Neotrop. Helminthol., 8(2), 2014
2014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
MONOGENOIDEA AND DIGENEA PARASITES OF THUNNUS ATLANTICUS (PERCIFORMES,
SCOMBRIDAE) FROM RIO DE JANEIRO COAST, BRAZIL
MONOGENOIDEA Y DIGENEA PARÁSITOS DE THUNNUS ATLANTICUS
(PERCIFORMES, SCOMBRIDAE) DE LA COSTA DE RIO DE JANEIRO, BRASIL
1 1,2
Marcia Cristina Nascimento Justo & Anna Kohn
Abstract
Keywords: Digenea - Fish parasites - Monogenoidea – Scombridae.
Suggested citation: Justo, MCN & Kohn, A. 2014. Monogenoidea and Digenea parasites of Thunnus atlanticus (Perciformes,
Scombridae) from Rio de Janeiro coast, Brazil. Neotropical Helminthology, vol. 8, n°2, jul-dec, pp. 339-348.
1,2Laboratório de Helmintos Parasitos de Peixes, Instituto Oswaldo Cruz, Fiocruz
Av. Brasil, 4365 Manguinhos, Rio de Janeiro, Brazil.
2Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq
Thunnus atlanticus is of great commercial importance in Brazil, but infections caused by helminth
parasites can reduce its commercial value. In this paper, 15 species of Digenea and three of
Monogenoidea were recovered from 61 specimens of T. atlanticus collected from the coastal zone
of the State of Rio de Janeiro. Species of the family Didymozoidae were the dominant species,
with highest prevalence and abundance values. The parasites showed the typical aggregated
distribution pattern, except for Nasicola brasiliensis, which had an aleatory distribution pattern.
Prevalence and abundance of Didymosulcus philobranchiarca, Didymocystis lamotheargumedoi
and Didymosulcus wedli and prevalence of Koellikerioides internogastricus were positively
correlated with the total length of the host. The abundance of Coeliotrema thynni was negatively
correlated with total length of the host. New hosts records resulted for four Digenea:
Didymosulcus orbitalis, Didymosulcus wedli, Rhipidocotyle pentagonum and Lecithochirium
microstomum, and one Monogenoidea: Nasicola brasiliensis.
Resumen
Palabras clave: Digenea - Monogenoidea - Parásitos de peces - Scombridae
Thunnus atlanticus es de gran importancia comercial en Brasil, pero las infecciones causadas por
helmintos parásitos puede reducir su valor comercial. En este trabajo, 15 especies de Digenea y
tres de Monogenoidea fueron recuperados de 61 ejemplares de T. atlanticus recogidos de la zona
costera del Estado de Río de Janeiro. Las especies de la familia Didymozoidae eran las especies
dominantes, con mayores valores de prevalencia y de abundancia. Los parásitos mostraron el
patrón de distribución agregado típico, excepto para Nasicola brasiliensis, que tenía un patrón de
distribución aleatoria. La prevalencia y abundancia de Didymosulcus philobranchiarca,
Didymocystis lamotheargumedoi y Didymosulcus wedli y la prevalencia de Koellikerioides
internogastricus se correlacionaron positivamente con la longitud total del hospedador. La
abundancia de Coeliotrema thynni se correlacionó negativamente con la longitud total del
hospedador. Nuevos registros de hospedadores resultaron para cuatro especies de Digenea:
Didymosulcus orbitalis, Didymosulcus wedli, Rhipidocotyle pentagonum y Lecithochirium
microstomum, y uno Monogenoidea: Nasicola brasiliensis.
339
Justo & Kohn
Monogenoidea and Digenea parasites of Thunnus
Studies on helminth parasites of Brazilian
scombrids had been published by Alves et al.
(2003), Alves & Luque (2006), Cardenas et al.
(2009), Dias et al. (2011), Fernandes et al.
(2002), Hsu (1968), Justo & Kohn (2005, 2009,
2010, 2011, 2012a, 2012b), Justo et al. (2008,
2009, 2013), Kohn & Justo (2006, 2008), Kohn
et al. (2001, 2003, 2004), Mogrovejo et al.
(2004), Mogrovejo & Santos (2002), Moravec et
al. (1999), Rego & Eiras (1987), Rego & Santos
(1983) and Pamplona-Basilio et al. (2001).
