Resumen
Abstract
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
FIRST REPORT OF METACERCARIAE (DIGENEA) INFECTING ASTRONOTUS
OCELLATUS (PERCIFORMES: CICHLIDAE) FROM THE AMAZON REGION, BRAZIL
PRIMER REGISTRO DE METACERCARIAS (DIGENEA) INFECTANDO ASTRONOTUS
OCELLATUS (PERCIFORMES: CICHLIDAE) DE LA REGIÓN AMAZÓNICA, BRASIL
1 1 2
Marcos Tavares-Dias , Ligia Rigôr Neves & Berenice M.M. Fernandes
1 Laboratório de Aquicultura e Pesca, Embrapa Amapá. Rodovia Juscelino Kubitschek, km 5, 2600, 68903-419, Macapá, AP,
Brasil. marcostavares@cpafap.embrapa.br.
2 Laboratório de Helmintos Parasitos de Peixes, Instituto Oswaldo Cruz (FIOCRUZ). Av. Brasil 4365, 21045-900 Rio de
Janeiro, RJ. Brasil. berenice@ioc.fiocruz.br
Suggested citation: Tavares-Dias, M., Neves, L.R. & Fernandes, B.M.M. First report of metacercariae (Digenea) infecting
Astronotus ocellatus (Perciformes: Cichlidae) from the Amazon region, Brazil. Neotropical Helminthology, vol 5, nº 2, pp.
235-240.
Key-words: Brazil – Digenea - Freshwater fish – Metacercariae.
Este estudio tiene como objetivo el registro de la infestación por metacercarias de los géneros
Posthodiplostomum Dubois, 1936 (Diplostomidae) y Dubois Herpetodiplostomum, 1936
(Proterodiplostomidae) en las branquias del Astronotus ocellatus Agassiz, 1831 (Cichlidae) del lago Pracuúba, en
el Municipio de Pracuúba, Estado de Amapá, Brasil. De doscientos ejemplares de A. ocellatus examinados, 142
tenian las branquias infestadas por Herpetodiplostomum sp. (prevalencia = 70,3%) y por Posthodiplostomum sp.
(prevalencia = 59,4%). Sin embargo 97 hospederos fueron infestados por estas dos especies de metacercarias
(prevalencia = 48,0%). Del total de ejemplares de A. ocellatus examinados fueron extraidos 1.123 parasitos de
Herpetodiplostomum sp. y 463 parasitos de Posthodiplostomum sp., y la media de intensidad de la infestación fue
de 7,8 ± 3,9 y 11,6 ± 4,4, respectivamente. Este es el primer registro de Digenea en A. ocellatus.
Palabras claves: Brasil - Digenea - Metacercarias - Peces de agua dulce.
INTRODUCTION
During studies on the parasitic fauna of freshwater
fish from the Amapá State, Brazil, two hundred and
two specimens of Astronotus ocellatus Agassiz,
1831 (Perciformes: Cichlidae) were examined.
One hundred and forty-two specimens were
parasitized in the gills by metacercariae belonging
to the genera Herpetodiplostomum Dubois, 1936
and Posthodiplostomum Dubois, 1936.
This study aimed to report infection by metacercariae ofthe genera Posthodiplostomum Dubois, 1936
(Diplostomidae) and Herpetodiplostomum Dubois, 1936 (Proterodiplostomidae) in the gills of Oscar
Astronotus ocellatus Agassiz, 1831 (Cichlidae) from Lake Pracuúba, in the municipality of Pracuúba,
State of Amapá (eastern Amazonia), Brazil. Out of 202 A. ocellatus examined, 142 had gills infected by
metacercariae of Herpetodiplostomum sp. (prevalence= 70.3%) and Posthodiplostomum sp.
(prevalence= 59.4%). However, 97 hosts were infected by both metacercariae species (prevalence=
48.0%). A total of 1123 specimens of Herpetodiplostomum sp. and 463 specimens of
Posthodiplostomum sp. were collected and the mean intensity of infection was 7.8 ± 11.6 and 3.9 ± 4.4,
respectively. This is the first report of Digenea in A. ocellatus.
Neotrop. Helminthol., 5(2), 2011
2011 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
Versión Impresa: ISSN 2218-6425 / Versión Electrónica: ISSN 1995-1043
235
The A. ocellatus, commonly named as “acará-açu”
or Oscar, is a benthopelagic species, commonly
caught in lakes of “white, “clear” and “black”
waters from the Amazonia. In lakes, this fish
inhabits shallow water and with low flow water,
margins, aquatic vegetation or flooded forest. It
usually forms small groups. It is carnivorous,
feeding on fish, mollusks, crustaceans and aquatic
insects. This species is much appreciated by the
riverine population and it is also sold in markets in
the Amazonian region (Soares et al., 2007). In
Brazil, in 2007, the caught of A. ocellatus was of
1825.5 t (Ibama, 2007), and this species is already
being bred in captivity. The present work studied
the infection by metacercariae of the digeneans
Posthodiplostomum sp. and Herpetodiplostomum
in the gills of A. ocellatus from the Lake Pracuúba,
in State of Amapá, Brazil.
