Research Note
Rev. Bras. Parasitol. Vet., Jaboticabal, v. 22, n. 3, p. 427-432, jul.-set. 2013
ISSN 0103-846X (impresso) / ISSN 1984-2961 (eletrônico)
Petasiger Dietz, 1909 (Trematoda: Echinostomatidae)
in Birds and Mollusks from Brazil
Petasiger Dietz, 1909 (Trematoda: Echinostomatidae) em aves e moluscos do Brasil
Hudson Alves Pinto1*; Germán Arturo Bohórquez Mahecha2; Alan Lane de Melo1
1
Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais – UFMG,
Belo Horizonte, MG, Brasil
2
Departamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais – UFMG,
Belo Horizonte, MG, Brasil
Received March 18, 2013
Accepted May 9, 2013
Abstract
Species of Petasiger Dietz, 1909 are intestinal trematodes of aquatic birds. Despite the diversity of described species
in Europe and North America, only two South American species are known and no species have been previously
reported in birds from Brazil. During a study of helminths recovered from the Least Grebe, Tachybaptus dominicus
(Linnaeus, 1766), from the state of Minas Gerais, Brazil, adult trematodes identified as Petasiger novemdecim Lutz,
1928 were found. The prevalence of infection was 55% (5/9), and the mean intensity of infection was 8 (1-32)
parasites. Additionally, Biomphalaria straminea (Dunker, 1848) and Biomphalaria tenagophila (d’Orbigny, 1835)
obtained from aquatic collections in the same state were found to harbor two species of echinostome cercariae of
the Magnacauda group. These cercariae developed into metacercariae in experimentally infected Poecilia reticulata
Peters, 1859. Attempts to obtain adult parasites in vertebrate host models (mice, chickens, ducks and canaries) were
unsuccessful. The present study is the first report of Petasiger in Brazilian birds and the first morphological description
of larvae of these parasites in Brazilian mollusks. Taxonomic aspects related to South American species of Petasiger
are discussed. It is suggested that, based on significant morphological differences observed in larval stages (i.e., larval
dimensions) and adult parasites (i.e., disposition of the testes), Petasiger caribbensis Nassi, 1980 should be reconsidered
as a distinct species from P. novemdecim.
Keywords: Trematodes, grebes, mollusks, cercariae, Petasiger, Brazil.
Resumo
Espécies do gênero Petasiger Dietz, 1909 são trematódeos intestinais de aves aquáticas. Apesar da diversidade de
espécies descritas na Europa e América do Norte, somente duas espécies são conhecidas na América do Sul, e nenhuma
espécie reportada previamente em aves do Brasil. Durante o estudo de helmintos recuperados de Mergulhão pequeno,
Tachybaptus dominicus (Linnaeus, 1766), do estado de Minas Gerais, Brasil, trematódeos adultos identificados como
Petasiger novemdecim Lutz, 1928 foram encontrados. A prevalência de infecção foi 55% (5/9) e a intensidade média
de infecção 8 (1-32) parasitos. Adicionalmente, Biomphalaria straminea (Dunker, 1848) e Biomphalaria tenagophila
(d’Orbigny, 1835) obtidas em coleções aquáticas do mesmo estado foram encontradas albergando duas espécies de
cercárias do tipo equinóstoma pertencentes ao grupo Magnacauda. Estas cercárias desenvolveram-se em metacercárias
em Poecilia reticulata Peters, 1859 experimentalmente infectados. Tentativas de obtenção de parasitos adultos em
modelos experimentais (camundongos, frangos, patos e canários) demonstraram-se sem sucesso. O presente estudo é o
primeiro relato de Petasiger em aves brasileiras e primeira descrição morfológica de larvas destes parasitos em moluscos
do Brasil. Aspectos taxonômicos relacionados às espécies sul-americanas de Petasiger são discutidos. Sugere-se que, em
vista das diferenças morfológicas observadas nos estágios larvais (i.e., dimensões das larvas) e dos parasitos adultos (i.e.,
disposição dos testículos), Petasiger caribbensis Nassi, 1980 seja reconsiderada espécie distinta de P. novemdecim.
