ORIGINAL ARTICLE /ARTÍCULO ORIGINAL

1,3 2,* 1,4

Bianca Porto Kuraiem ; Marcelo Knoff ; Nilza Nunes Felizardo ;

2 1,4

Delir Corrêa Gomes & Sérgio Carmona de São Clemente

1Laboratório de Inspeção e Tecnologia do Pescado, Universidade Federal Fluminense - UFF, Niterói, RJ, Brasil.

2 Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, Fiocruz IOC, Rio de Janeiro, RJ, Brasil.

3Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES.

4 Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq.

*Correspondence to author/ Autor para correspondencia: Marcelo Knoff

Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz – Fiocruz, Av. Brasil,

4365, Manguinhos, CEP 21045-900, Rio de Janeiro, RJ, Brasil. Phone: +55(21) 25621462, Fax: +55(21) 25621511

E-mail/correo electrónico: knoffm@ioc.fiocruz.br

Neotropical Helminthology, 2016, 10(1), ene-jun: 33-40.

ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

CALLITETRARHYNCHUS SPECIOSUS (LINTON, 1897) CARVAJAL & REGO, 1985

TRYPANORHYNCHA (CESTODA) PARASITIZING PRIACANTHUS ARENATUS

(CUVIER, 1829) (OSTEICHTHYES, PRIACANTHIDAE) FROM RIO DE JANEIRO

COAST, BRAZIL

CALLITETRARHYNCHUS SPECIOSUS (LINTON, 1897) CARVAJAL & REGO, 1985

TRYPANORHYNCHA (CESTODA) PARASITANDO PRIACANTHUS ARENATUS

(CUVIER, 1829) (OSTEICHTHYES, PRIACANTHIDAE) DE LA COSTA DE RÍO DE

JANEIRO, BRASIL

ABSTRACT

Keywords: Brazil - Callitetrarhynchus speciosus - Cestode - Priacanthus arenatus - seafood safety - Trypanorhyncha

Thirty specimens of Priacanthus arenatus (Cuvier, 1829) were commercially obtained in the

municipalities of Niterói and Rio de Janeiro, State of Rio de Janeiro, Brazil and examined for

parasites from July to December 2013. The fish were necropsied to investigate the presence of

cestodes larvae. Three fish were parasitized with trypanorhynchids identified as

Callitetrarhynchus speciosus (Linton, 1897) Carvajal & Rego, 1985 based on morphological and

morphometric characters. The parasite indices of prevalence, mean abundance, mean intensity

and the infection sites are presented. Plerocerci were found in mesentery, intestine and ovary

serosa. These parasites were studied because of their importance during fish sanitary inspection,

if one considers the harm that the repulsive aspect of infected fish causes to consumers.

RESUMEN

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016

INTRODUCTION

The Priacanthus arenatus (Cuvier, 1829), the

Atlantic bigeye, has large eyes and reddish

body, is a nocturnal teleostean species, lives on

rocky bottoms at 10 to 200 meters depths,

occurs in tropical and subtropical waters of the

Atlantic Ocean, from Canada to Argentina. It

feeds mainly on small fishes, crustaceans and

polychaetes. Reaches an average length of 40

cm and has high commercial value meat

(Figueiredo & Menezes, 1980).

In the State of Rio de Janeiro, this species was

studied concerning to the parasitism by

helminths by Pinto et al. (1988), De Fabio

(2000), Tavares et al. (2001), Lima (2004) and

Ferreira et al. (2006).

The Trypanorhyncha order consists of great

diversity of species, all parasitizing marine fish

and invertebrates. Adult worms live in the

intestine of elasmobranchs fish (sharks and

rays) while the larval forms are found in the

coelomic cavity and muscles of teleost fish,

crustaceans and molluscs cephalopods

(Campbell & Beveridge, 1994). In the fish

sanitary inspection, trypanorhynch cestodes,

even not having zoonotic potential, acquire

importance by the disgusting appearance.

