Resumen
Abstract
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
NEW DATA ON THREE SPECIES OF KOELLIKERIOIDES
(DIGENEA, DIDYMOZOIDAE) IN BRAZILIAN TUNA FISH
NUEVOS DATOS SOBRE TRES ESPECIES DE KOELLIKERIOIDES
(DIGENEA, DIDYMOZOIDAE) EN ATÚN DE BRASIL
1 1,2
Márcia Cristina Nascimento Justo & Anna Kohn
1,2Laboratório de Helmintos Parasitos de Peixes, Instituto Oswaldo Cruz, Fiocruz Av. Brasil, 4365 Manguinhos, Rio de Janeiro, Brasil.
1 2
Financial support: Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro - Faperj, Conselho Nacional de Desenvolvimento
1
Científico e Tecnológico – CNPq. Corresponding author: marciajusto@ioc.fiocruz.br
Suggested citation: Justo M.C.N. & Kohn, A. 2011. New data on three species of Koellikerioides (Digenea, Didymozoidae)
in Brazilian tuna fish. Neotropical Helminthology, vol 5, nº 2, pp. 113-123.
Cuatro especies de peces escómbridos (Perciformes) de la zona costera de Río de Janeiro, Brasil,
fueron examinados para estudiar sus helmintos parásitos: Thunnus albacares (Bonnaterre, 1788),
Thunnus atlanticus (Lesson, 1831), Thunnus obesus (Lowe, 1839) y Euthynnus alletteratus
(Rafinesque, 1810). Tres especies del género Koellikerioides Yamaguti, 1970: K. apicalis Yamaguti,
1970, K. externogastricus Yamaguti, 1970 y K. intestinalis Yamaguti, 1970, se registraron en las
branquiespinas, en la capa muscular externa de la pared del estómago y en la superficie interna del
intestino delgado, respectivamente. Se presentan las medidas originales, los parámetros de la
infeccióny las ilustraciones originales. K. apicalis y K. intestinalis mostraron el patrón típico de
distribución agregada. El análisis estadístico mostro que había una correlación negativa significativa
entre la longitud total de E. alletteratus y la prevalencia de K. intestinalis. Los resultados de K. apicalis
en T. atlanticus y de K. intestinalis en T. atlanticus y E. alletteratus representan nuevos registros de
hospedadores. Todas las especies se reportan por primera vez en el Océano Atlántico Sudoccidental.
Palabras clave: Parásitos de peces-Koellikerioides apicalis - Koellikerioides externogastricus - Koellikerioides intestinalis
- Scombridae.
Four species of scombrid fishes (Perciformes) from the coastal zone of Rio de Janeiro, Brazil, were
examined for helminth parasites. These are Thunnus albacares (Bonnaterre, 1788), Thunnus atlanticus
(Lesson, 1831), Thunnus obesus (Lowe, 1839) and Euthynnus alletteratus (Rafinesque, 1810). Three
species of the genus Koellikerioides Yamaguti, 1970: K. apicalis Yamaguti, 1970, K. externogastricus
Yamaguti, 1970 and K. intestinalis Yamaguti, 1970, were recorded from the gill raker, the outer muscle
layer of the stomach wall and the inner surface of the small intestine, respectively. Original
measurements, parameters of infection and original figures are presented. K. apicalis and K. intestinalis
showed the typical aggregated distribution pattern. Statistical analysis showed that there was a
significant negative correlation between the total lengths of E. alletteratus and the prevalence of K.
intestinalis. The findings of K. apicalis in T. atlanticus and of K. intestinalis in T. atlanticus and E.
alletteratus represent new host records. All species are reported for the first time in the Southwest
Atlantic Ocean.
Keywords: Fish parasites - Koellikerioides apicalis - Koellikerioides externogastricus - Koellikerioides intestinalis -
Scombridae.