Palavras-chave: Trematódeos, mergulhões, moluscos, cercárias, Petasiger, Brasil.
*Corresponding author: Hudson Alves Pinto
Laboratório de Taxonomia e Biologia de Invertebrados, Departamento de
Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas
Gerais – UFMG, CP 486, CEP 30123-970, Belo Horizonte, MG, Brasil
e-mail: hudsonalves13@ig.com.br
www.cbpv.com.br/rbpv
428
Pinto, H.A. et al.
Species of the genus Petasiger Dietz, 1909 are intestinal
trematodes of aquatic birds that are mainly found in grebes. This
genus currently includes 19 valid species and has a worldwide
distribution (KOSTADINOVA, 2005; FALTÝNKOVÁ et al., 2008;
LUNASCHI; DRAGO, 2010). The life cycle of these parasites was
elucidated by experimental infection studies and more recently
with the aid of molecular approaches. Echinostome cercariae of
the Magnacauda group are formed within planorbid mollusks.
After emerging from the mollusks, cercariae display a fishing lure
swimming behavior and are ingested by fish, in which they encyst
in the oral cavity. Upon ingestion of the fish by fish-eating birds,
the metacercariae develop into adult parasites in the small intestines
of these hosts (BEAVER, 1939; ABDEL-MALEK, 1952, 1953;
KOSTADINOVA; CHIPEV, 1992; GEORGIEVA et al., 2012).
Despite the diversity of species of Petasiger in Europe and
North America, only two species have been identified in birds
from South America: Petasiger novemdecim Lutz, 1928, described
in the Least Grebe, Tachybaptus dominicus (Linnaeus, 1766) in
Venezuela (LUTZ, 1928), and Petasiger argentinensis Lunaschi
and Drago, 2010 described in both the Great Grebe, Podiceps
major (Boddaert, 1783), and the White-Tufted Grebe, Rollandia
rolland (Quoy and Gaimard, 1824) in Argentina (LUNASCHI;
DRAGO, 2010). In addition, two undetermined species of
Petasiger were reported in Argentina: Petasiger sp. 1 was found in
the Cocoi Heron, Ardea cocoi Linnaeus, 1766, and Petasiger sp. 2
was recovered from the Black Vulture, Coragyps atratus (Bechstein,
1793) (DRAGO; LUNASCHI, 2011). Information regarding the
occurrence of larval stages of Petasiger in South America is scarce.
However, records are available of mollusks naturally infected
with P. novemdecim in Venezuela (NASIR et al., 1972) and with
Petasiger sp. in Argentina, Brazil, and Venezuela (MILWARDDE-ANDRADE; CAMPOS, 1969; OSTROWSKI DE NÚÑEZ,
1981; OSTROWSKI DE NÚÑEZ et al., 1991).
In the present study 9 specimens of T. dominicus that were
collected by one of us (GABM) from locations in the state of Minas
Gerais, Brazil, in the 1990s were evaluated for the presence of
parasites. The birds were fixed in 10% formalin, and the viscera were
subsequently examined under a stereomicroscope. The digeneans
were collected, stained with alum acetocarmine, dehydrated using
an ascending ethanol gradient, cleared in beechwood creosote and
mounted on permanent slides in Canada balsam.
Additionally, species of Biomphalaria Preston, 1910 were
collected during malacological surveys carried out in water
bodies in the state of Minas Gerais, Brazil, and examined for
infection with larval trematodes. Some of these planorbids were
found to harbor echinostome cercariae of the Magnacauda
group. Rediae were recovered from naturally infected mollusks
after they were pressed between glass slides and examined using
a stereomicroscope. Laboratory-reared Poecilia reticulata Peters,
1859 were experimentally infected with cercariae following the
protocol described by Pinto and Melo (2012). Metacercariae
were obtained from the oral cavities of these fish 10 days after
infection and force fed orally to experimental definitive hosts
(mice, chickens, ducks, and canaries). These hosts were killed
by cervical dislocation 5 days after infection, and their intestines
were examined for the presence of parasites.
