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Acta Scientiarum 

 

 

http://www.uem.br/acta 
ISSN printed: 1679-9283 
ISSN on-line: 1807-863X 
Doi: 10.4025/actascibiolsci.v39i3.35615 

 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 389-395, July-Sept., 2017 

Detection of Anisakidae larvae parasitizing Plagioscion 
squamosissimus
 and Pellona castelnaeana in the State of Pará, Brazil  

Núbia Lorena Farias Rabelo

1

, Thatyana Cristina Muniz e Silva

1

, Laudemir Roberto Ferreira 

Araujo

1

, Raul Henrique da Silva Pinheiro

2

 and Carlos Alberto Machado da Rocha

3*

 

1

Coordenação de Ciências Biológicas, Instituto Federal de Educação, Ciência e Tecnologia do Pará, Belém, Pará, Brazil. 

2

Instituto 

Socioambiental e dos Recursos Hídricos, Universidade Federal Rural da Amazônia, Belém, Pará, Brazil. 

3

Coordenação de Recursos Pesqueiros, 

Instituto Federal de Educação, Ciência e Tecnologia do Pará, Av. Almirante Barroso, 1155, 66093-020, Belém, Pará, Brazil. *Author for 
correspondence. E-mail: carlos.rocha@ifpa.edu.br  

ABSTRACT. Five specimens of Plagioscion squamosissimus from Xingu River and ten specimens of Pellona 

castelnaeana from Mosqueiro Island, both in the State of Pará, Brazil, were examined to investigate the 
presence of anisakid nematodes, due to their zoonotic potential. Their parasitism indices and sites of 
infection were also determined. This is the first record of Anisakidae parasitizing Pellona castelnaeana. Four-
hundred and eighty-four third-stage larvae (L

3

) of Anisakidae were found, of which 42 were found in P. 

squamosissimus and 442 in P. castelnaeana. The parasitism indices of the anisakid collected from the P. 
squamosissimus
 comprised prevalence (P) of 100%, mean infection intensity (MI) of 8.4, range of infection 
(RI) of 1-13, mean abundance (MA) of 8.4, and infection site (IS) in the abdominal cavity. P. castelnaeana 
showed P = 100%, MI = 44.2, RI = 10-114, MA = 44.2, and IS = abdominal cavity, cecum and stomach. 
The life cycle of these nematodes can be completed in the Amazon basin, since the two hosts fish are part 
of the cetacean diet of the region, which participate as final hosts. These findings have an important 
consequence on epidemiology of anisakiasis, so attention should be extended to human protection against 
this public health risk.

 

Keywords: freshwater fish, zoonosis, Anisakidae, Amazon basin. 

Detecção de larvas de Anisakidae parasitando Plagioscion squamosissimus Pellona 
castelnaeana 
no Estado do Pará, Brasil 

RESUMO. Cinco espécimes de Plagioscion squamosissimus do rio Xingu e dez espécimes de Pellona 
castelnaeana  
da Ilha do Mosqueiro, ambos no Estado do Pará, Brasil, foram examinados para investigar a 
presença de nematodas Anisakidae, devido ao seu potencial zoonótico. Também foram determinados seus 
índices de parasitismo e sítios de infestação. Esse é o primeiro registro de Anisakidae parasitando Pellona 
castelnaeana
. Foram encontradas 484 larvas de Anisakidae de terceiro estágio (L

3

), sendo 42 em P. 

squamosissimus e 442 em P. castelnaeana. Os índices parasitários de anisaquídeos coletados de P. squamosissimus 
compreenderam prevalência (P) de 100%, intensidade de infecção média (IM) de 8.4, amplitude de 
infecção (AI) de 1-13, abundância média (AM) de 8,4 e local de infecção (LI) na cavidade abdominal. P. 
castelnaeana
 apresentou P = 100%, IM = 44,2, AI = 10-114, AM = 44,2 e LI = cavidade abdominal, ceco e 
estômago. O ciclo de vida desses nematodas pode ser completo na bacia Amazônica, já que os dois 
hospedeiros fazem parte da dieta de cetáceos da região, que atuam como hospedeiros finais. Esses achados 
têm consequência importante na epidemiologia de anisaquíases, devendo haver mais atenção em relação à 
proteção humana contra esse problema de saúde pública. 

Palavras-chave: peixes de água doce, zoonoses, Anisakidae, Bacia Amazônica. 