Neotrop. Helminthol., 5(2), 2011
2011 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
Versión Impresa: ISSN 2218-6425 / Versión Electrónica: ISSN 1995-1043
113
The 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. Species of Thunnus are found worldwide
and are known to migrate extensively (Collete &
Nauem, 1993), except Euthynnus alletteratus
(Rafinesque, 1810) that is less migratory than other
tuna (Fischer, 1978). According Madhavi & Ram
(2000) the high vagility and endothermy require
high metabolic energy which is met through
foraging on large quantities of food items
comprising crustaceans, fish, mollusks and
polychaetes that serve as intermediate and
paratenic hosts for didymozoid and other helminth
parasites. Didymozoids are parasites of marine
teleosts, mainly scombrids and rarely are found in
freshwater fishes. They represent a different group
of parasites by the general morphology highly
adapted to different habitats, not common to other
digenean parasites.
In our studies with helminth parasites of
Scombridae from Brazil, the most prevalent and
abundant species belong to the Digenea family
Didymozoidae Monticelli, 1888 (Justo & Kohn
2005, 2009, 2010; Kohn & Justo, 2008; Justo et
al., 2008, 2009) which agree with the results in
different parts of the world (Ishii, 1935; Yamaguti,
1970; Lester et al. 1985; Nikolaeva, 1985;
Pozdnyakov, 1996; Madhavi & Ram 2000;
Munday et al., 2003; Mladineo et al., 2010). Brazil
is the most important South American country for
fishing of scombrids in the Southwest Atlantic
Ocean, but very little is known about the parasites
of these species.
The aim of this study is to contribute to the increase
of the knowledge and expansion of the
geographical distribution of didymozoid parasites
of tuna in the area of the Southern Atlantic Ocean.
INTRODUCTION
MATERIAL AND METHODS
A total of 149 specimens of tuna fishes were
examined between January of 2004 and April
of 2007: 38 specimens of Thunnus albacares
(Bonnaterre, 1788) (34 - 76 cm total body
length; 0.550 - 7.8 kg), of which 15 (39.4%)
were males and 23 (60.6%) were females; 45
Thunnus atlanticus (Lesson, 1831) (45 - 82 cm total
body length; 1.3 - 6.0 kg) 16 (35.5%) males and 29
(64.5%) females; 35 Thunnus obesus (Lowe, 1839)
(42 - 80 cm total body length; 1.2 - 8.0 kg) 21 (60%)
males and 14 (40%) females and 31 Euthynnus
alletteratus (Rafinesque, 1810) (31 - 80 cm total
body length; 0.525 - 4.0 kg) 16 (51.6%) males and
15 (48.4%) females.
The fishes were obtained from local fishermen
from the coastal zone of the State of Rio de Janeiro,
off Cabo Frio, Brazil (22º52'46”S, 42º01'07"W).
The parasites were released from dissected cysts
and fixed with or without compression in AFA
(alcohol 93%, formalin 5%, acetic acid 2%),
stained in alcoholic-acid carmine, dehydrated in an
alcohol series, cleared in methyl salicilate and
mounted in Canada balsam. Measurements are in
micrometers, with the mean in parentheses
followed by the number of specimens measured in
brackets, where applicable. Analysis of the
parameters of infection, related to prevalence (P),
mean intensity (MI), mean abundance (MA) and
range of infection (RI) were based on Bush et al.
(1997). Confidence intervals (95%) were
calculated assuming a binominal distribution,
using software Quantitative Parasitology 3.0
(Rózsa et al., 2000). The quotient between variance
and mean of 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) was used to determine
s
possible host length correlations with parasitism
abundance. Pearson's coefficient of correlation (r)
was used to determine possible correlations
between the host's total length and prevalence of
parasites, with angular transformation of
prevalence values; Mann-Whitney's U Test with Zc
normal approximation, to determine host sex effect
on infection/infestation abundance of each parasite
species (Zar, 1996). The tests were only applied to
species that showed prevalence higher than
10% (Bush et al., 1990). Statistical
significance level p ≤ 0.05 was adopted. Light
micrographs were taken with a digital camera
connected to a Nikon Eclipse E 800
microscope and confocal laser scanning light
micrographs with a ZEISS LSM 510.