Tunas (Thunnini) are unique among bony fishes
in having counter-current heat exchange
systems that allow them to retain metabolic heat,
maintaining a warmer internal temperature than
the surrounding water (Collette & Nauem,
1983). In addition to their endothermic
adaptations, they have a suite of morphological
characters appear to be adaptations for efficient,
and relativity rapid, sustained swimming
(Altringham & Block, 1997). Thunnus
atlanticus (Lesson, 1831) is the only tuna
scombrid species whose distribution limits are in
the western Atlantic. It is reported from the
North of the USA to the Southeast of Brazil,
where is known as “albacorinha”. It is a highly
migratory species, mainly found in coastal
o
waters, in temperatures above 20 C.
“Albacorinhas” form schools with other species
of tuna, spawn near the coast and feed on small
fish, squids, crustaceans, and plankton (Collette
& Nauen, 1983). T. atlanticus is commercially
very important in Brazil, where high rates of
infection caused by helminth parasites often
reduce the commercial value of the fish.
According to Mladineo et al. (2009), the long-
distance migrations typical of tuna fish and their
consequent exposure to a wide range of ambient
water temperatures facilitate infections with
several parasitic groups, mainly by members of
Didymozoidae Monticelli, 1888, which display
remarkable diversity and high levels of
prevalence and abundance.
Sixty one specimens of T. atlanticus (45 - 82 cm
total body length; 1.3 - 6.0 kg) were surveyed for
helminth parasites. Fish were obtained from
local fishermen, from the coastal zone of the
State of Rio de Janeiro, Cabo Frio, Brazil
(22º52'46”S, 42º01'07" W). The parasites were
fixed with or without compression in AFA
(alcohol 93%, formalin 5% and acetic acid 2%),
stained in alcoholic-acid carmine, dehydrated in
alcohol series, cleared in beachwood creosote
and mounted in Canada balsam. Parasitism
indexes proposed by Bush et al., (1997) were
used. The quotient between variance and mean
parasite abundance (index of dispersion) was
used to determine distribution patterns and was
tested by the d statistical index (Ludwig &
Reynolds, 1988).
The Spearman's rank correlation coefficient (r)
s
was used to determine possible host length
correlations with parasitism abundance.
Pearson's coefficient of correlation (r) was used
to determine possible correlations between total
length and prevalence, with angular
transformation of prevalence values. The effect
of host sex on abundance and prevalence of
parasites was tested using the Z normal
c
approximation to the Mann-Whitney test and the
Fisher exact test, respectively (Zar, 1996). The
tests were only applied to species that showed
prevalence higher than 10% (Bush et al., 1990).
The significance level adopted was p 0.05.
The studied specimens are deposited in the
Helminthological Collection of Instituto
Oswaldo Cruz (CHIOC), Rio de Janeiro, Brazil.
A total of 61 specimens of T. atlanticus were
examined, of which 24 (39.4%) were males and
37 (60.6%) females. All hosts were parasitized
by at least three helminth species. Eighteen
different species had been identified: 15 species
of Digenea and three Monogenoidea. Among the
Digenea, 13 species (86.6%) belong to the
family Didymozoidae: Coeliotrema thynni
Yamaguti, 1938 – CHIOC: 37100, 37101,
37209-37211; Didymocystis bifasciatus
(Yamaguti, 1970) – CHIOC: 37966, 37967;
INTRODUCTION
MATERIALS AND METHODS
RESULTS
340
341
Neotrop. Helminthol., 8(2), 2014
Didymocystis lamotheargumedoi Kohn & Justo,
2008 – CHIOC: 36927, 36929, 36930-36932;
Didymocystis neothunni (Yamaguti, 1970) –
CHIOC: 37128, 37129; Didymosulcus orbitalis
(Yamaguti, 1970) – CHIOC: 37969, 37970a-b;
Didymosulcus palati (Yamaguti, 1970) –
CHIOC: 36944, 36945, 36947; Didymosulcus
philobranchiarca (Yamaguti, 1970) – CHIOC:
37971, 37972; Didymosulcus wedli (Ariola,
1902) – CHIOC: 37968a-b; Didymozoon
longicolle Ishii, 1935 – CHIOC: 37160, 37133;
Koellikerioides apicalis Yamaguti, 1970 –
CHIOC: 37143, 37148; Koellikerioides
internogastricus Yamaguti, 1970 – CHIOC:
37010, 37011; Koellikerioides intestinalis
Yamaguti, 1970 – CHIOC: 37132 and
Nephrodidymotrema ahi Yamaguti, 1970 –
CHIOC: 37139-37142; one Bucephalidae
(6.7%): Rhipidocotyle pentagonum (Ozaki,
1924) – CHIOC: 37062 and one Hemiuridae
(6.7%): Lecithochirium microstomum Chandler,
1935 – CHIOC: 37071. Three species of
Monogenoidea were found, representing 16.7%
of all parasites: Capsala biparasitica (Goto,
1894) – CHIOC: 37976, 37977; Capsala
katsuwoni (Ishii, 1936) – CHIOC: 37975 and
Table 1. Prevalence (P), intensity range (IR), intensity (I), mean intensity (IM), mean abundance (AM) and site
infection (SI) of parasites of T. atlanticus, from the coastal zone of the State of Rio de Janeiro coast, Brazil. Standard
deviation follows of mean values.
