (2001)
(Linnaeus, 1758) Ribeiroia ondatrae (Price, 1931) present study
Stomylotrema sp. present study
Nematoda
Avioserpens sp. Arruda et al. (2001)
Contracaecum sp. Vicente et al. (1995b)
Contracaecum microcephalum (Rudolphi, 1819) present study
Contracaecum multipapillatum (Drasche, 1882) Pinto et al. (2004)
Desportesius invaginatus (Linstow, 1901) present study
Eustrongylides ignotus Jagerskiold, 1909 Pinto et al. (2004)
Eustrongylides ignotus Jagerskiold, 1909 present study
Pelecitus sp. Pinto & Noronha (2003)
Tetrameres cochleare Travassos, 1917 Arruda et al. (2001)
Cestoda
Valipora mutabilis Linston, 1927 Pinto et al. (2004)
Acanthocephala
Andracantha sp. present study
Arhytmorhynchus sp. present study
Polymorphus sp. present study
Polymorphus striatus (Goeze, 1782) Travassos (1926)
Trematoda
Nycticorax nycticorax hoacli Clinostomum marginatum (Rudolphi, 1819) Travassos et al. (1969)
(Gmelin, 1789) Ephishmium proximum Travassos, 1922 Travassos et al. (1969)
Nematoda
Avioserpens sp. Arruda et al. (2001)
Capilaria brasiliana Freitas, 1933 Vicente et al. (1995b)
Contracaecum sp. Vicente et al. (1995b)
Contracaecum multipapillatum (Drasche, 1882) Vicente et al. (1995b)
Contracaecum plagiaticium Lent & Freitas, 1948 Vicente et al. (1995b)
Porrocaecum reticulatum (Linstow, 1899) Vicente et al. (1995)
Neotropical Helminthology, 2017, 11(2), jul-dic
371
Continuation Table 2
Ardeidae species Taxon Reference
Nycticorax nycticorax hoacli
(Gmelin, 1789)
Acanthocephala
Polymorphus mutabilis (Rudolphi, 1819) Travassos (1926)
Polymorphus inerme Travassos, 1923 Travassos (1926)
Trematoda
Nyctanassa violacea (Linnaeus, 1758) Apatemom globiceps Dubois, 1937 Arruda et al. (2001)
Apharyngostrigea brasiliana (Szidat, 1929) Arruda et al. (2001)
Clinostomum marginatum Rudolphi, 1819 Arruda et al. (2001)
Diplostomum sp. Arruda et al. (2001)
Gynaecotyla adunca (Linton, 1905)
Arruda et al. (2001); Muniz-Pereira et al. (2004)
Levinseniella sp. Arruda et al. (2001)
Levinseniella cruzi Travassos, 1920 Arruda et al. (2001)
Maritrema sp. Arruda et al. (2001)
Maritrema nicolli Travassos, 1920 Arruda et al. (2001)
Phagicola angrense (Travassos, 1916) Arruda et al. (2001)
Philophtalmus lacrymosus Braun, 1902 Arruda et al. (2001)
Proctobium proctobium Arruda et al. (2001)
Pygidiopsis pindoramensis Travassos, 1929 Arruda et al. (2001)
Nematoda
Nyctanassa violacea (Linnaeus, 1758) Acuaria sp. Arruda et al. (2001)
Cheilospirura hamulosa (Diesing, 1851) Arruda et al. (2001)
Acanthocephala
Polymorphus mutabilis (Rudolphi, 1819) Travassos (1926)
Polymorphus corynosoma Travassos, 1915 Travassos (1926)
Filicollis sphaerocephalus (Bremser, 1819) Travassos (1926)
Trematoda
Nyctanassa violacea cayennensis Clinostomum heluans Braun, 1899 Travassos et al. (1969)
(Gmelin, 1789) Clinostomum marginatum (Rudolphi, 1819) Travassos et al. (1969)
Cloacitrema oswaldoi Travassos, 1940 Travassos et al. (1969)
Echinostoma revolutum (Froelich, 1802) Travassos et al. (1969)
Lyperosomum sinuosum Travassos, 1917 Travassos et al. (1969)
Parorchis proctobium (Travassos, 1918) Travassos et al. (1969)
