Suggested citation: Felizardo, N.N.; Knoff, M.; Pinto, R.M.; Gomes, D.C. Larval anisakid nematodes of the flounder,

Paralichthys isosceles Jordan, 1890 (Pisces: Teleostei) from Brazil. Neotropical Helmintology, vol. 3,n

2,pp.57-64.

Key words: Anisakidae larvae – Brazil - flounder - Paralichthys isosceles - zoonotic potential.

Abstract

Between October 2006 and March 2008, 60 specimens of Paralichthys isosceles were captured in the littoral of the

State of Rio de Janeiro, Brazil, to be investigated for anisakid nematodes, due to their zoonotic relevance. Five

species of larval anisakid were present, in a total amount of 1,900 worms. One thousand eighty hundred and twenty

larvae of Hysterothylacium sp., 71 of Raphidascaris sp., four of Terranova sp., three of Anisakis simplex and two

of Contracaecum sp. were recovered. Parasites were found infecting the abdominal cavity, mesentery, intestine,

liver, stomach mucosa, stomach, ovaries, abdominal musculature, and serosas of the heart, spleen, stomach,

kidneys and ovaries. Hysterothylacium sp. appeared with a prevalence (P) of 100%, mean intensity (MI) of 30.3,

range of infection (RI) of 1 to 596 and mean abundance (MA) of 30.3; Raphidascaris sp. with P = 36.7%, MI = 3.2,

RI = 1 to 29 and MA = 1.18; Anisakis simplex with P = 5%, intensity (I) = 1 and MA = 0.05; Terranova sp. with P =

5%, MI = 1.3, RI = 1 to 2 and MA = 0.07; Contracaecum sp. with P = 3.3% I = 1 and MA = 0.03. This is the first

report of parasitological indexes and sites of infection related to larval A. simplex, Contracaecum sp., Terranova

sp., Hysterothylacium sp. and Raphidascaris sp. in Paralichthys isosceles. Larvae are described and illustrated.

Paralichthys isosceles is a new host record for larvae of Anisakis simplex and Hysterothylacium sp.

Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz-Fiocruz.

CNPq research fellows.

Neotrop. Helminthol., 3(2), 2009

2009 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

LARVAL ANISAKID NEMATODES OF THE FLOUNDER,

PARALICHTHYS ISOSCELES JORDAN, 1890 (PISCES: TELEOSTEI) FROM BRAZIL

NEMÁTODOS ANISAKIDOS LARVARIOS DEL LENGUADO

PARALICHTHYS ISOSCELES JORDAN, 1890 (PISCES: TELEOSTEI) EN BRASIL

1 1 1,2 1,2,*

Nilza Nunes Felizardo ; Marcelo Knoff ; Roberto Magalhães Pinto & Delir Corrêa Gomes

ORIGINAL ARTICLES/ ARTICULOS ORIGINALES

Resumen

Palabras clave: larva de Anisakidae - lenguado - Paralichthys isosceles - importancia en zoonosis - Brasil.

Desde Octubre hasta Marzo, 2006, 60 ejemplares de Paralichthys isosceles fueron colectados en el litoral del

Estado do Rio de Janeiro, Brasil, con el objetivo de hacer un inventario de nematodos anisákidos considerando su

importancia en las zoonosis. Cinco especies larvales son representadas con un total de 1.900 parásitos, siendo

1.850 muestras de Hysterothylacium sp., 71 de Raphidascaris sp., cuatro of Terranova sp., tres de Anisakis

simplex y dos de Contracaecum sp. Los parásitos fueron encontrados en la cavidad abdominal, mesenterio,

intestino, hígado, mucosa estomacal, estomago, ovarios, musculatura abdominal, y en las serosas del corazón,

bazo, estomago, riñones y ovarios. Larvas de Hysterothylacium sp. aparecieron con una prevalencia (P) de 100%,

intensidad media (MI) de 30,3, amplitud de intensidad (RI) de 1 a 596 y abundancia media (MA) de 32,

Raphidascaris sp. con P = 39%, MI = 3,2, RI = 1 a 29 y MA= 1,2, Anisakis simplex con P = 5%, Intensidad (I) = 1

y MA= 0,06, Terranova sp. con P = 5%, (I) = 1 y MA= 0,05, Contracaecum sp. con P = 3,0%, I =1 y MA = 0,03. Este

es el primero reporte de índices parasitarios y sitios de infección de larvas de A. simplex, Contracaecum sp.