PARASITES P (%) IR I*/IM AM SI
DIGENEA
Didymozoidae
Coeliotrema thynni
37.8
1 - 71 12.12 ± 8.61 4.58 ± 3.60
Caeca
Didymocystis bifasciatus
13.3
8 - 71
31.50 ± 22.06
4.20 ± 4.30
Gills, operculum
Didymocystis lamotheargumedoi
26.7
20 - 1000
273.33 ± 198.07
72.89 ± 62.40
Operculum,
palate
Didymocystis neothunni
4.4
2 - 14
8.00±11.76
0.36 ± 0.61
Tongue
Didymosulcus orbitalis♦
20.0
2 - 40
9.78 ± 7.71
1.96 ± 1.90
Periorbital region
Didymosulcus palati
15.6
4 - 280 68.86 ± 73.75
10.71 ± 13.00
Gills, operculum
Didymosulcus philobranchiarca
42.2
32 - 1400 267.37 ± 145.32
112.89 ± 71.90
Operculum
Didymosulcus wedli♦
11.1
4 - 32 16.80 ± 9.07 1.87 ± 1.80
Gills
Didymozoon longicolle
6.7
1 - 92 39.00 ± 53.55 2.60 ± 4.12
Gills
Koellikerioides apicalis
4.4
1 - 4 2.50 ± 2.9 0.11 ± 0.18
Gills
Koellikerioides internogastricus
75.6
1 - 92 120.88 ± 48.09
91.33 ± 39.30
Stomach
Koellikerioides intestinalis
35.6
6 - 88 49.75 ± 18.13
17.69 ± 9.50
Intestine
Nephrodidymotrema ahi
11.1
1 - 12 4.20 ± 3.94 0.47± 0.60
Kidney
Bucephalidae
Rhipidocotyle pentagonum ♦
4.4
8 - 11 9.50 ± 2.94 0.42 ± 0.59
Stomach
Hemiuridae
Lecithochirium microstomum
♦
8.9
4 - 20 7.50 ± 8.22
0.67 ± 0.90
Stomach
MONOGENOIDEA
Capsalidae
Capsala biparasitica
4.4
1 - 7 4.00 ± 5.88
0.18 ± 031
Gills
Capsala katsuwoni 6.6 - 1* 0.07 ± 0.07 Gills
Nasicola brasiliensis ♦ 68.9 1 - 4 3.03 ± 0.34 2.09 ± 0.50 Nasal cavities
* Only one specimen was parasitized; ♦ New host record.
Justo & Kohn
Monogenoidea and Digenea parasites of Thunnus
Nasicola brasiliensis Kohn, Baptista-Farias,
Santos & Gibson, 2004 – CHIOC: 37973,
37974.
From the different Digenea species recovered,
the Didymozoidae represent the dominant
group, with 14,537 specimens collected
(81,25% of all digenetic parasites). The
dominant species among Monogenoidea was
Nasicola brasiliensis, with 94 specimens
collected (89.5% of all monogenetic).
Among the didymozoid species found, D.
lamotheargumedoi, D. philobranchiarca and K.
internogastricus were the dominant species with
highest average intensity and abundance.
Infection parameters are shown in table 1.
The studied parasites showed the typical
aggregated distribution pattern, except for N.
brasiliensis that showed an aleatory distribution
pattern. Didymocystis lamotheargumedoi, D.
phil o b r a nchiarc a, D. palati and K.
internogastricus presented the highest
dispersion index (table 2).