Prohemistomum odhneri Travassos, 1924 Travassos et al. (1969)
Stephanoprora singularis ( Lutz, 1924) Travassos et al. (1969)
Nematoda
Nyctanassa violacea cayennensis Contracaecum sp. Vicente et al. (1995b)
(Gmelin, 1789) Tetrameres micropenis Travassos, 1925 Vicente et al. (1995b)
Trematoda
Pilherodius pileatus (Boddaert, 1783) Amphimerus interruptus (Braun, 1909) Arruda et al. (2001)
Neotropical Helminthology, 2017, 11(2), jul-dic
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Continuation Table 2
Ardeidae species Taxon Reference
Trematoda
Pilherodius pileatus (Boddaert, 1783)
Ephishmium proximum Travassos, 1922 Travassos et al. (1969)
Nematoda
Contracaecum plagiaticium Lent & Freitas, 1948 Vicente et al. (1995b)
Contracaecum sp. Vicente et al. (1995b)
Cestoda
Dendroteurina pilherodiae Mahon, 1956 Yamaguti (1959); Arruda et al. (2001)
Valipora sp. Arruda et al. (2001)
Trematoda
Syrigma sibilatrix (Temminck, 1824) Amphimerus interruptus (Braun, 1909) Arruda et al. (2001)
Apharyngostrigea ardearum (Lutz, 1928) present study
Ascocotyle sp. present study
Nephrostomum limai Travassos, 1922 Travassos et al. (1969)
Nephrostomum limai Travassos, 1922 present study
Stomylotrema sp. present study
Stomylotrema gratiosus Travassos, 1922 Arruda et al. (2001)
Nematoda
Contracaecum microcephalum (Rudolphi, 1819) present study
Desmidocercella ardeae (Nawrotzki, 1914) present study
Desportesius invaginatus (Linstow, 1901) present study
Cheilospirura harmulosa (Diesing, 1851) Arruda et al. (2001)
Pelecitus sp. Arruda et al. (2001)
Pelecitus vuylstekae (Molin, 1860) Pinto & Noronha (2003)
Tetrameres sp. Vicente et al. (1995b)
Viktocara sp. Vicente et al. (1995b)
Acanthocephala
Syrigma sibilatrix (Temminck, 1824) Andracantha sp. present study
Arhytmorhynchus sp. present study
Polymorphus sp. present study
Nematoda
Tigrisoma sp. Contracaecum sp. Vicente et al. (1995b)
Trematoda
Tigrisoma lineatum (Boddaert, 1783) Amphimerus interruptus (Braun, 1909) Arruda et al. (2001)
Clinostomum marginatum Rudolphi, 1819 Arruda et al. (2001)
Ithyoclinostomum dimorphum (Diesing, 1850) Arruda et al. (2001)
Apharyngostrigea ardearum (Lutz, 1928) present study
Nematoda
Pelecitus sp. Vicente et al. (1995b); Arruda et al. (2001)
Desmidocercella ardeae (Nawrotzki, 1914) present study
Neotropical Helminthology, 2017, 11(2), jul-dic
373
Continuation Table 2
Ardeidae species Taxon Reference
Trematoda
Tigrisoma lineatum marmoratum
Clinostomum detruncatum Braun, 1899
Travassos et al. (1969)
(Vieillot, 1817)
Episthmium oscari Travassos, 1922
Travassos et al. (1969)
Nematoda
Contracaecum sp.
Vicente et al. (1995b)
Eustrongylides sp.
Vicente et al. (1995b)
Porrocaecum reticulatum (Linstow, 1899)
Vicente et al. (1995b)
ACKNOWLEDGMENTS
We thank the “Núcleo de Reabilitação e Centro de
Triagem de Animais Silvestres” (NURFS-CETAS-
UFPel) for donating the material. The
“Coordenação de Aperfeiçoamento do Pessoal de
Nível Superior (CAPES)” for the master
scholarship of the first author and for the financial
support provided through the edict no. 2010/32.
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