Representative specimens were deposited in
114
Koellikerioides in Brazilian tuna fish Justo & Kohn
the Helminthological Collection of the Oswaldo
Cruz Institute (CHIOC), Rio de Janeiro, Brazil.
RESULTS
During a survey of the helminth parasites of
scombrid fishes from Rio de Janeiro coast, three
species of didymozoid described by Yamaguti
(1970) in the genus Koellikerioides were
recovered. The trematodes were found parasitizing
four species of scombrid fishes: T. albacares, T.
atlanticus, T. obesus and E. alletteratus.
Specimens of Koellikerioides apicalis Yamaguti,
1970 were found encysted in pairs on the gill raker
from two (4.4%) out of 45 T. atlanticus (new host
record), four (10.5%) out of 38 T. albacares and
two (5.7%) out of 35 T. obesus examined.
Specimens of Koellikerioides intestinalis
Yamaguti, 1970 were easily observed in the wall
and lengthwise on the inner surface of the small
intestine from 16 (35.8%) out of 45 T. atlanticus
(new host record), eight (23.7%) out of 38 T.
albacares, five (14.3%) out of 35 T. obesus and six
(19.4%) out of 31 E. alletteratus (new host record)
examined. Specimens of K. externogastricus
Yamaguti, 1970 were found encysted in the
external wall of the stomach from one (2.6%) out of
38 T. albacares examined.
Brief descriptions with main measurements are
presented, considering that the morphology of the
studied species was already originally well
described. Measurements of K. apicalis and K.
intestinalis are presented in Tables 1 and 2
respectively and parameters of infection in Tables 3
and 4.
K. apicalis and K. intestinalis showed a typical
aggregated distribution pattern (Table 5). Pearson's
correlation coefficient demonstrates that the
prevalence of K. intestinalis was negatively
correlated with the total length of E. alletteratus
(r= -0.596, P= >0.001) (Table 6). There was no
correlation between the abundance of parasites and
the total length of their hosts (Table 6). The mean
abundance and prevalence of K. intestinalis
parasitizing T. albacares were influenced by the
sex (Z = -2.70, P= 0.044; F= 0.006) occurring only
in females (Table 7).
Koellikerioides apicalis Yamaguti, 1970 (Figs. 1A
-D, Table 1)
Hosts: T. atlanticus (new host record), T. albacares
and T. obesus.
Site of infection: Encysted in pairs in gill raker.
Deposition of voucher specimens: CHIOC n:
37143-37147, 37148 a-b.
Cysts are easily observed in the gill raker and
contain a pair of worms (Fig. 1A) with strong
sexual dimorphism expressed by the male being
smaller than the female and located in a special
cavity in the female's body. Measurements of
specimens from the three hosts are presented in
Table 1.
Male (Fig. 1C): Brief description based on three
compressed specimens. Body divided into two
regions (anterior and posterior). Anterior region
scoop-shaped, widest at oesophageal level.
Figure 1. Koellikerioides apicalis Yamaguti, 1970: A: Light
micrograph of male and female; B - Light micrograph of
female; C - Light micrograph of male; D – Confocal scanning
light micrograph of eggs. Scale bars= 500 µm (A, B); 200 µm
(C); 10 µm (D).
115
Neotrop. Helminthol., 5(2), 2011
Table 1.- Original measurements (µm) of females and males of Koellikerioides apicalis from T. atlanticus (new host record),
T. albacares and T. obesus.
L= lenght; W = width.
Posterior region rounded. Oral sucker well
developed, globular, muscular, terminal; pharynx
present; oesophagus surrounded by gland-cells,
bifurcated into two caeca. Testis single, tubular;
vas deferens opening ventral to oral sucker.
Female (Fig. 1B): Brief description of seven
compressed specimens. Body divided into two
regions (anterior and posterior). Anterior region of
body scoop-shaped widest at level of oesophagus.
Posterior region with a special cavity for male. Oral
sucker terminal, muscular, globular, followed by
pharynx; oesophagus surrounded by gland-cells,
bifurcated into two caeca. Ovary long, bifurcated,
with a total of four long winding terminal branches,
ending in the middle of posterior region of body.