Terranova sp., Hysterothylacium sp. y Raphidascaris sp. en Paralichthys isosceles que es un nuevo registro de

hospedero para larvas de Anisakis simplex y Hysterothylacium sp.

INTRODUCTION

The anisakid nematodes can be transmitted to man

and fishes act as intermediate, paratenic or definitive

hosts for these helminths (Anderson, 2000). Third

stage larvae remains infective for over three years

(Lopez Sabater & Lopez Sabater, 2000), and are

considered in public health approaches, as a

potential risk factor when ingested (Roepstorff et

al., 1993).

Species of flounders included in Paralichthyidae

occurring in the Brazilian coast and allocated under

Paralichthys Girard 1858, represent one of the most

outstanding fishery resources in Brazil (Figueiredo

& Menezes, 2000), being largely utilized in the

internal and external markets.

The present investigation aimed at the identification

of larval anisakid worms recovered from

specimens of Paralichthys isosceles Jordan, 1890 in

the littoral of the State of Rio de Janeiro, Brazil, with

data on taxonomy, parasitological indexes and

infection sites.

From October 2006 to March 2008, sixty specimens

of Paralichthys isosceles Jordan, 1890, measuring

35.0±5.9 cm and weighting 625±25.2 g, were

captured in the littoral of the State of Rio de Janeiro,

Brazil (21º15'S-23º23'S, 40º29'W-44º28'W) to be

further investigated for helminths. Fishes were

maintained in isothermal boxes with ice and carried

to the Laboratory of Helminth Parasites of

Vertebrates, Oswaldo Cruz Institute, Oswaldo Cruz

Foundation, Rio de Janeiro.

Identification of specimens was obtained in

accordance with Figueiredo & Menezes (2000).

Nematodes were collected, fixed, clarified and

preserved according to Eiras et al. (2006). To better

understand the structure of the lateral alae in

specimens of Hysterothylacium sp. and

Raphidascaris sp., transversal sections at the level

of the esophagus were obtained by means of the

techniques after Anderson (1958), and Esser (1986).

The study of the buccal structures was made on the

basis of the method of Moravec (1998). The adopted

taxonomic classification of the Anisakidae follows

Hartwich (1974) and larval identification was

obtained after Rego et al. (1983), Smith (1984),

Peter & Maillard (1988), Incorvaia & Díaz de

Astarloa (1998), Timi et al. (2001) and Bicudo et al.

(2005). Figures were made by means of a drawing

tube connected to a Olympus BX41 brightfield

microscope. Measurements ranges are in

millimeters (mm) with means in parentheses (Table

1). Parasitological indexes related to prevalence (P),

intensity (I), mean intensity (MI), range of infection

(RI) and mean abundance (MA), are in accordance

with Bush et al. (1997). Representative specimens

were deposited in the Helminthological Collection

of the Oswaldo Cruz Institute (CHIOC).

Comparison of species of Anisakis, Contracaecum,

Terranova, Hysterothylacium and Raphidascaris,

presently studied, was made with those previously

reported by Rego et al. (1983) and Bicudo et al.

(2005), also obtained from fishes of the Brazilian

littoral and that are deposited in the CHIOC nos.

31945 a-b, 31946 a-b, 31947 a-b, 31948 a-b, 35351,

35352 and 35353.

The 60 investigated fishes were parasitized with

anisakid larvae (prevalence = 100%), in a total

amount of 1,900 free or encapsulated larvae. One

thousand-eight hundred and twenty larvae

represented L3 and L4 larval stages of

Hysterothylacium sp., 71 of Raphidascaris sp., four

of Terranova sp., three of Anisakis simplex, and two

of Contracaecum sp. (Table 1). Parasitological

indexes, infection sites and CHIOC deposit numbers

are depicted in Table 2.