According to the Brazilian Industrial and

Sanitary Inspection of Animal Origin Products

Regulation, in his item 4 of Article 445 are

considered unsafe to eat the fish that have

massive muscle infestation by parasites

(Brasil, 1952). Reinforcing the importance of

cestodes for fish inspection in many species of

teleost is common to see up high rates of

infection in the muscles (Dollfus, 1942; Amato

et al., 1990; Pereira Jr., 1993; São Clemente et

al., 1995, 1997).

Some trypanorhynch species such as

Gymnorhynchus gigas (Cuvier, 1817)

Rudolphi, 1819 larvae have antigenic

components able to cause anaphylactic

episodes (Rodero & Cuellar, 1999). Vázquez-

López et al. (2002) showed that proteins of G.

gigas may alter the motility and the intestinal

transit. Mattos et al. (2013) demonstrated by

inoculation that the gross extracts of

Pterobothrium heteracanthum Diesing, 1850

molecules are capable of inducing the

production of specific IgE and IgG, thus

inducing an allergic reaction in murine models.

The Callitetrarhynchus speciosus (Linton,

1897) Carvajal & Rego, 1985 was reported in

several teleost fish worldwide (Bates, 1990;

Kuraiem et al.

De julio a diciembre de 2013, fueron comprados 30 ejemplares de Priacanthus arenatus (Cuvier,

1829) comercializados en los municipios de Niterói y Rio de Janeiro, Estado de Rio de Janeiro,

Brasil. A los peces se les practicó la autopsia y se filetearon para investigar la presencia de larvas

de cestodos. Tres peces fueron parasitados con trypanorhyncha y fueron identificados como

Callitetrarhynchus speciosus (Linton, 1897) Carvajal & Rego, 1985 basado en caracteres

morfológicos y morfométricos. Los índices parasitarios de prevalencia, abundancia media, la

intensidad media y los sitios de infección son presentados. Los plerocercos se encontraron en el

mesenterio, y serosas del ovario y del intestino. Estos parásitos se estudiaron por su importancia

para la inspección sanitaria de los peces, teniendo en cuenta el daño que el aspecto repulsivo de

los peces infectados impulsa a los consumidores.

Palabras clave: Brasil - Callitetrarhynchus speciosus - Cestodo - Priacanthus arenatus - seguridad del pescado - Trypanorhyncha

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016

Palm, 2004; Abdou & Palm, 2008; Al-Zubaidy

& Mhaisen, 2014; Beveridge et al., 2014; Palm

& Bray, 2014). The last records of this species

in Brazil were made by Lima (2004), Dias et al.

(2009, 2010, 2011).

The aim of this study was to determine the

species of trypanorhynch parasitizing P.

arenatus, their parasitary indices and infection

sites, and to discuss about zoonotic

importance.

From July to December 2013, thirty P.

arenatus specimens were acquired with 20-63

(38.3 ± 13.05) cm total length and 400-3,600

(1,210 ± 751) g weight from the fish markets in

the municipalities of Niterói and Rio de

Janeiro, State of Rio de Janeiro, Brazil. The

fish were transported in isothermal box to the

Laboratory of Inspection and fish Technology

of the Veterinary Medicine School of

Fluminense Federal University, where they

were necropsied and filleted. The fish species

was identified according to Figueiredo &

Menezes (1980). Collected plerocerci of

Trypanorhyncha were opened, with the aid of

sharp needles, under the stereomicroscope to

release the larvae, that were put in the

refrigerator for at least 24h to permit the

relaxing of scolices and tentacular

extroversion. Further, the larvae were fixed in

cold AFA, stained with Langeron´s carmine,

clarified in beechwood creosote, and

preserved either as whole mounts on Canada

balsam according to Knoff & Gomes (2012).

The classification of Trypanorhyncha was

based on Palm (2004). The parasitic indices on

the prevalence, mean intensity and mean

abundance were calculated according to Bush

et al. (1997). Representative speciments were

deposited in the Helminthological Collection

of the Oswaldo Cruz Institute (CHIOC).