Seminal receptacle oval, near anterior extremity of
body's posterior region. Vitelline gland tubular,
ramified. Uterine coils occupying most of the
available space in posterior region. Eggs bean-
shaped, embryonated (Fig. 1D).
Remarks
Koellikerioides apicalis described by Yamaguti
(1970) from the gill raker of T. obesus
(=Parathunnus sibi) from Hawaii, Pacific Ocean,
was reported by Pozdnyakov (1990, 1996) in T.
albacares, T. alalunga (Bonnaterre, 1788) and T.
obesus also from the Pacific Ocean. Mladineo &
Tudor (2004) reported this species in the
cartilaginous part of the gill arch and in the apical
part of the pseudobranch of Thunnus thynnus
(Linnaeus, 1758) from the Adriatic Sea. In the
present study, K. apicalis was isolated from the gill
raker of T. obesus (type-host), T. albacares and
from a new host T. atlanticus. Morphology and
116
Koellikerioides in Brazilian tuna fish Justo & Kohn
Brief descriptions and main measurements based
on compressed specimens of two males and three
females. Cysts rounded and easily observed as
yellowish prominences in outer muscle layer of
stomach wall. Male smaller than female, placed in
special cavity of female. Body divided into two
regions (anterior and posterior) in both sexes.
Male: Anterior region scoop-shaped 4600 – 5400
long by 220 – 360 wide at oesophageal level.
Posterior region reniform measuring, 900 long by
550 wide, enclosed in special hollow of female.
Oral sucker muscular 102 – 120 long by 85 – 92
wide; pharynx 50 – 62 long by 35–50 wide;
oesophagus bifurcated into two caeca. Testis single,
cylindrical; vas deferens opening ventral to oral
sucker.
Female: Anterior region of body scoop-shaped,
4400 – 5100 (4700) long by 320 – 550 (470) wide.
Posterior region rounded, 5500 – 8300 (6930) long
by 5200 – 9200 (6933) wide, with a special cavity
to accommodate the male. Oral sucker muscular,
162 – 197 (180) long by 117 – 187 (152) wide,
followed by pharynx 87 – 105 long [n=2] by 60 – 92
wide [n=2]; oesophagus narrow, sigmoid,
bifurcated into caeca. Ovary long consisting of two
long branches. Vitelline gland tubular, ramified,
with several terminal branches. Uterine coils
occupying most of the available space in posterior
region. Metraterm well differentiated, opening
ventral to the oral sucker. Eggs bean-shaped,
embryonated, 20 long by 10 – 12 (10) wide [n=30].
Host: T. albacares
Site of infection: Encysted in pairs in outer muscle
layer of stomach wall.
Deposition of voucher specimens: CHIOC n:
37095 a-c.
Koellikerioides externogastricus Yamaguti, 1970 (Fig. 2)
Figure 2. Koellikerioides externogastricus Yamaguti, 1970.
Light micrograph of male and female. Scale bar= 2 mm.
Remarks
Koellikerioides externogastricus was found by
Yamaguti (1970) encysted in the outer muscle layer
of the stomach of T. albacares (= Neothunnus
macropterus) and T. obesus from Hawaii, Pacific
Ocean. It was later reported by Pozdnyakov (1990)
from T. alalunga, T. albacares and T. obesus also in
the Pacific Ocean. Our specimens were collected
from the type-host T. albacares, in the same site of
infection and the morphology and measurements
agree with the original description.
Hosts: T. obesus, T. albacares, T. atlanticus (new
host record) and E. alletteratus (new host record).
Site of infection: Encysted in pairs on inner surface
of small intestine.
Deposition of voucher specimens: CHIOC n:
37131 a-c, 37132 a-e.
Brief descriptions and main measurements (Table
2) based on compressed specimens of four males
and eight females.
measurements of studied specimens agree with the
original description except in the size of the
anterior region of the male's body: 800-1600 long
in our specimens compared to with 500-600 and
400-600 in Yamaguti's and Pozdnyakov's papers,
respectively.