MATERIAL AND METHODS
Between May 2010 and April 2011, 202 specimens
of Oscar A. ocellatus from the Lake Pracuúba
(01º43'47''N, 50º47'45”W), in the municipality of
Pracuúba, State of Amapá, Brazil were examined.
The fish measured 23.4 ± 3.0 cm in total length and
had 367.7 ± 134.1 g of body weight. Specimens
were necropsied and their organs were analyzed.
Only the gills were found being parasitized by
helminths. The gills were placed in vials and fixed
in formalin 5%; the metacercariae collected were
counted and stored in cold AFA (alcohol-
formaldehyde-acetic acid), without compression,
for identification. Specimens were stained with
Langeron's alcoholic acid carmine, dehydrated in
an ethyl alcohol series, cleared in beechwood
creosote and mounted in Canada balsam as
permanent slides. Light micrographs were made
using a Nikon Eclipse 800 camera. Terms
ecological were according to Bush et al. (1997).
The specimens studied were deposited in the
Helminthological Collection of the “Instituto
O s w a l d o C r u z ” ( C H I O C ) , B r a z i l .
Posthodiplostomum sp. (CHIOC: 37530) and
Herpetodiplostomum sp. (CHIOC: 37531).
RESULTS AND DISCUSSION
Metacercariae specimens of Posthodiplostomum
Dubois, 1936 (Fig. 1) and of Herpetodiplostomum
Dubois, 1938 (Fig. 2) were collected from the gills
of A. ocellatus from Lake Pracuúba, eastern
Amazona.
Notes concerning the infection by these digeneans
are provided. This is the first report of both Digenea
metacercariae for A. ocellatus. Members of the
family Diplostomidae have wide geographic
distribution, and most of them are known for
infecting fish species from Europe, Asia and North
America (Kent & Fournie, 2007; Yamada et al.,
2008); just a small number of species is known for
infecting Neotropical fish (Scholz et al., 1995;
Yamada et al., 2008; Takemoto et al., 2009). Scholz
et al. (1995) noticed that from a geographical point
of view, the fauna of metacercariae is diversified.
It is composed of cosmopolitan species, species
widely distributed in North and South America and
of trematodes species whose distribution is
restricted to Mexico and Central America.
Several species of diplostomids metacercariae
have been reported in Brazilian freshwater fishes,
but Austrodiplostomum compactum Lutz, 1928
(Diplostomidae) has been the most frequent.
Species of diplostomids have been responsible for
“wormy cataract”, also called diplostomiasis. Fish
heavily infected by metacercariae in the eyes have
loss of vision and reduced growth or deformation
of the vertebral column, brain tumor, cellular
necrosis which eventually leads to death (Eiras et
al., 2010; Zica et al., 2010).
Digeneans are parasites of the intestine, and has
been assumed that this is their plesiomorphic site of
infection. However, numerous families of
digeneans have adopted new sites of infection in
hosts (Cribb et al., 2002). Historically, infection of
fish gills by metacercariae of Diplostomidae
species has been uncommon. It can cause moderate
to severe hyperplasia of epithelial gill of the
primary gill lamellae, forming cysts surrounded
with multiple cellular reactions, including
mononuclear inflammatory cells (Eissa et al.,
2011). In addition, a massive and widespread
infection by these metacercariae, particularly in
little fish can cause intensive inflammatory
response and mortality (Mitcheli et al., 1982;
Paperna & Dzikowski, 2006).
Adult members of the family Diplostomidae
Poirier, 1886 has been reported parasitizing birds
and mammals. Adult specimens of the genus
Posthodiplostomum Dubois, 1936 have been
reported in almost all countries of South America
parasitizing birds. Only metacercariae
Metacercariae (Digenea) infecting Astronotus ocellatus Tavares-Dias et al.
236
Posthodiplostomum macrocotyle Dubois, 1937
(Diplostomidae) has been reported in fish from
Brazil; it was found in the eyes, buccal cavity,
stomach and gonads of Geophagus brasiliensis
Quoy & Gairmad (Cichlidae) from Guandu River,
State of Rio de Janeiro (Azevedo et al., 2006) and
in the stomach of Trachelyopterus striatulus
Steindachner, 1877 (Auchenipteridae), also from
Guandu River (Mesquita et al., 2011).
