ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2017, 11(1), jan-jun: 9-16.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
DIPLOSTOMUM (AUSTRODIPLOSTOMUM) COMPACTUM (LUTZ, 1928)
(PLATYHELMINTHES, DIGENEA) FREE METACERCARIAE IN THE EYES OF FISHES FROM
THE FLOODPLAIN LAKES TO THE LOWER SOLIMÕES RIVER, BRAZIL
DIPLOSTOMUM (AUSTRODIPLOSTOMUM) COMPACTUM (LUTZ, 1928)
(PLATYHELMINTHES, DIGENEA) METACERCARIA LIBRE EN LOS OJOS DE LOS PECES DE
LOS LAGOS DE INUNDACIONES AL RIO INFERIOR DE SOLIMÕES, BRASIL
Laboratório de Parasitologia de Peixes/ Coordenação de Biodiversidade/ Instituto Nacional de Pesquisas da
Amazônia – INPA.
Corresponding author* atjsouza15@gmail.com
Amanda Karen Silva de Souza*; Daniel Brito Porto & José Celso de Oliveira Malta
ABSTRACT
Keyword: Amazon – Diplostomidae – freshwater – parasites of fishes – Trematoda
Two hundred and eighty-nine fish of 24 species and four orders were captured in Catalão, Preto and Poraquê lakes in
the dry season. Thirteen species were parasitized by free metacercariae of Diplostomum (Austrodiplostomum)
compactum (Lutz, 1928) in the eyes: Pygocentrus nattereri Kner, 1858, Serrassalmus elongatus Kner, 1858
(Serrasalmidae); Acestrorhynchus falcirostris (Cuvier, 1819) (Characidae); Satanoperca jurupari (Heckel, 1840);
Geophagus surinamensis (Bloch, 1791), Crenicichla johanna Heckel, 1840, Mesonalta festivus (Heckel, 1840)
(Cichlidae); Plagioscion squamosissimus Heckel, 1840 (Sciaenidae); Loricariichthys acutus Valenciennes, 1840,
Pterygoplichthys pardalis (Castelnau, 1855) (Loricariidae); Pimelodus bloch Valenciennes, 1840 (Pimelodidae)
and Pellona castellneana Valenciennes, 1847 (Pristigasteridae). A total of 1065 free metacercariae of D. (A.)
compactum were collected. Plagioscion squamosissimus was the species with the greatest abundance of
metacercariae with 640 individuals. Species of benthic fish were more parasitized than pelagic fish.
Neotropical Helminthology
9
Volume11,Number1(ene-jun2017)
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
Auspiciado por:
INTRODUCTION
10
RESUMEN
Palabras clave: agua dulce – Amazonas – Diplostomidae – parásitos de peces – Trematoda
Doscientos ochenta y nueve peces de 24 especies y cuatro órdenes fueron capturados en los lagos Catalão, Preto y
Poraquê en la estación seca. Trece especies fueron parasitadas por metacercarias libres de Diplostomum
(Austrodiplostomum) compactum (Lutz, 1928) en los ojos: Pygocentrus nattereri Kner, 1858, Serrassalmus
elongatus Kner, 1858 (Serrasalmidae); Acestrorhynchus falcirostris (Cuvier, 1819) (Characidae); Satanoperca
jurupari (Heckel, 1840); Geophagus surinamensis (Bloch, 1791), Crenicichla johanna Heckel, 1840, Mesonalta
festivus (Heckel, 1840) (Cichlidae); Plagioscion squamosissimus Heckel, 1840 (Sciaenidae); Loricariichthys
acutus Valenciennes, 1840, Pterygoplichthys pardalis (Castelnau, 1855) (Loricariidae); Pimelodus bloch
Valenciennes, 1840 (Pimelodidae) y Pellona castellneana Valenciennes, 1847 (Pristigasteridae). Se recogieron un
total de 1065 metacercarias libres de D. (A.) compactum. Plagioscion squamosissimus fue la especie con mayor
abundancia de metacercarias con 640 individuos. Las especies de peces bentónicos fueron más parasitadas que las
pelágicas.