MATERIALS AND METHODS

The analysis of 30 specimens of P. arenatus

necropsied presented three infected fish with

one specimen of 2.5 to 3 cm lenght

trypanorhynch plerocerci each one, taxonomic

identified as beneath.

Lacistorhynchoidea Guiart, 1927

Lacistorhynchidae Guiart, 1927

Lacistorhynchinae Guiart, 1927

Callitetrarhynchus Pintner, 1931

Callitetrarhynchus speciosus (Linton, 1897)

Carvajal & Rego, 1985 (Figs. 1-3).

Description of main features: based on three

plerocerci collected of P. arenatus. Plerocerci

with blastocist present tail extension. Scolex

elongated, thin and acraspedote. Two

patteliform bothria with weakly notched

posterior margins. Pars vaginalis long, tentacle

sheaths regurlarly sinuous, enlarged anteriorly,

less sinuous on the pars botrialis region. Bulbs

elongated. Retractor muscles originate in

anterior 1/3 of bulbs. Pars postbulbosa present,

small. Metabasal armature poeciloacanthous

atypical, heteromorphous; hooks hollow, in

ascending half spirals of 8 principal hooks,

beginning on internal surface. The hooks 1(1´)

are large and uncinate, the hooks 2(2´) are

uncinate and long, the hooks 3(3´) are

falciform, large and has large bases, the hooks

4(4´) and 5(5´) are falciform, the hooks 6(6´)

are spiniform and be located near from external

surface, the satellite hooks 7(7') and 8(8') are of

same size and slender uncinate shape. A simple

chainette is present.

The parasitic indices of prevalence, mean

abundance and mean intensity of infection by

C. speciosus larvae, as well as the infection

sites and the deposit number at CHIOC are

depicted in Table 1 and the morphological and

morphometric data of C. speciosus larvae

colleted in P. arenatus are presented in Table 2.

RESULTS

Callitetrarhynchus speciosus in Priacanthus

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Kuraiem et al.

Figures 1-3. Callitetrarhynchus speciosus plerocercus from Priacanthus arenatus . Fig. 1. Entire plerocercus, lateral view.

Squares 2 and 3 indicate the area where the figures were obtained. Scale bar of fig.1 = 1000 µm. Fig. 2. Detail of the external face

hooks arrangement of the basal armature tentacle, showing the 3, 4, 5, 6, 7 (7') 8 (8') hooks and chainette (c). Fig. 3. Detail of

external face hooks arrangement of the metabasal armature tentacle, showing the 6, 7 (7 '), 8 (8') hooks and chainette (c). Scale

bars of figs. 2 and 3 = 50 µm.

presented the range “...ppb absent (160-

340)...” (page 347). Al-Zubaidy & Mhaisen

(2014) reported the presence of ppb measuring

250 (150-280). In the specimens collected

from Cynoscion guatucupa (Cuvier, 1830) off

coast of the State of Rio Grande do Sul,

deposited in the CHIOC under the numbers:

33905, 33906, 33907, was possible to observe

the absence of pars post-bulbosa; such as Lima

(2004) related that absence in collected

plerocerci of P. arenatus, Epinephelus morio

(Valenciennes, 1828), E. guaza Linnaeus,

1758, E. flavolimbatus Poey, 1865 and E.

Table 1. Parasitary indices of prevalence (P), mean intensity (MI) and mean abundance (MA), infection sites (IS),

and number of deposit in the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC) of the

Callitetrarhynchus speciosus larvae from Priacanthus arenatus off the coast of State of Rio de Janeiro, Brazil.

P (%)

MA MI IS CHIOC

Callitetrarhynchus speciosus

0.1 1 M, IS,

37994,

37995,

37996

M= mesentery; IS= intestine serosa; OS= ovary serosa.

Table 2. Morphological and morphometric data of the Callitetrarhynchus speciosus plerocerci from Priacanthus

arenatus off the coast of State of Rio de Janeiro, Brazil.