Koellikerioides intestinalis Yamaguti, 1970 ( Fig. 3,
Table 2)
117
Neotrop. Helminthol., 5(2), 2011
Table 2. Original measurements (µm) of females and males of Koellikerioides intestinalis from T. atlanticus (new host record),
E. alletteratus (new host record), T. albacares and T. obesus.
L= lenght; W = width.
Table 3. Prevalence (P%), mean intensity (MI), mean abundance (MA), range (R), Intensity (I) and confidence interval (CI) of
Koellikerioides apicalis and Koellikerioides externogastricus.
* One host parasitized.
Table 4. Prevalence (P%), mean intensity (MI), mean abundance (MA), range (R), Intensity (I) confidence interval (CI) of
Koellikerioides intestinalis.
W
118
Koellikerioides in Brazilian tuna fish Justo & Kohn
Table 5. Dispersion index (DI) and d test of Koellikerioides intestinalis and Koellikerioides apicalis
(*) significant values.
Table 6. Values of Spearman's rank correlation coefficient (r) and Pearson's correlation coefficient (r) obtained in relations
s
between total length of hosts, and abundance and prevalence of Koellikerioides intestinalis.
P= level of significance, (*) significant values.
Table 7. Normal approximation Zof Mann-Whitney test and Fisher's (F) test values used to evaluate possible relationships
c
between the sex of hosts and abundance and prevalence of Koellikerioides intestinalis.
P= level of significance, (*) significant values.
Small cysts containing male and female worms
were easily visible to the naked eye, located just
under the mucosa of the small intestine. Male
smaller than female, placed in special cavity of
female. Body divided into two regions (anterior
and posterior) in both sexes.
Male: Anterior region of body scoop-shaped wide
at level of oesophagus. Posterior region rounded
placed in special hollow of posterior region of
female, very difficult to see, due to large amount of
eggs. Oral sucker terminal, followed by globular
pharynx; oesophagus narrow, long, bifurcated into
two caeca. Testis single, tubular, curved along
convex margin of body's posterior region; vas
deferens opening ventral to oral sucker.
Female: Anterior region of body scoop-shaped
wide at oesophageal level. Posterior region oval
K.intestinalis
DI d
k. apicalis
DI d
119
Neotrop. Helminthol., 5(2), 2011
Remarks
Koellikerioides intestinalis was described from the
Pacific Ocean by Yamaguti (1970) in T. obesus and
reported by Pozdnyakov (1990) in T. albacares, T.
alalunga and T. obesus. In the Adriatic Sea this
species was reported by Mladineo & Tudor (2004)
from T. thynnus. Lately, Mladineo & Bočina (2009)
published a paper on the type and ultratructure of K.
intestinalis and concluded that the ultrastructure of
cysts does not differ in architecture or type of
connective tissue fibers expressed at the parasitism
site, being of host origin. Our specimens were
found encysted lengthwise on the inner surface of
the small intestine, the same site of infection as in
the original description, parasitizing T. albacares,
T. obesus and two new hosts: T. atlanticus and E.
alletteratus. No significant differences between
our specimens and those of the original description
were observed.
DISCUSSION
The Digenea family Didymozoidae represents a
very important group of trematodes parasites of
tuna fish. In South America, mainly in the southern
Atlantic Ocean, there is a small number of species
reported, in contrast to well studied regions of the
Pacific Ocean. The present study contributes to
increase the knowledge and expansion of the
geographical distribution of three species of
Koellikerioides. Till now only two species of
Koellikerioides had been reported in South
America: one undetermined species referred by
Tantaleán et al. (1992) from Sarda chiliensis
chiliensis (Cuvier, 1832) in Peru and
Koellikerioides internogastricus Yamaguti, 1970
reported by Justo et al. (2009) from T. atlanticus, T.
albacares and T. obesus in Brazil.
Koellikerioides apicalis and K. intestinalis were
reported by Mladineo & Tudor (2004) parasitizing
the cage-reared northern bluefin tuna, Thunnus
thynnus thynnus in the Adriatic-Sea showing high
prevalence: 73.68 % and 57.89 %, respectively. In
2008, Mladineo et al. referred that the mean
prevalence of these species collected in the same
locality from the Atlantic bluefin tuna, T. thynnus,
was 10.93% for K. apicalis and 54.64% for K.
intestinalis.