Introduction 

The presence of parasites in fish is relatively 

frequent and has many consequences related mainly 
with economic and health aspects. Some parasites 
generate high mortality in fish and also cause tissue 
damage leading to economic loss (Ferre, 2001). Like 
other vertebrate hosts, fish have their own parasitic 
fauna  with  numerous  parasitic  species  distributed 

and classified in major taxonomic groups (Luque, 

2004). The fauna of freshwater parasites may have 

different compositions, depending on the host 

species, trophic level occupied by the host, age, size, 

sex, and other biotic and abiotic factors. Moreover, 

the fish can harbor adult worms and their larvae 

(Takemoto, Lizama, Guidelli, & Pavanelli, 2004). 

Nematodes might occur in fish, both in adult 

and larval forms. Larvae are frequently found 

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390 

Rabelo et al. 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 389-395, July-Sept., 2017 

encysted in the muscles, liver, visceral surfaces and 
cavities, intestines and, rarely, in the integument 

(Dick & Choudhury, 1995). Its life cycle is 

heteroxenic and complex; moreover, six stages of 

development are recognized: egg, four larval stages, 

and adulthood. Generally, the cycle involves 

intermediate hosts, sometimes paratenic hosts. In 

adulthood, the site of infection is, for most species, 

the gastrointestinal tract (Takemoto et al., 2004). 

Included in the Phylum Nematoda, the family 

Anisakidae contains 24 genera and its representatives 

have great zoonotic potential (Martins, Onaka, & 

Fenerick, 2005; Fontenelle, Knoff, Felizardo, Lopes, 

& São Clemente, 2013). In the larval stage, 

nematodes of this family are common parasites of 

fishes, cephalopods and prawns while the adults are 

parasites of fish, reptiles, birds and mammals 

(Moravec, 1998; Klimpel & Palm, 2011). Accidental 

ingestion of these larvae by humans can cause the 

gastrointestinal infection, anisakiasis, and a series of 

allergic reactions. However, in Brazil, there is a lack 

of information about the anisakiasis (Iñiguez, 

Carvalho, Motta, Pinheiro, & Vicente, 2011). A 

single case of anisakiasis has been reported in Brazil, 

in a man in the State of Mato Grosso, with the larvae 

located in the mucosa of the duodenum (Cruz, 

Souto, Ferrari, Allegretti, & Arrais-Silva, 2010). 

Plagioscions quamosissimus (Heckel, 1840) 

commonly called “corvina” or “pescada branca”, is a 

sciaenid fish mainly found in large rivers and 

constitute an important resource for commercial 

and sport fishing (Casatti, 2003). This species is a 

carnivorous freshwater fish restricted to South 

America and originally from the Amazon basin with 

a wide distribution in Brazil (Rocha et al., 2016). 

Pellona castelnaeana Valenciennes, 1847, commonly 

called “apapá amarelo” or “sarda”, is considered the 

largest sardine of South America, and one of the largest 

species known from the order Clupeiformes (Queiroz 

et. al., 2013). It is a piscivorous species, inhabit lakes 

and rivers and can also be found in flooded forest. 

Pellona castelnaeana is a pelagic migratory species, with 

full spawn and external fertilization (Freitas & 

Siqueira-Souza, 2009). 

The present study aimed to report the presence of 

larval stages of anisakid nematodes in Plagioscion 

squamosissimus from Xingu River, near the municipality 

of Altamira, and Pellona castelnaeana from Mosqueiro 

Island, in the municipality of Belém, both in the State 

of Pará, Brazil, and to determine their parasitism 

indices and infection sites.  

Material and methods 

Between September and October 2013, five 

specimens of the fish species P. squamosissimus (with 

46.8 ± 4.9 cm mean length and 437.60 ± 57.17 g 
mean weight) were purchased in Xingu River near 

Altamira (coordinates: 3° 12′ S and 52° 12′ W), Pará, 

Brazil. Between May and July 2015, ten specimens 

of the fish species P. castelnaeana (with 45.36 ± 4.79 

cm mean length and 779.72 ± 317.80 g mean 

weight) were purchased in warehouse fishing 

“Cajueiro”, located on the Mosqueiro Island 

(coordinates: 1º 10’ S and 48º 28’ W), Pará, Brazil. 