Spearman's correlation coefficient (r) showed
s
that the abundance of D. philobranchiarca, D.
wedli and D. lamotheargumedoi were positively
correlated with total length of the host (r =
s
Table 2. Dispersion index (DI) and d statistical of the parasites of T. atlanticus from the coastal zone of the State of
Rio de Janeiro coast, Brazil.
Parasites DI d
Didymosulcus philobranchiarca 536.5 208.0
Didymosulcus palati
185.7 118.5
Didymocystis lamotheargumedoi
625.3 225.3
Koellikerioides intestinalis
59.7 63.2
Didymosulcus orbitalis
21.0 33.6
Didymocystis wedli
20.5 33.1
Didymocystis bifasciatus
52.1 58.4
Koellikerioides internogastricus
198.3 122.8
Nephrodidymotrema ahi
7.8 16.8
Coeliotrema thynni
33.8 45.2
Nasicola brasiliensis 1.3 1.3
Table 3. Values of Spearman's rank correlation coefficient (r) to evaluated possible relationships among the host
s
total length abundance of the helminth parasites of T. atlanticus from the coastal zone of the State of Rio de Janeiro
coast, Brazil.
Parasites rsP
Didymosulcus philobranchiarca
Didymosulcus palati
Didymocystis lamotheargumedoi
Koellikerioides intestinalis
Didymosulcus orbitalis
Didymocystis wedli
Didymocystis bifasciatus
Koellikerioides internogastricus
Nephrodidymotrema ahi
Coeliotrema thynni
Nasicola brasiliensis
0.326
0.041
0.309
-0.186
0.193
0.335
-0.007
0.047
-0.033
-0.407
-0.126
0.029*
0.789
0.039*
0.221
0.204
0.024*
0.965
0.759
0.830
0.006*
0.411
* Significant values.
342
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Neotrop. Helminthol., 8(2), 2014
0.326, P = 0.029; r = 0.335, P = 0.024; r= 0.309,
s s
P = 0.039) respectively, and C. thynni was
negatively correlated with total length of the
host (r = -0.407, P = 0.006) (table 3). Pearson's
s
correlation coefficient (r) demonstrated that the
prevalence of K. internogastricus was correlated
with the total length of the host (r = 0.668, P =
0.025) (table 4).
Sex and parasite abundance were not correlated,
while sex and parasite prevalence were
correlated in C. thynni (F= 0.023) (table 5).
In this paper T. atlanticus represents a new host
record to four species of Digenea (D. orbitalis,
D. wedli, R. pentagonum e L. microstomum) and
one species of Monogenoidea (N. brasiliensis).
Table 4. Values of Pearson's correlation coefficient (r) obtained in relations between total length and prevalence of
the helminth parasites of T. atlanticus from the coastal zone of the State of Rio de Janeiro coast, Brazil.
Parasites rP
Coeliotrema thynni
-0.458 0.157
Didymocystis bifasciatus
-0.338 0.309
Didymocystis
lamotheargumedoi
0.142
0.677
Didymosulcus orbitalis
0.229 0.497
Didymocystis wedli
0.484 0.131
Didymosulcus palati
0.122 0.720
Didymosulcus philobranchiarca
0.534 0.091
Koellikerioides internogastricus 0.668 0.025*
Koellikerioides intestinalis
-0.114 0.739
Nasicola brasiliensis
0.005 0.988
Nephrodidymotrema ahi -0.372 0.260
*Significant values.
Table 5. Normal approximation Zof Mann-Whitney test and Fisher's (F) test values used to evaluate possible
c
relationships between the sex and abundance and prevalence of the helminth parasites of T. atlanticus from the
coastal zone of the State of Rio de Janeiro coast, Brazil.
Parasites
Zc PF
Coeliotrema thynni -1.9 0.059 0.023*
Didymocystis bifasciatus
-0.3 0.764 0.686
Didymocystis
lamotheargumedoi
-0.2
0.855 0.728
Didymosulcus orbitalis
-0.7 0.508 0.700
Didymocystis wedli
-0.3 0.728 1.000
Didymosulcus palati
-0.3 0.764 1.000
Didymosulcus
philobranchiarca
-1.7
0.089 0.212
Koellikerioides
internogastricus
-0.7
0.474 1.000
Koellikerioides intestinalis
-0.5 0.624 0.749
Nasicola brasiliensis
-1.2 0.230 0.197
Nephrodidymotrema ahi -0.7 0.501 0.641
*Significant values.