Rev. Bras. Parasitol. Vet.
Parasite developmental stages were studied by light microscopy.
Images were obtained using a Leica ICC50 HD digital camera
attached to a light microscope. Measurements were obtained
during microscopy using an ocular micrometer or after microscopy
using Leica Application Suite (LAZ EZ) software version 2.0
(Leica Microsystem Ltd, Switzerland) to analyze captured images.
Cercariae were studied using vital stains and were later killed in
water at 70°C and fixed in 10% formalin solution. Parasites were
identified using taxonomic keys and species descriptions from
different authors (LUTZ, 1928; NASIR et al., 1972; NASSI,
1980; KOSTADINOVA, 2005; FALTÝNKOVÁ et al., 2008;
LUNASCHI; DRAGO, 2010). Morphometric data, presented
in micrometers, are given as the mean followed by the standard
deviation and range in parentheses. Relationships (ratios) between
measurements of the internal structures of adult parasites were
determined according to Faltýnková et al. (2008) and Lunaschi
and Drago (2010). The specimens studied were deposited in
the collection of the Laboratory of Taxonomy and Biology of
Invertebrates, Department of Parasitology, Federal University of
Minas Gerais, Brazil, under the access number DPIC 2457-2459.
Among the 9 specimens of T. dominicus examined, 5 (55%)
were infected with trematodes identified as P. novemdecim
(Figure 1). The mean intensity of infection was 8 parasites, with
a range of 1-32. Morphometric data for adult parasites recovered
from T. dominicus in the present study and previously reported
measurements of species of Petasiger from South American birds
are presented in Table 1.
Malacological surveys of aquatic collections from the state of
Minas Gerais, Brazil, revealed 2 species of Petasiger developing in
Biomphalaria spp. (Figure 2a-d). Infection rates were generally low
(<0.1%). Larvae from Petasiger sp. 1 were found in Biomphalaria
straminea (Dunker, 1848), while Petasiger sp. 2 was found in
B. straminea and Biomphalaria tenagophila (d’Orbigny, 1835).
Figure 1. Petasiger novemdecim obtained from Tachybaptus dominicus
in Brazil. (a) Adult parasite, entire view. (b) Detailed view of angle
and lateral collar spines. (c) Detailed view of dorsal collar spines.
429
Petasiger in Brazil
v. 22, n. 3, jul.-set. 2013
Table 1. Morphometric data for Petasiger novemdecim recovered from Tachybaptus dominicus in Brazil and measurements presented by other
authors for Petasiger species from South America. Abbreviations: BL = Body length, BW = Body width, CSW = Cirrus sac width, L = length,
E = egg, PHW = pharynx width, ODIV = distance from anterior extremity to intestinal bifurcation, OSW = oral sucker width, VSW = ventral
sucker width, VSL = ventral sucker length, W = width. *Calculated from the drawing presented by Nassi (1980).