The fishes were collected in three lakes: Catalão
(3°10'04”S; 59°54'45”W), Preto (3°21'17''S;
1°37'28,6"W and Poraquê (3°53'54,8"S;
61°40'18,4"W) during the month of November of
2015 in dry season. Mesh gill nets were used in 25
and 35 mm distance between us opposite arranged
randomly on the lake, with fish removal every two
hours for 48 h. The fishes were measured (standard
length in cm), weighed in g, identified and
preserved in 85% ethanol. Later were transported
to the Fish Parasitology Laboratory where they
were necropsied (Paraguassú & Luque, 2007).
To collect the metacercariae eyes were removed
and was made the dissection of the ocular globe in
the Petri dish (Pavanelli et al., 2012). Helminthes
were collected and preserved in 70% ethanol. The
metacercariae were stained in carmine in the
reverse process by Amato et al. (1991).
Identification of A. compactum metacercariae was
based on the morphological studies of Kohn et al.
(1995) and Zica et al. (2009).
The drawings were made using a camera lucida
attached to a light microscope. The parasitic rates
were calculated according to Margolis et al. (1982)
and Bush et al. (1997). Metacercariae of A.
Austrodiplostomum compactum (Lutz, 1928) is a
digenetic trematode of the order Strigeoidea whose
metacercariae occur in the eyes of a wide variety of
fish species (Kohn et al., 1995; Martins et al., 1999,
2002; Brasil-Sato& Pavanelli, 2004; Brasil-Sato &
Santon, 2005; Yamada et al., 2008; Zica et al.,
2009; 2010; Santos, 2011). The metacercariae of
these digeneans can infect the vitreous humour
(Amato et al., 2001) and, more rarely, the brains of
the intermediate fish hosts (Nuñez, 1982; Amato et
al., 2001).
Interest in this trematode group was stimulated in
recent years because the larvae of this family can
infect humans and, when present in sufficient
numbers, can cause you death (Thatcher 2006).
This group is closely related to fish because they
are the second intermediate hosts (Santos et al.,
2001, 2012). In recent years, it has been reported
several fish species in Brazil as host of this species.
Because of the great diversity of the Amazon fish, it
is evident that there is a huge amount of hosts
(Malta, 1981). The aim of the present study was to
investigate the occurrence of infection by A.
compactum metacercariae in the eyes of fish from
the floodplain lakes to the lower Solimões river,
Brazil.
Silva de Souza et al.
Neotropical Helminthology, 2017, 11(1), jan-jun
MATERIAL AND METHODS
compactum were deposited in the Coleção Não
Insecta do INPA, Manaus, Amazonas State, Brazil.
Two hundred and eighty-nine fish of 24 species and
4 orders were collected. Characiformes order:
P ro c h i lodu s n i g r i c ans Agassiz, 1 829
(Curimatidae); Serrassalmus elongatus Kner, 1858
(Serrasalmidae); Potamorhyna altamazonica
Cope, 1878 (Curimatidae); Potamorhyna
pristigaster (Steindachner, 1876) (Curimatidae);
Hoplias malabaricus (Bloch 1794) (Erytrinidae);
Triporteus albus Cope, 1872 (Characidae);
Pygocentrus nattereri Kner, 1858 (Serrasalmidae)
e Acestrorhynchus falcirostris (Cuvier, 1819)
(Characidae), (Table 1).
Fishes of Perciformes order: Crenicichla johanna
Heckel, 1840 (Cichlidae); Mesonauta festivus
(Heckel, 1840) (Cichlidae); Satanoperca jurupari
(Heckel, 1840) (Cichlidae); Geophagus
surinamensis (Bloch, 1791) (Cichlidae) and
Plagioscion squamosissimus Heckel, 1840
(Sciaenidae). Fishes of Clupeiformes order:
Pellona castelnaeana Valenciennes, 1847
(Pristigasteridae); P. flavipinnis (Valenciennes,
1837) (Pristigasteridae), Ilisha amazonica
(Miranda Ribeiro, 1920) (Pristigasteridae) and
Pristigaster cayana Cuvier, 1829 (Pristigasteridae)
(Table 1).