Justo & Kohn
Monogenoidea and Digenea parasites of Thunnus
A diverse community of Digenea and
Monogenoidea parasites infect T. atlanticus in
the coastal zone of southeastern Brazil. In this
study, didymozoids were the dominant parasites
of this tuna. The highly migratory habits of
widely distributed tuna, which migrate to
different oceans may leave the fish vulnerable to
several parasitic groups, mainly didymozoids,
which are widely distributed among oceanic
fishes. The dominance of didymozoids among
the Digenea parasitizing T. atlanticus in this
study is consistent with observations for other
tunas studied in other oceans (Madhavi & Ram
2000; Mladineo et al., 2008). This result was
expected, since tunas have a broad predatory diet
consisting of small fish, crustaceans and squids,
which brings them into contact with several
potential intermediate didymozoid hosts.
According to Sasal et al. (1999), the diet of the
host species is the main factor affecting parasite
community structure, especially for digenean
trematodes, since their final host is infected by
predating on the intermediate host. Several
reports on the didymozoids larvae parasitizing
small fishes (Køie & Lester, 1985; Korotaeva,
1985; Karlsbakk, 2001) and squids (Naidenova
et al., 1985; Shukhgalter & Nigmatullin, 2001;
Nigmatullin et al., 2009) confirm this
hypothesis. According to Naidenova et al.
(1985) heavy infection of squids is correlated
with high infection rates of the final hosts,
mainly scombrids.
According to Sasal et al. (1999), larger fish
generally eat more and for that reason they tend
to ingest greater amounts of intermediate hosts.
The correlation coefficient found between total
host length and the abundance of D.
p h i l o b r a n c h i a rc a , D. w e dli and D .
lamotheargumedoi may explain accumulative
infections.
Among all parasite species identified, only one,
C. thynni, showed sex preferences, being more
prevalent on T. atlanticus males. This is
surprising, because biological differences
between males and females of T. atlanticus have
not been reported in the literature.
The presence of didymozoid species in Atlantic
Ocean is evidence of their cosmopolitan
distribution and the cosmopolitan geographical
distribution of the host, showing that tuna fish
migration in different oceans may facilitate
infections by members of Didymozoidae.
Among the 15 species of Digenea and three
Monogenoidea studied, we report herein T.
atlanticus as a new host record for
Didymosulcus orbitalis, Didymosulcus wedli,
Rhipidocotyle pentagonum, Lecithochirium
microstomum, and Nasicola brasiliensis.
Didymosulcus orbitalis was originally described
from T. albacares and T. obesus by Yamaguti
(1970) from Hawaii and later redescribed by
Pozdnyakov (1989) from the shark
Pterolamiops longimanus; In Brazil, South
America this parasite was referred by Justo &
Kohn (2005) from T. obesus. D. wedli, had been
found in different oceans and hosts: in the
Mediterranean from Euthynnus alletteratus,
Thynnus vulgaris, Thunnus thynnus and
Katsuwonus pelamis (Ariola, 1902; Dollfus,
1926; Okada, 1926, Mladineo & Tudor, 2004);
in the Pacific from Scomber japonicus, K.
pelamis, T. thynnus, Seriola quinqueradiata
and Thunnus orientalis (Kobayashi, 1921;
Yamaguti, 1934; Ishii, 1935); in India from
Auxis thazard and Thunnus tonggol (Madhavi,
1982; Murugesh & Madhavi, 1995) and in the
Atlantic from T. albacares (Kohn et al., 2001).
Since its original description from
Scomberomorus nipponicus in Japan, R.
pentagonum had been referred in different hosts
and localities: It was found parasitizing T.
thynnus in the Mediterranean by Eckmann
(1932) and in the Pacific by Yamaguti (1938); In
the Gulf of Bengal from A. thazard by Madhavi
(1974) and Euthynnus affinis by Madhavi &
Ram (2000); In Mexico from Euthynnus lineatus
by Castillo-Sanchez et al. (1997) and in South
America from A. thazard and K. pelamis by
Fernandes et al. (2002). L. microstomum was
referred by different authors in several hosts: by
Manter (1940) from E. alletteratus in
Galapagos; by Pozdnyakov (1990) from E.
alletteratus and E. affinis from Pacific and by
Mogrovejo et al. (2004) from A. thazard in the
DISCUSSION
344
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Neotrop. Helminthol., 8(2), 2014
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Received July 30, 2014.
Accepted October 18, 2014.
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