Anisakinae Railliet & Henry, 1912

Anisakis Dujardin, 1845

Anisakis simplex (Rudolphi, 1809) (Figs. 1 and 2)

Description based on three third-stage larvae:

cuticle with thin transversal striation. Anterior

extremity with a dorsal and two poorly developed

ventro-lateral lips. Six cephalic papillae, one pair in

the dorsal lip and a pair in each ventro-lateral lip.

Boring tooth below the oral aperture, between the

two ventro-lateral lips. Excretory pore opening

beneath the boring tooth. Deirids inconspicuous.

Ventriculus longer than large. Ventricular appendix

and intestinal cecum absent. Two nearly spherical

rectal glands. Tail conical, mucron present.

MATERIAL AND METHODS

Felizardo et al.

RESULTS

Nematodes of the flounder

Contracaecum Railliet & Henry, 1912

Contracaecum sp. (Figs. 3 and 4).

Description based on two third-stage larvae: cuticle

with thin transversal striation, more evident in the

posterior extremity of the body. Anterior extremity

with a dorsal lip and two poorly developed ventro-

lateral lips. Six cephalic papillae, one pair in the

dorsal lip and a pair in each ventro-lateral lip. Boring

tooth near the oral aperture, between the two ventro-

lateral lips. Excretory pore opening beneath the

boring tooth. Deirids inconspicuous. Ventriculus

small and sub spherical. Ventricular appendix nearly

twice longer than the intestinal cecum. Two almost

spherical rectal glands. Tail conical, mucron absent.

Terranova Leiper & Atkinson, 1914

Terranova sp. (Figs. 5 and 6).

Description based on four third-stage larvae: cuticle

with thin transversal striation more evident in the

posterior extremity of the body. Anterior extremity

with a dorsal and two poorly developed ventro-

lateral lips. Six cephalic papillae, one pair in the

dorsal lip and a pair in each ventro-lateral lip. Boring

tooth below the oral aperture, between the two

ventro-lateral lips. Excretory pore opening beneath

the boring tooth. Deirids inconspicuous. Ventriculus

longer than large. Ventricular appendix absent.

Intestinal cecum twice the length of the ventriculus.

Two nearly spherical rectal glands. Tail conical,

mucron absent.

Raphidascaridinae Hartwich, 1954

Hysterothylacium Ward & Margath, 1917

Hysterothylacium sp. (Figs. 7-10).

Description based on 54 third-stage larvae; cuticle

with lateral alae extending along the body with a

wedge-shaped support, devoid of basal extension.

Anterior extremity with a dorsal and two poorly

developed ventro-lateral lips.Nine cephalic

papillae, two pairs in the dorsal lip together with a

large papilla and a pair in each ventro-lateral lip.

Boring tooth absent. Excretory pore opening below

the nerve ring. Ventriculus nearly spherical.

Ventricular appendix twice longer than the

esophagus. Intestinal cecum present. Four sub-

spherical rectal glands. Tail conical, mucron

present.

Description based on 50 four-stage larvae:

morphological characteristics similar to those

present in third-stage larvae were observed, except

for the more developed lips and the presence of a

caudal multispinous process responsible for the

cactus-tail format in the former.

Raphidascaris Railliet & Henry, 1915

Raphidascaris sp. (Figs. 11-13)

Description based on ten third-stage larvae: cuticle

smooth, devoid of striations. Lateral alae extending

along the body. Poor developed lips. Ventral boring

tooth present. Ventriculus larger than long.

Ventricular appendix present. Intestinal cecum

absent. Excretory pore below the nerve ring. Two

rectal glands nearly spherical. Tail pointed with well

defined transversal striations in the terminal portion.

Larvae of Anisakis recovered from Paralichthys

isosceles were identified to A. simplex, taking into

account the defined morphological characteristics

of the species, in accordance with Timi et al. (2001).

Some differences were related to the wider range

observed in the length of the worms in comparison

with those reported by Timi et al. (2001) in

Engraulis anchoita Hubbs & Marini, 1935, Anisakis

(type I) in P. patagonicus Jordan, 1889 by Incorvaia

& Diaz de Astarloa (1998) in Argentina, Anisakis sp.

in Pomatomus saltatrix (L.) by Rego et al. (1983), in

Trichiurus lepturus L. by Barros & Amato (1993)

and in Prionotus punctatus (Bloch, 1793) by Bicudo

et al. (2005) captured in the Brazilian coast. Bicudo

et al. (2005) affirmed that the measurements so far

obtained were close to those reported for A. simplex

by Smith (1983) in euphausiids, differing from them

by the smaller proportion related to body and

esophagus length.