Fishes of Siluriformes order: Pimelodus bloch
Va l e n c i e n n e s , 1 8 4 0 ( P i m e l o d i d a e ) ;
Loricariichthys acutus Valenciennes, 1840
(Loricariidae); Ageneiosus inermis (Linnaeus,
1766) (Ageneiosidae), Hypophtalmus edentatus
Spix & Agassiz, 1829 (Hypophthalmidae),
Pterygoplichthys pardalis (Castelnau, 1855)
(Loricariidae), Calophysus macropterus
(Lichtenstein, 1819) (Pimelodidae) and
Hoplosternum litoralle (Hancock, 1828)
(Callichthyidae).
Twenty four species of fish were collected and
thirteen were parasitized by free metacercariae of
D. (A.) compactum (INPA – 688) in the eyes: P.
nattereri; A. falcirostris; S. jurupari; G.
surinamensis; P. squamosissimus; L. acutus; S.
elongatus; P. bloch; P. castelnaeana P. pardalis; C.
RESULTS
11
Neotropical Helminthology, 2017, 11(1), jan-jun
johanna; P. castelnaeana e M. festivus.
Loricariichthys acutus e P. pardalis were also
collected in the lakes Poraquê and Preto.
The length and the average weight of infected fish
by metacercariae were: P. nattereri 19,8±1,5 and
280±50,8, A. falcirostris 32,6 ± 2,3 and 346,3 ±
74,8; S. jurupari 14,7 ± 0,8 andand100,6 ± 12,5, G.
surinamensis13,2 ± 1,5 and 64,6 ± 27,5, P.
squamosissimus 21,9 ± 2,6 e 157,4 ± 46,4, L.
acutus 21,5 ± 1,1 and 51,3 ± 9,6. The fishes P.
pardalis 22 e 130, P. bloch, 14 e 98, P. castelnaeana
25 e 306, M. festivus 10 e 22 and C. johanna 19 e
265 were captured only one fish of each species.
1065 metacercariae parasitizing 12 species of fish
from Catalão Lake were collected. Plagioscion
squamosissimus was the species with the greatest
abundance 640 and average abundance 27.8. The
largest number of metacercariae to the eye also
occurred in P. squamosissimus with 116
specimens, followed L. acutus and S. jurupari
(Figure 2). C. johanna exception that although a
single specimen collected had a significant amount
of parasites in their eyes (56). The parasitological
indices and trophic habitat of the fish caught are
presented in Table 1.
The metacercariae found was identified as
Diplostomum (A.) compactum. This is the first case
record of metacercariae of A. compactum
parasitizing the C. johanna eyes, P. bloch, L.
acutus, S. jurupari, G. surinamensis, P.
castelnaeana and P. nattereri in the Amazon.
Fisheries occurred during the dry season, and the
depth of the lakes was minimal, and the fish had a
very small space to live. The species of benthic fish
were more parasitized by A. compactum than
pelagic species. Despite having a prevalence of
100% most species with the exception of L. acutus
showed a low average intensity.
The main characteristics of A. compactum
metacercariae were: foliaceous body, slightly
concave in the ventral face; small conical segment
in the posterior region. Small subterminal oral
sucker; two lateral pseudosuckers in the anterior
region. Acetabulum absent. Oval pharynx; short
oesophagus; intestinal caeca ending near the
posterior region. Morphometric data of A.
compactum metacercariae are summarized in table 1.
Diplostomum in the eyes of shes
Silva de Souza et al.
Neotropical Helminthology, 2017, 11(1), jan-jun
Table 1. Fish species and number of collected metacercariae of thirteen species of sh captured in the lakes, Catalão,
Preto and Poraquê in the Brazilian Amazon.