Fishes were transported in isothermal boxes with 

ice to the Laboratory of Histology and Embryology, 

Institute of Animal Health and Production, 

Universidade Federal Rural da Amazonia, Belém, State 

of Pará, Brazil, and identified in accordance with 

Reis, Kullander, & Ferraris (2003). The content of 

the visceral cavity was separated in Petri dishes with 

physiological saline for parasitological analysis as 

described by Fontenelle et al. (2015). 

Anisakidae larvae were fixed in AFA and stored 

in glycerin-alcohol in proportion 1:1 and examined 

with the aid of a magnifying glass. The material was 

cleaned and clarified with Amman’s lactophenol, as 

described by Knoff and Gomes (2012). Posteriorly, 

the parasites were placed between two glass slides 

and observed under an Olympus CX41 light 

microscope. 

The taxonomic classification of nematode larvae 

was made in accordance with Moravec (1998) and 

Fontenelle et al. (2013). The parasitism indices of 

prevalence, mean intensity and mean abundance 

were obtained as described by Bush, Lafferty, Lotz, 
and Shostak (1997). 

Morphometrical analysis was performed on ten 

larval samples obtained from Pellona castelnaeana. 

stereomicroscope Leica DM 2500 coupled with a 

camera lucida was used. For topographic 

characterization of the cuticular surface, the material 

was processed as described by Giese, Furtado, 

Lanfredi, and Santos (2010): third-stage larvae were 

washed in phosphate-buffered saline (pH 7.0), post-

fixed in 1% osmium tetroxide, dehydrated to the 

CO

critical point, metalized with gold-palladium, 

and analyzed with a scanning electron microscope 

VEGA 3 LMU/TESCAN in the Laboratory of 

Histology and Animal Embryology at the Institute of 

Animal Health and Production, Universidade Federal 

Rural da Amazônia (UFRA), Campus Belém, State of 

Pará, Brazil. 

One exemplar of each fish species was deposited 

in the Ichthyological Collection of the Fishery and 

Agribusiness Resource Coordination of Instituto 

Federal do Pará (IFPA). The parasites found were 

deposited in the Helminthological Collection of 

Laboratory of Histology and Animal Embryology, 

UFRA, Belém, State of Pará, Brazil. 

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Anisakid in Plagioscion squamosissimus and Pellona castelnaeana 391 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 389-395, July-Sept., 2017 

Results 

All fish specimens investigated were infested 

with living third-stage larvae (L

3

) of Anisakidae 

(prevalence = 100%): five specimens of P. 
squamosissimus
 containing 42 L

3

; and ten specimens 

of  P. castelnaeana containing 442 L

3

. In both host 

species, the parasite intensity was not correlated with 
the length and weight of fish. Table 1 lists the 
prevalence (P), mean infection intensity (MI), range 
of infection intensity (RI), mean abundance (MA), 
and infection site (IS). 

Table 1. Prevalence (P), mean intensity (MI), range of infection 
(RI), mean abundance (MA), infection/infestation site (IS) and 
Identification code (IC) of anisakid third-stage larvae collected in 
Plagioscion squamosissimus from Xingu River, municipality of 
Altamira, and Pellona castelnaeana from Mosqueiro Island, 
municipality of Belém; both in the State of Pará, Brazil. 

Hosts P 

(%) 

MI 

RI 

MA 

IS 

IC 

P. squamosissimus  100  8.4 1-13 8.4  AC APVII-048

P. castelnaeana 

100 

44.2  10-114  44.2 

AC, C, S APIII-006

(AC) Abdominal Cavity, (C) Cecum, (S) Stomach. 

Measurements were taken on ten anisakid L

3

 

collected from P.  castelnaeana: body length 11.8-

15.14 (13.04 ± 1.43); body width 0.186-0.266 (0.217 

± 0.025); nerve ring 0.067-0.210 (0.164 ± 0.043); 
esophagus length 0.673-1.026 (0.867 ± 0.095); 

esophagus width 0.060-0.106 (0.080 ± 0.015); 

ventriculus length 0.266-0.433 (0.354 ± 0.057); 

ventriculus width 0.086-0.160 (0.132 ± 0.024); 

cloaca 0.060-0.210 (0.102 ± 0.047). 