Species
Reference
Petasiger novemdecim
Present study
Host
Locality
Body
Collar
Angle spines
Dorsal spines
Lateral spines
Oral sucker
Prepharynx
Pharynx
Esophagus
Ventral sucker
Cirrus sac
Ovary
Anterior
testis
Posterior
testis
Eggs
ODIV
ODIV/BL
OSW/PHW
CSW/BW
CSW/VSW
BW/VSW
VSW/CSW
BL/E
BL/VSL
L
W
L
W
L
L
L
L
W
L
L
W
L
L
W
L
W
L
W
L
W
L
W
L
W
Nasir et al., 1972 Faltýnková et al., 2008
P. caribbensis
P. argentinensis
Nassi, 1980
Lunaschi and Drago, 2010
Podiceps major
Rollandia rolland
Argentina
970 (890-1,060)
347 (286-396)
115 (107-131)
214 (202-226)
80 (67-95)
52 (43-62)
52 (48-57)
68 (62-80)
67 (60-71)
30 (15-45)
63 (48-77)
35 (31-40)
155 (119-193)
306 (256-338)
248 (208-314)
138 (121-167)
156 (107-195)
67 (54-81)
66 (52-82)
77 (68-87)
138 (119-159)
82 (57-101)
115 (100-126)
81 (75-90)
48 (36-58)
277 (231-312)
–
1.9 (1.7-2.2)
–
–
3.2 (2.7-3.9)
1.6 (1.1-2.2)
12 (10-13)
3.2 (2.7-3.9)
T. dominicus
T. dominicus
T. dominicus
Canary
Brazil
1,125 ± 54 (1,066-1,213)
349 ± 45 (294-407)
131 ± 17 (105-164)
227 ± 18 (205-250)
114 ± 8 (93-129)
97 ± 10 (75-109)
78 ± 7 (66-88)
78 ± 7 (67-90)
65 ± 6 (57-71)
39 ± 7 (32-50)
62 ± 5 (58-70)
38 ± 4 (30-43)
143 ± 17 (116-161)
273 ± 45 (205-328)
225 ± 26 (198-264)
186 ± 26 (150-205)
203 ± 34 (177-253)
76 ± 10 (61-89)
71 ± 10 (55-82)
111 ± 7 (102-116)
154 ± 14 (137-171)
121 ± 18 (102-137)
147 ± 20 (130-171)
72 ± 4 (70-78)
39 ± 2 (37-42)
329 ± 29 (286-372)
0.29 (0.25-0.33)
1.7 (1.4-2.3)
0.6 (0.5-0.6)
1.0 (0.9-1.3)
1.6 (1.4-1.7)
1.0 (0.8-1.1)
15 (14-16)
4.1 (3.5-4.9)
Venezuela
1,211-1,577
448-564
–
224-286
72-130
47-74
–
72-84
–
23-47
72-86
44-64
156-180
224-288
–
197-248
224-289
120-159
110-122
140-168
200-249
168-179
160-186
60-72
30-44
–
–
–
–
–
–
–
–
–
Venezuela
1,575
602
183
325
96-111
84-90
68-69
100
94
53
83
53
189
301
325
293
348
148
–
165
277
183
260
–
–
–
0.27
1.8
0.58
1.07
1.9
0.9
20
5.2
Guadalupe
1,250-1,580
400-520
–
210-270
–
64-79
70-95
70-90
70-106
–
57-78
41-58
–
235-286
235-264
–
–
95-135
100-136
140-220
160-225
144-214
180-230
70-84
48-55
432*
0.27*
1.8*
0.46*
0.77*
1.8*
1.3*
20*
5.5*
Cercariae from these 2 species have similar characteristics, such
as the presence of a long tail, S-shaped movement, a body with
a head collar bearing 19 spines, including 4 angle spines on each
side, a pharynx area with a yellow-brown interior, and cystogenous
gland-cells with rhabditiform contents covering the entire body
posterior to the pharynx. Cercariae of Petasiger sp. 1 differ from
Petasiger sp. 2 mainly in possessing a substantially smaller tail.
The cercariae originate from yellow-orange elongated rediae that
have a pair of locomotory appendages in the posterior region and
a collar with 4 lobes in the anterior region. Rediae of Petasiger sp.
1 are smaller than those of Petasiger sp. 2. Metacercariae of both
species were obtained from the oral cavity of experimentally infected
P. reticulata; the metacercariae are oval and possess a thin external
wall (Figure 2d-f ). Cysts of Petasiger sp. 1 are significantly larger
than those of Petasiger sp. 2. Although experimental attempts to
infect birds and mammalian hosts were performed, adult parasites
were not recovered. Measurements of developmental stages of both
Petasiger species, including the cercariae and rediae obtained from
mollusks and the metacercariae obtained experimentally from
P. reticulata, are presented in Table 2.
430
Pinto, H.A. et al.
Rev. Bras. Parasitol. Vet.