Data on larvae of Contracaecum sp. presently

studied are in accordance with those reported by

Rego et al. (1983), when larvae were recovered from

specimens of Pomatomus saltatrix, from Engraulis

anchoita by Timi et al. (2001) and Contracaecum

sp. (type B) from P. patagonicus and from P.

orbignyanus (Valenciennes, 1839) by Incorvaia &

Diaz de Astarloa (1998). Tavares and Luque (2006)

listed Contracaecum sp. larvae parasitizing several

teleosteans, including P. isosceles from the

Brazilian littoral.

Larvae identified as Terranova sp., are similar to

those described by Rego et al. (1983) from P.

saltatrix in Brazil and by Timi et al. (2001) from

Engraulis anchoita in Argentina and Uruguay.

They differ from Terranova type HB in Carangidae

hosts reported by Deardorff et al. (1982) since these

larvae present bigger ventriculus and intestinal

DISCUSSION

Neotrop. Helminthol., 3(2), 2009

cecum, from Terranova sp. by Rego et al. (1985)

recovered from specimens of Pagrus pagrus L., by

the absence of mucron, and from Terranova type B

that present larger ventriculus and that were reported

by Incorvaia & Díaz de Astarloa (1998) parasitizing

specimens of P. orbignyanus and P. patagonicus.

Terranova sp. larvae were referred in several marine

teleosteans in Brazil by Eiras & Rego, (1987) and

Tavares & Luque (2006).

Third-stage larvae of Hysterothylacium sp. found in

s p e c i m e n s o f P. i s o s c e l e s r e s e m b l e

Hysterothylacium sp. no. 2 of Petter & Maillard

(1988) from Mullus surmuletus (L.), Muraena

Helena L. and Trachinus araneus Cuvier, 1825, in

the Mediterranean sea, Hysterothylacium MD of

Deardorff & Overstreet (1981) collected in

Scomberomorus maculatus (Mitchill, 1815) from

the Northern Gulf of Mexico, Hysterothylacium KB

in Mene maculata (Bloch & Schneider, 1801),

Mulloidichthys auriflamma (Forsskal, 1775),

Otolithes argenteus Cuvier, 1830, Pseudorhombus

arsius (Hamilton, 1822), Sphyraena jello Cuvier,

1829, Sphyraena obtusata Cuvier, 1829 and

Upeneus sulphureus Cuvier, 1829 from Kuwait by

Petter & Sey (1997). These larvae are also similar to

those reported in Brazil, previously identified as

Hysterothylacium MD in Micropogonias furnieri

(Desmarest, 1823) by Pereira Jr. et al. (2004) and

Hysterothylacium sp. in P. punctatus by Bicudo et

al. (2005). Revising the samples that were deposited

in the CHIOC by the latter authors, it became

evident that the larval tooth is absent in the

examined larvae and that the specimens present, in

fact, a prominent lip papilla. Moreover, third-stage

larvae recovered from P. isosceles present the lateral

alae with the wedge-shaped support and conical tail

with mucron, identical to the observed in

Hysterothylacium MD of Deardorff & Overstreet

(1981). These larvae differ from those of two species

that occur in fishes of the Brazilian littoral: H.

fortalezae (Klein, 1973) in which the support of the

lateral alae is T-shaped and tail ends in an

agglomerate of six spines and H. reliquens (Norris &

Overstreet, 1975) in which the lateral alae and the

multispinous structure in the tail are absent

(Deardorff & Overstreet, 1980); besides, larvae of

both species present larval tooth during the third-

stage (Deardorff & Overstreet, 1981).

Fourth-stage larvae are similar to Hysterothylacium

sp. no. 2 of Petter & Maillard (1988) collected in

several teleosteans from the Mediterranean and to

Hysterothylacium MD of Deardorff & Overstreet

(1981) in Mugil cephalus L. from the Gulf of

Mexico.