Species of sh
Individuals
number Length (cm) Weight (g) Metacercariae
P. nattereri
12
19,8 ± 1,5
280 ± 50,8,
11
A. falcirostris
3
32,6 ± 2,3
346,3 ± 74,8
23
S. jurupari
26
14,7 ± 0,8 100,6 ± 12,5
111
G. surinamensis
10
13,2 ± 1,5 64,6 ± 27,5 44
P. squamosissimus
26
21,9 ± 2,6 157, 4 ± 46,4
640
L. acutus
1
21,5 ± 1,1 51,3 ± 9,6 136
P. pardalis
1
22 130 37
P. bloch
1
14 98 1
P. castelnaeana
1
25 306 1
M. festivus
1
10
22
1
C. johanna 1 19 265 59
S. elongatus 1 17 112 1
Table 2. Parasitological indexes of Diplostomum (Austrodiplostomum) compactum parasites of thirteen species of
sh captured in the lakes, Catalão, Preto and Poraquê in the Brazilian Amazon.
Host P% IM AV HA FH Nm
Acestrorhynchus falcirostris
100
7,6±3,2
4 -
10
Pel
P
23
Crenicichla johanna
α
100
59
-
Ben-pel
C
59
Geophagus surinamensis
100
4,4±3,7 1 -
10
Ben-pel
O
44
Loricariichthys acutus1
α
100
36,6±20,2 16 -
64
Ben D
112
Loricariichthys acutus2
80
16,3±13,6 2 -
47
Ben D
24
Mesonauta festivus
α
100
1 2 Ben-pel
O
1
Pygocentrus nattereri
100
2,3±1 1 -
4 Pel P
11
Pimelodus bloch α
100
1 - Ben-pel
O
1
Plagioscion squamosissimus
100
27,8±29,1 1 -
116
Ben-pel
C
640
Pellona castelnaeana α
100
1 - Pel P
1
Pterygoplichthys pardalis
29,4
1,4±0,8 1 –
4
Ben D
37
Satanoperca jurupari 100 4,2±3,6 1 - 15 Ben-pel O 111
Serrassalmus elongatus α100 1 - Pel O 1
P - prevalence; IM - mean intensity; AV - amplitude variation; HA - Habitat; FH - food habit; Pel - Pelagic; Ben-pel -
Benthopelagic; P- piscivore; C - carnivore; O – omnivorous; D – detritivore; Nm - Number of metacercariae. α - First
record. 1 – catalão, 2 – poraquê.
DISCUSSION species). The fishes of the Cichlidae family (10
species) and Loricariidae (eight species) showed
the most parasitized species (Ramos et al., 2013).
Diplostomum (Austrodiplostomum) compactum
was cited parasitizing the eyes of P.
squamosissimus (Kohn et al., 1995), Geophagus
brasiliensis Quoy & Gaimard, 1824 (Novaes et al.,
In Brazil, metacercarial D. (A.) compactum are
cited for 40 species of fish (Ramos et al., 2013;
Pinto et al., 2014). Most species of fish parasitized
belong to the Perciformes order (12 species),
Siluriformes (13 species) and Characiformes (nine
12
13
2006; Carvalho et al., 2012), Hypostomus regani
Ihering, 1905 (Zica et al., 2009), H. ancistroides
Ihering, 1911, H. hermanni Ihering, 1905, H.
iheringii Regan, 1908, H. margaritifer Regan,
1908, H. strigaticeps Regan, 1908, Hypostomus sp.
e Megalancistrus parananus Peters, 1881 (Zica et
al., 2011). The eyes of Hoplias malabaricus Bloch,
1794, Geophagus surinamensis Bloch, 1791
(Santos et al., 2012); Cichla monoculus Spix &
Agassiz, 1831, Crenicichla britskii Kullander,
1982, Cichlasoma paranaense Kullander, 1983
and Satanoperca pappaterra Heckel, 1840
(Machado et al., 2005).