Figure 2. Cercariae and metacercariae of Petasiger spp. obtained from mollusks in Brazil. Petasiger sp. 1. (a, c, e). Petasiger sp. 2. (b, d, f ). Total
view of larvae (a, b). Detailed view of cercariae body (c, d). Total view of metacercariae obtained experimentally from Poecilia reticulata (e, f ).
Table 2. Morphometric data for larval stages of Petasiger spp. obtained from Biomphalaria spp. in Brazil and measurements presented by other
authors for similar larvae from the neotropics. Abbreviations: L = length, N = number, W = width.
Species
Reference
Host
Locality
Cercariae
Body
Petasiger sp. 1
Present study
Petasiger sp. 2
Present study
B. straminea
B. straminea,
B. tenagophila
Brazil
Brazil
L 197 ± 12 (177-218)
W
75 ± 7 (67-94)
Oral sucker
L
32 ± 2 (27-34)
W
31 ± 2 (27-34)
Spines
N
19
Ventral sucker L
33 ± 2 (29-36)
W
35 ± 1 (33-39)
Tail
L 486 ± 45 (410-594)
W 94 ± 11 (75-115)
TL/BL
4 (3-5)
Metacercariae L 109 ± 5 (102-122)
W
76 ± 4 (70-81)
Rediae
Body
L 985 ± 85 (887-1,195)
W 127 ± 16 (102-171)
Pharynx
L
45 ± 6 (33-53)
W
40 ± 6 (32-50)
Caecum
L 432 ± 77 (334-614)
W
41 ± 6 (33-50)
P. novemdecim P. caribbensis
Nasir et al.,
Nassi, 1980
1972
B. glabrata
B. glabrata
Venezuela
175 ± 13 (137-205)
68 ± 5 (55-75)
30 ± 1 (27-33)
28 ± 1 (26-31)
19
30 ± 2 (27-33)
31 ± 2 (27-34)
883 ± 94 (774-1,152)
135 ± 18 (102-184)
5 (4-6)
88 ± 4 (80-98)
53 ± 5 (46-68)
140-180
60-79
24-28
–
19-21
26-36
–
394-451
47-117
3
130-186
72-103
1,577 ± 238 (1,289-2,098)
202 ± 37 (120-258)
48 ± 11 (38-75)
50 ± 13 (38-83)
709 ± 204 (410-1,204)
72 ± 20 (34-102)
376-846
94-141
33-48
24-45
–
–
The specimens of P. novemdecim that were obtained from
T. dominicus in Brazil have smaller measurements for some body
structures than those reported for the species by other authors. These
differences may result from the use of uncompressed specimens
in this study. Despite the noted size differences, other differential
Guadalupe
Petasiger sp.
Ostrowski de
Núñez, 1982
B. glabrata
Petasiger sp.
Ostrowski de
Núñez et al., 1991
B. occidentalis
Venezuela
Argentina
100-200
183 ± 16 (158-199) 187 ± 23 (135-216)
60-110
62 ± 4 (58- 66)
66 ± 4 (63-72)
26-30
32 ± 3 (25-33)
31 ± 2 (29-32)
28-34
–
31 ± 2 (29-32)
19
19-20
19-20
26-32
34 ± 3 (33-42)
31 ± 2 (29-32)
30-36
–
31 ± 2 (29-32)
1,100-1,400 480 ± 47 (415-540) 780 ± 115 (540-990)
150-190
83 ± 13 (66-108) 104 ± 24 (72-135)
10-14
7
–
85
100 ± 6 (84-109)
78-88
53
59 ± 6 (48-67)
44-52
2,300
140
42
36
–
–
784-1,004
73-122
42-50
–
–
783-1,620
108-189
38-76
43-54
–
–
characteristics, such as the equivalent sizes of the anterior and
posterior portions of the parasite, the similar widths of the cirrus
pouch and the ventral sucker, the presence of vitellaria that are
confluent in the region below the ventral sucker, the tandem
positioning of the testes, and the arrangement and size of the collar
v. 22, n. 3, jul.-set. 2013
Petasiger in Brazil
spines, are in agreement with those reported for P. novemdecim
(LUTZ, 1928; NASIR et al., 1972; FALTÝNKOVÁ et al.,
2008). In addition, the specimens examined in this study have
larger dimensions than those reported for P. argentinensis. These
specimens can be further distinguished from P. argentinensis by
a number of morphological differences, such as the presence of
vitellaria that are confluent below the ventral sucker and the
positioning of the cirrus sac almost entirely anterior to the ventral
sucker (LUNASCHI; DRAGO, 2010). Tachybaptus dominicus is
the only natural host known for P. novemdecim, and this is the
first report of the occurrence of this parasite in Brazil.