Callitetrahynchus speciosus

Scolex (L) 11.175 – 12.200 (11.758)

Scolex (W) 2.025 – 2.350 (2.191)

Appendix (L)

10.750

–

14.975 (12.416)

Appendix (W)

1.275 –

1.475 (1.358)

Pars bothrialis (L)

2.025 –

2.125 (2.066)

Pars bothrialis (W)

2.075 –

2.25 (2.166)

Pars vaginalis (L)

8.625 –

9.200 (9.008)

Pars vaginalis (W)

1.675 –

2.300 (1.958)

Pars bulbosa (L)

2.100

–

2.375 (2.250)

Pars bulbosa (W)

0.975 –

1.375 (1.166)

Pars post-bulbosa

(L)

0.300

–

0.570 (0.440)

Bulbs (L) 1.970

–

2.370 (2.170)

Bulbs (W) 0.250 – 0.320 (0.290)

Tentacles (L) 0.940 – 3.840 (2.578)

Tentacles (DB) 0.060- 0.100 (0.080)

Tentacles (MBD) 0.060 – 0.090 (0.060)

L = length; W = width; BD = basal diameter; MBD = metabasal diameter.

Measurements are presented in millimeters.

DISCUSSION

The collected specimens of C. speciosus of the

present study are in accordance with the

morphological and morphometric data of

species redescription did by Carvarjal & Rego

(1985). It was observed that the present study

specimes showed a small pars post–bulbosa,

measuring 440 (300-570) µm, as observed by

Carvajal & Rego (1985) which reported it with

200 (160-340) µm lenght (pages 162 and 163).

Palm (2004) related it as absent, but has

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Callitetrarhynchus speciosus in Priacanthus

Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Kuraiem et al.

niveatus (Valenciennes, 1828). This fact shows

that the pars post-bulbosa can presents a little

lenght or even be absent in C. speciosus, like an

intraspecific variation.

Lima (2004) reported C. speciosus in P.

arenatus with prevalence of 12.5%, near to the

result of this study. Differently for the present

study he had reported that all the fish harboring

C. speciosus presented concomitant infection

with C. gracilis Pintner, 1931. Differently,

Pinto et al. (1988), De Fabio (2000), Tavares et

al. (2001) and Ferreira et al. (2006) which

studied helminth infection for the same host

have not found trypanorhynchs.

In other fishes from the coast of State of Rio de

Janeiro, the same parasite was found with

lower prevalence, P = 2% in Balistes capriscus

Gmelin, 1789; P = 6% in Aluterus monoceros

(Linnaeus, 1758), and P = 6% in

Scomberomorus cavalla (Cuvier, 1829) (Dias

et al., 2009, 2010, 2011). In the present study

larvae were collected in the mesentery and

intestine and ovarian serosas, differently Lima

(2004) which previously reported this species

parasitizing P. arenatus found it only in the

mesentery; and in other teleostean hosts

collected from the State of Rio de Janeiro, C.

speciosus were found in the mesentery (Dias et

al., 2009, 2010, 2011), and in the liver (Dias et

al., 2010). Therefore, suggesting that future

seasonal studies need to be make aiming to

establish the parasitic indices of this host and

the role of P. arenatus as one of the

intermediate hosts of C. speciosus.

This study was limited to research due some

papers had no complete information about

parasitary indices and sites of infection.

In the present study the prevalence and mean

intensity of C. speciosus in P. arenatus were

low and was not found infecting the

musculature, however this trypanorhynch

species gave a repugnant aspect to the fish,

considering the large size of the blastocyst. We

suggest that studies be done to set up his

allergenic potential.

The authors would like to thank Heloisa Maria

Nogueira Diniz (Serviço de Produção e

Tratamento de Imagens do IOC) for processing

the plate of figures; the Conselho Nacional de

Desenvolvimento Científico e Tecnológico

(CNPq) and Coordenação de Aperfeiçoamento

de Pessoal de Nível Superior (CAPES) for

partial financial supports.

ACKNOWLEDGMENTS

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