The eyes of Geophagus proximus Castelnau, 1855
(Zica et al., 2010); Serrasalmus maculatus Kner,
1858; H. regani; Schizodon borellii Boulenger,
1900; Auchenipterus osteomystax Miranda-
Ribeiro, 1918 (Yamada et al., 2008). The kidneys,
body cavity, peritoneum around the viscera and
brain of Loricariichthys anus Valenciennes, 1835
(Amato et al., 2001).
Twenty-two species of fish captured in the Santa
Bárbara River (municipality of Buritama, São
Paulo State. Five species were parasitized by A.
compactum: P. squamosissimus; S. nasutus; S.
papaterra; H. malabaricus and M. maculatus.
Plagioscion. squamosissimus was the species with
the highest prevalence (90%) followed by S.
papaterra (60%) (Paes et al., 2010).
This first case record of D. (A.) compactum in a fish
in the Amazon were in 355 P. nattereri captured in
six floodplain lakes of Solimões River. Of fishes
85% were female and only three D. (A.)
compactum were collected in the muscles of three
male (15%) during dry season. The prevalence was
0.845%; intensity 3; average intensity 1.0 ± 0.45;
average abundance 0.01 and the range of variation
1 (Morais et al., 2011).
The second case record of D. (A.) compactum in
fish in the Amazon were in Acestrorhynchus
falcirostris (Cuvier, 1819) captured in six
floodplain lakes of Solimões River e one from
Purus River. Seventy-nine fishes were examined,
34 were infected and 180 D. (A.) compactum were
collected. The prevalence was 43.04; intensity
ranged from 1 to 25; average intensity 5.29 ± 4.9
and mean abundance 2.26 ± 4.14. The free
metacercariae were collected in the eyes, visceral
and gill cavities and the intestine. The gill and
visceral cavities and intestines are new sites of
infection (Dumbo, 2014).
This paper is the third case record of D. (A.)
compactum parasitizing fish in the Brazilian
Amazon. Thirteen species of fishes occurred as a
host of D. (A.) compactum. For P. nattereri
parasitological indices were much higher than
those found by Morais et al. (2011) and the
metacercariae were collected only in the eyes, a
new place of infestation by D. (A.) compactum in P.
nattereri. For A. falcirostris parasitological indices
too were much higher than found by Dumbo
(2014), but the free metacercariae were founded
only in the eyes.
In populations of H. malabaricus, S. pappaterra, P.
squamosissimus, C. britskii and C. monoculus from
the oodplain of the upper Parana´ River, the
metacercariae of D.(A.) compactum tend to present
aggregated distribution, with a low degree of
aggregation (Machado et al., 2005). In the
aggregated distribution, few individuals of the host
population shelter many parasites, while many are
not parasitized (Ludwig & Reynolds, 1988).
In P. squamosissimus from the oodplain of the
upper Parana´ River, the majority of the specimens
were found parasitized by D. (A.) compactum,
although few sheltered many metacercariae and the
remaining a lesser number (Machado et al., 2005;
Lacerda et al., 2012). The most severe effects
caused by elevated intensities of infection are
conned to few individuals and have little effects
on the population as a whole (Crofton, 1971).
In this paper D. (A.) compactum parasite the eyes of
thirteen species of fish showing the natural
susceptibility of fish to this parasite (Martins et al.,
2002). The high prevalence rates and the average
intensity are associated with environmental quality
in the collection period, the dry season, which
limits the living space and promotes contact
between intermediate and definitive hosts, thus
favoring the life cycle of D. (A.) compactum is
complete (Mesquita et al., 2011).
Probably A. compactum enjoy the period of less
space in the aquatic environment to disperse the
largest possible number of hosts in the lake. This
can be seen because not all fish collected were
Neotropical Helminthology, 2017, 11(1), jan-jun Diplostomum in the eyes of shes
14
infected, because of their different eating habits
and habitat areas. The species of benthic and
pelagic fish were the ones that showed the highest
abundances of A. compactum. The highest
parasitism occurred in P. squamosissimus and L.
acutus.
Silva de Souza et al.
Neotropical Helminthology, 2017, 11(1), jan-jun
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