Nasir et al. (1972) elucidated the life cycle of P. novemdecim
in Venezuela. These authors found cercariae in Biomphalaria
glabrata (Say, 1818) and obtained metacercariae and adults in
P. reticulata and T. dominicus, respectively. The morphology of
the Petasiger sp. 1 larvae identified in this study is similar to the
morphology of P. novemdecim larvae, as described by Nasir et al.
(1972). However, we cannot determine whether the 2 species are
conspecific because adult parasites were not obtained experimentally
in the present study. In fact, recovery of Petasiger species from
experimental definitive hosts has proved to be a difficult task,
and several other authors have been unsuccessful in recovering
parasites from different laboratory models (canaries, chicks, rats,
snakes, ducks, pigeons, cats, mice, and rats). Previous studies
have only been able to obtain these parasites from canaries, which
were often observed to have a low prevalence and intensity of
infection (BEAVER, 1939; ABDEL-MALEK, 1953; NASSI,
1980; OSTROWSKI DE NÚÑEZ, 1982; KOSTADINOVA;
CHIPEV, 1992; KOSTADINOVA, 1997). It is expected that
the advent of molecular approaches, such as those recently used
to elucidate the life cycle of Petasiger islandicus Kostadinova and
Skírnisson, 2007 (GEORGIEVA et al., 2012), will promote an
understanding of the association between larvae and adults of
different species of Petasiger, including South American species.
Another Latin American Petasiger species, Petasiger caribbensis
Nassi, 1980, was obtained experimentally from canaries in
Guadalupe, where B. glabrata was reported as the natural first
intermediate host (NASSI, 1980). Later, Faltýnková et al. (2008),
in the magnificent review of the genus Petasiger, based exclusively
on adult morphology considered P. caribbensis to be a junior
synonym of P. novemdecim. However, in addition to morphological
differences observed between adult parasites of these species,
including the disposition of the testes, which are always oblique
in P. caribbensis and in tandem in P. novemdecim, these species
display significant differences in the morphology of larval stages.
The cercariae, metacercariae, and rediae of P. caribbensis are
significantly larger than those described for P. novemdecim by
Nasir et al. (1972), and we believe that such differences are
sufficiently consistent for the species to be considered distinct.
The cercariae and metacercariae of Petasiger sp. 2 obtained from
B. straminea and B. tenagophila in Brazil are similar to the larvae
of P. caribbensis and other larvae found in B. glabrata in Venezuela
(OSTROWSKI DE NÚÑEZ, 1982) and in Biomphalaria
peregrina (d’Orbigny, 1835) and Biomphalaria occidentalis
Paraense, 1981 in Argentina (OSTROWSKI DE NÚÑEZ,
1981; OSTROWSKI DE NÚÑEZ et al., 1991).
431
It is likely that P. novemdecim and other South American
Petasiger species occur in places where both the intermediate
and definitive hosts are present. Given the wide distribution
of both T. dominicus and other podicipedids and mollusks of
the genus Biomphalaria in the neotropics, it is possible that the
diversity of Petasiger species in South America, specifically in
Brazil, is underestimated. Further studies are needed to increase
our understanding of the species diversity and life cycle of these
parasites. In addition, characteristics of larval stages, when available,
should be considered as important differential traits, as they can
contribute significantly to the understanding of taxonomic issues
related to these parasites.
Acknowledgements
We thank the National Council for the Development of
Science and Technology (CNPq) for financial support and doctoral
scholarship to HAP.
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