Third-stage larvae of Raphidascaris sp. studied

now, are similar to those of Rego et al. (1983) in

Pomatomus saltatrix L. from the Brazilian littoral

and to R. acus (Bloch, 1772) in Perca flavescens

(Mitchill, 1814) collected by Smith (1984) in

Canada, by presenting lateral alae. Nevertheless,

they differ from the larvae collected in Prionotus

punctatus from the Brazilian coast by Bicudo et al.

(2005) since these larvae are devoid of lateral alae.

Tavares & Luque (2006) report the distribution of

Raphidascaris sp. larvae found parasitizing 31

species of teleostean hosts in Brazil, reinforcing the

importance of these occurrences.

Timi et al. (2001), affirm that morphometric

differences observed in specimens of a same species

may occur due to the individual allometric

development and also in accordance with Koie

(1993) that the spatial confinement the first

intermediate hosts (crustaceans and mollusks) are

submitted can interfere in the size of the larvae

parasitizing the fishes.

Five species included in Paralichthys, were

investigated for larval anisakid in the North and

South America: P. californicus (Ayres, 1859) by

Castillo-Sanches et al. (1998), P. adspersus

(Steindachner, 1867) by Oliva et al. (1996), P.

patagonicus and P. orbignyanus by Incorvaia &

Díaz de Astarloa (1998) and P. microps (Günther,

1881) by Torres et al. (2000), when some

parasitological indexes and infection sites were

reported. In Chile, Anisakis simplex in specimens of

P. microps, appeared with a prevalence 10% higher

than the presently reported for P. isosceles.

Moreover, former data refer to liver and ovaries

found parasitized with A. simplex. The anisakid

nematodes were present in all specimens of

flounders from South and North Americas, with a

higher mean abundance than the observed here and

also occurring in the stomach and intestinal cecum.

In Argentina, references to Terranova sp. are related

to three species (Types A, B, B') in P. patagonicus

and P. orbignyanus occurring with higher mean

abundance when compared to the obtained in P.

isosceles. Nevertheless, Terranova (Type A)

appeared with a mean abundance of 0.08 similar to

the values presently observed in despite of the

difference related to other three infection sites

reported now. For Hysterothylacium sp. parasitizing

P. isosceles in Brazil, values referring to prevalence,

mean intensity and mean abundance were higher

Nematodes of the flounder

Felizardo et al.

than those reported for other investigated flounders

from South and North Americas. For Raphidascaris

sp. recovered from P. patagonicus the mean

abundance of the parasitism was of 4.8 when

compared to 1.18 in P. isosceles also occurring in

other four sites of infection, since previous reports

only refer to the intestinal cecum.On the basis of the

present results, the high infection levels, mainly

considering the larvae of Hysterothylacium sp., as

well as the infection sites, such as musculature and

ovaries (Table 2) indicate a major importance, since

the larvae, of zoonotic potential, when accidentally

ingested can infect man, in accordance with data

Neotrop. Helminthol., 3(1), 2009

after Yagi et al. (1996) that referred to a case of

human anisakidosis in Japan, caused by the

ingestion of raw fish parasitized with larval

Hysterothylacium aduncum (Rudolphi, 1802).

To Flávia de Carvalho, Communication Service

(ICICT/Fiocruz) and Heloisa Nogueira Diniz,

Images Production and Treatment Service

(IOC/Fiocruz), for processing the figures.

Table 1. Morphological and morphometric data on third stage larval anisakid in Paralichthys isosceles from the littoral of the

State of Rio de Janeiro, Brazil.

Anisakis simplex Contracaecum sp. Terranova sp. Hysterothylacium sp. Raphidascaris sp.