The family Proterodiplostomidae Dubois, 1936 is
represented by a genus reported parasitizing
exclusively reptiles. Adult members of these
genera have been found in Neotropical
crocodilians and occasionally, in snakes. Several
species belonging to eleven genera of
Proterodiplostomidae have been described in
South American reptiles. Metacercariae belonging
to the genus Herpetodiplostomum Dubois, 1938
have been reported in South American fishes from
Argentina by Szidat (1969), who erected the new
species Herpetodiplostomum gymnoti for
metacercariae recovered from skin, particularly of
the head of Gymnotus carapo Linnaeus, 1758
(Gymnotidae). In Brazil, metacercariae of H.
gymnoti was reported in the gonads of
Ih e ri ng ich th ys lab ros us Lütken, 1874
(Pimelodidae) by Moreira et al. (2005) and
Herpetodiplostomum sp. (metacercariae) has been
find in the eyes of Astyanax altiparanae Garutti &
Britski, 2000 (Characidae) by Lizama et al. (2008);
of Leporinus elongatus Valenciennes, 1850,
Leporinus friderici Bloch, 1794, Leporinus
obtusidens Valenciennes, 1837, Leporinus
lacustris Amaral Campos, 1945 (Anostomidae), G.
carapo, I. labrosus and A. altiparanae by
Takemoto et al. (2009), and in the swim bladder of
L. lacustris (Pavanelli, 2006); all records above
are from upper Paraná River (South of Brazil).
Isaac et al. (2004) reported the presence of
metacercariae of Herpetodiplostomum sp. in the
gonads and mesentery of Gymnotus spp. from Baía
River, State of Mato Grosso do Sul (Midwest
Brazil) and Abdallah et al. (2006) find progenetic
metacercariae of Herpetodiplostomum caimancola
Dollfus, 1935 in the intestine of Hoplosternum
littorale Hancock, 1828 (Callichthyidae) from
Guandu River, State of Rio de Janeiro (Southeast
B r az i l) . T hi s is t he f ir st r ep o rt o f
Herpetodiplostomum sp. and Posthodiplostomum
sp. (metacercariae) regarding the Brazil, and
occurred in A. ocellatus from the eastern Amazonia
(North of Brazil).
Parasitological studies need to be encouraged
because they may demonstrate the intricate
relationships among organisms in systems and the
need for biodiversity conservation (Brasil-Sato &
Santos, 2005; Takemoto et al., 2009). The
prevalence of Herpetodiplostomum sp. was 70.3%
and the mean intensity 7.8 ± 11.6; while for
Posthodiplostomum sp. the prevalence was 59.4%
and the mean intensity 3.9 ± 4.4. For
Posthodiplostomum sp. the lowest prevalence was
o b s e r v e d i n S e p t e m b e r , a n d f o r
Herpetodiplostomum sp. it was in April and
September (Table 1), probably because the
emergence of cercariae can be affected by increase
of the temperature. The epidemiology of digeneans
metacercariae can also reflect differences due to
exposure time to cercariae in the environment.
Azevedo et al. (2006) described mean intensity of
2.4 ± 1.23 to metacercariae of P. macrocotyle in
88.0% from G. brasiliensis examined. For the same
host and locality, Carvalho et al. (2010) reported a
prevalence of 74.5% and mean intensity of 7.3 ±
7.8 in the eyes, swim bladder and intestine. Levels
of infection by digeneans can vary according to the
environment or the species of host, and they can be
related to size, longevity and particularly the
feeding habits of the host. Moreover, fish with
longer lifespan may have more exposure time to
these parasites, favoring cumulative processes in
the host (Cribb et al., 2002; Takemoto et al., 2009;
Carvalho et al., 2010). However, we found not
correlation between the size of A. ocellatus and the
intensity of digeneans metacercariae. Therefore,
for A. ocellatus from the Lake Pracuúba (State of
Amapá, Brazil), the prevalence and intensity of
Herpetodiplostomum sp. and Posthodiplostomum
sp. metacercariae indicates that the abundance of
bird hosts and the presence of favorable conditions
for the first intermediate host, being a snail the most
common, are the causes of the infections on the
gills of this host fish. In addition, the definitive host
in the lake is a fish-eating bird. Furthermore, these
results corroborate that the life-habit of the fish
have a great importance in its levels of infection by
digenean species.
ACKNOWLEDGEMENTS
The authors thank Conselho Nacional de Pesquisa
e Desenvolvimento Tecnológico (CNPq) for
supporting a fellowship to Tavares-Dias, M. (Grant
# 300472/2008-0) and a scholarship to Neves, L.R.
Neotrop. Helminthol., 5(2), 2011
237
Figures 1-2. Metacercarie of Posthodiplostomum sp. (1) and Herpetodiplostomum sp. (2) in the gills from Astronotus
ocellatus collected in Lake Pracuúba, State of Amapá, Brazil. Bar = 100 µm.
Table 1. Levels of infection by Digenea metacercariae species in the gills of Astronotus ocellatus from the Lake
Pracuúba, in the State of Amapá, Brazil. Examined fish (EF), parasitized fish (PF), prevalence (P), mean intensity
(MI).
Metacercariae (Digenea) infecting Astronotus ocellatus Tavares-Dias et al.
238
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Correspondence to author /Autor para
correspondencia:
Marcos Tavares-Dias.
Embrapa Amapá, Rodovia Juscelino Kubitschek,
km 5, N° 2600, 68903-419, Macapá, AP, Brasil.
E-mail/ correo electrónico:
marcostavares@cpafap.embrapa.br
Received October 05, 2011.
Accepted October 31, 2011.
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