Comparing with our results we conclude that the
prevalence of K. apicalis (T. albacares: 10.5%, T.
atlanticus: 4.4%, T. obesus: 5.7%) and of K.
intestinalis (E. alletteratus: 19.4%, T. albacares:
21.1%, T. atlanticus: 35.6%, T. obesus: 14.3%)
from Atlantic Ocean are smaller than the presented
in the northern bluefin tuna and similar with the
prevalence of K. apicalis from Atlantic bluefin tuna
from the Adriatic.
Several papers about parasites of scombrid fishes
in Brazil showed high prevalence for different
species of didymozoids (Justo & Kohn, 2005,
2009, 2010; Alves & Luque, 2006; Kohn & Justo,
2008; Justo et al., 2008, 2009), demonstrating wide
geographical distribution for these trematodes.
It was not observed in our study, any correlation
between the abundance of parasites and the total
length of their hosts. Although, the prevalence of K.
intestinalis was negatively correlated with the total
length of E. alletteratus. As mentioned by
Polyanski (1961), quantitative and qualitative
changes in parasitism are expected as the fish
to rounded with a special cavity for male. Oral
sucker terminal, muscular, globular, followed by
muscular pharynx; oesophagus short. Ovary long,
branched. Vitelline gland tubular, ramified.
Seminal receptacle opening into genital junction.
Uterine coils occupying most of the available space
in posterior region. Eggs bean-shaped.
Figure 3. Koellikerioides intestinalis Yamaguti, 1970.
Confocal scanning light micrograph of male (m) and female
(f). Scale bar= 500 µm.
120
Koellikerioides in Brazilian tuna fish Justo & Kohn
grows. Saad-Fares & Combes (1992) related that
ontogenetical changes in the feeding behavior
might have an influence on parasite prevalence and
abundance in the host size classes.
In our results we observed that host sex does not
influence the prevalence and intensity of infection.
However, K. intestinalis showed a correlation in
the abundance and prevalence with the sex host, as
it was found only in the females of T. albacares.
These correlations were surprising since
differences in biological conditions of males and
females of T. albacares are unknown. According to
Luque et al. (1996) and Alves et al. (2002) the
absence of correlations in parasite prevalence and
abundance with the sex of the host fish is a widely
documented pattern, and interpreted as a
consequence of absence of sexual differences in
some biological aspects of the fish. Our result
could have been purely accidental in the studied
sample and influenced by the higher number of
females examined, making it necessary to study a
larger number of individuals to confirm these
results.
In this opportunity we report K. apicalis, K.
externogastricus and K. intestinalis, for the first
time in Brazil, representing the first record of these
species in the southwest Atlantic Ocean and in new
host records: T. atlanticus (K. apicalis and K.
intestinalis) and E. alletteratus (K. intestinalis).
These results increase the knowledge and
geographic distribution of the family
Didymozoidae in South America and indicate the
importance of expanding the study to other species
of tuna from the Atlantic Ocean.
The authors are grateful to ''Instituto de Estudos do
Mar Almirante Paulo Moreira–IEAPM'' and to
Eliane Gonzalez Rodriguez, head of the
''Departamento de Oceanografia'' for the facilities
provided for examination of the fishes; to Eduardo
Pimenta for giving us the opportunity to obtain the
fishes; to Mariana dos Santos Lopes from the
“Laboratório de Helmintos Parasitos de Peixes,
Instituto Oswaldo Cruz” for help both in the field
and in the laboratory.
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Received May 26, 2011.
Accepted August 27, 2011.
Correspondence to author/Autor para correspondencia:
E-mail/correo electrónico:
marciajusto@ioc.fiocruz.br
Márcia Cristina Nascimento Justo
Laboratório de Helmintos Parasitos de Peixes, Instituto
Oswaldo Cruz, Fiocruz
Av. Brasil, 4365 Manguinhos, Rio de Janeiro, Brasil.
123
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