Length 15.3 – 16.0 (15.6) 4.88 – 5.06 (4.97) 5.63 – 7.75 (6.13) 3.62 – 16.7 (10.1) 6.85 – 11.5 (9.17)

Width 0..35 – 0.37 (0.36) 0..9 – 0.22 (0.20) 0.16 – 0.18 (0.17) 0.11– 0.40 (0.25) 0.28 – 0.31 (29.5)

Larval tooth present present present absent present

Escretory pore* opens beneath

boring tooth

opens beneath

boring tooth

opens beneath

boring tooth

0.25 – 0.46 (0.36) 0.27 – 0.42 (0.36)

Nerve ring* 0.26 – 0.28 (0.27) 0.14 – 0.18 (0.16) 0.11– 0.22 (0.17) 0.12 – 0.46 (0.29) 0.12 – 0.28 (0.20)

Esophagus 1.53 –1.62 (1.57) 0.64 – 0.70 (0.67) 0.78 – 1.20 (0.99) 0.23 – 1.16 (0.69) 0.57 – 0.93 (0.85)

Ventriculus

0.55 – 0.60 (0.55)

0.22 – 0.25 (0.22)

0.03 – 0.09 (0.06)

0.04 – 0.10 (0.07)

0.36 – 0.41 (0.39)

0.15 – 0.17 (0.16)

0.04 – 0.19 (0.12)

0.05 – 0.15 (0.10)

0.05 – 0.10 (0.06)

0.08 – 0.15 (0.12)

Vap absent 0.42 – 0.50 (0.46) absent 0.35 – 1.37 (0.86) 0.28 – 0.80 (0.48)

Intestinal cecum absent 0.28 – 0.33 (0.30) 0.35 – 0.36 (0.35) 0.05 – 0.32 (0.18) absent

Tail 0.07 – 0.08 (0.08) 0.14 – 0.17 (0.15) 0.23 – 0.25 (0.24) 0.10 – 0.32 (0.20) 0.13 – 0.34 (0.25)

Mucron 0.02 – 0.03 (0.02) absent absent 0.03 – 0.08 (0.05) absent

*From anterior end; Vap - ventricular appendix

Table 2. Prevalence (P), intensity (I), mean intensity (MI), range of infection (RI), mean abundance (MA), infection sites (IS) and

deposit numbers in the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC) of larval anisakids parasitizing

specimens of Paralichthys isosceles from the littoral of the State of Rio de Janeiro, Brazil.

(%)

I* / MI RI MA IS CHIOC

No.

Hysterothylacium sp.

100

30.3

1-596

30.3

AC, AM, IN, HS, KS, LS, M,

O, OS, S, SM, SS

35642

Raphidascaris sp.

36.7

3.2

1-29

1.18

AC, IN, L, S, STS

35643

Anisakis simplex

0.05

AC, IN, STS

35644

Terranova sp.

5 1.3 1-2 0.07 L, IN, M, SM 35646

Contracaecum sp.

3.3 1* - 0.03 IN 35645

ACKNOWLEDGEMENTS

AC-Abdominal cavity; AM-abdominal musculature; IN-intestine; HS- heart serosa; KS- kidney serosa; L-liver; LS-liver serosa; M-

mesentery; O-ovary; OS-ovary serosa; S-stomach; SM-stomach mucosa; SS-spleen serosa; STS-stomach serosa

Figures 7-13. Third

stage anisakid larvae.

Hysterothylacium sp.

Fig. 7. Anterior portion.

Fig. 8. Posterior end.

Fig. 9 Posterior end of a

t h i r d - s t a g e lar v a ,

containing a four-stage

molt, with a caudal

multi-spinous structure.

Fig. 10. Cross section at

t h e m i d d l e o f

esophagus, lateral alae

with a wedge-shaped

support. Raphidascaris

sp. Fig. 11. Anterior

p o r t i o n . F i g . 1 2 .

Posterior end. Fig. 13.

Cross section at the

middle of esophagus.

Scale bars: Figs. 7-8,

11-12 = 0.2 mm; Fig. 9

= 0.025 mm; Fig. 10 =

0.1 mm; Fig. 13 = 0.05

mm.

Nematodes of the flounder

Felizardo et al.

Figures 1-6 Third stage anisakid larvae. Anisakis simplex. Fig. 1. Anterior portion.

Fig. 2. Posterior end. Contracaecum sp. Fig. 3. Anterior portion. Fig. 4. Posterior

end. Terranova sp. Fig. 5. Anterior portion. Fig. 6. Posterior end. Scale bars: Figs. 1-4

= 0.2 mm; Figs. 5-6 = 0.1mm.

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