 

Phylum Nematoda (Rudolphi, 1808)  

Class Secernentea von Linstow, 1905 

Subclass Rhabditia Inglis, 1983  

Order Ascaridida Skrajabin & Schulz, 1940  

Family Anisakidae Skrjabin & Karokhin, 1945 

(larvae) (Figures 1, 2) 

 

Description of the main morphological features 

observed in L

3

: cuticle with crosscutting narrow 

striations most evident on the posterior body 

portion, conical tail and mucron present (Figures 1b, 

1d, 2d); anterior end with a dorsal lip and two 

ventrolateral lips, all of them poorly developed; six 

cephalic papillae, one pair in the dorsal lip and a pair 

in each ventrolateral lip; boring tooth below the oral 

aperture, between the two ventrolateral lips; 

excretory pore opening beneath the boring tooth 

(Figures 1a, 1c, 2a, 2b, 2c). 

 

 

Figure 1. Anisakidae (L

3

) from Pellona castelnaeana observed by differential interference contrast. A and C 

-  Anterior portion showing 

esophagus (e) and boring tooth (t). B and D

 - Posterior portion showing rectal ampoule (ra) and tail with terminal mucron (m). Scale 

bars: A and B = 100 μm, C and D = 50 μm. 

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392 

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Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 389-395, July-Sept., 2017 

 

Figure 2. Anisakidae (L

3

) from Pellona castelnaeana observed by scanning electron microscopy. A, B, and C – anterior portion showing 

three lips (l), boring tooth (t) and excretory pore (ep). D - posterior portion showing striated tail with terminal mucron (m). Scale bars: A 
and B = 20 μm, C = 10 μm, and D = 50 μm. 

Discussion 

The prevalence of anisakid larvae in fish can vary 

greatly. Among the most recent studies, low 

prevalence rates were found in Selene setapinnis 

13.3% (Fontenelle et al., 2015), Sandelia capensis = 

23% (Moravec, van Rensburg, & Van As, 2016) and 

Plagioscion squamosissimus = 23.3% (Fontenelle et al., 

2016); high prevalence rates were recorded in 

Hoplias malabaricus = 100% and Hoplerythrinus 

unitaeniatus  = 80% (Martins et al., 2005), 

Dicentrarchus labrax = 95% (Bernardi et al., 2011) and 
Arapaima gigas = 98% (Andrade-Porto et al., 2015). 

In the present study, in Plagioscion squamosissimus and 

Pellona castelnaeana, the prevalence was 100%, and the 

highest average intensity and abundance values were 

observed in P. castelnaeana from the Mosqueiro 

Island (Table 1).  

Plagioscion squamosissimus showed a carnivorous 

diet with preference for fish, but also including 
prawns and insects (Odonata and Ephemeroptera) in 
areas with low fish density (Barros, Santos, 
Zanuncio, & Dergam, 2012); Pellona castelnaeana 
feeds mainly on small Characiformes and 
Perciformes, however, prawns and other aquatic 
invertebrates can be part of the diet (Freitas & 
Siqueira-Souza, 2009). Since the two host fish 
occupy the same trophic level and their specimens 
in the samples were adults, with similar sizes, the 
difference in parasite intensity is due to other biotic 
factors and most probable to seasonal changes. 

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Anisakid in Plagioscion squamosissimus and Pellona castelnaeana 393 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 389-395, July-Sept., 2017 

The life cycle stages of anisakid nematodes 

include four larval stages (L

1

–L

4

), within the eggs 

(L

1

–L

3

) and subsequently in the intermediate or 

paratenic hosts (L

3

), and as preadults (L

4

) and adults 

in the cetacean definitive hosts (Klimpel & Palm, 

2011). In the present study, Anisakidae larvae were 

collected in two municipalities, Altamira and Belém, 

in the Amazon hydrographic basin. The presence of 

third-stage larvae (L

3

) of Anisakidae parasitizing 

Plagioscion squamosissimus and Pellona castelnaeana 

suggests the participation of these fish as 

intermediate or paratenic hosts in said area. 

The final hosts of Anisakidae in the Amazon 

basin are cetaceans widely distributed in the fluvial 

waters of the region, particularly the tucuxi dolphin 

(Sotalia fluviatilis) and the pink river dolphin (Inia 

geoffrensis). 

Sotalia fluviatilis is endemic to the Amazon basin, 

with records for almost all major tributaries, lakes 

and smaller rivers. Essentially piscivorous, it feeds 

mainly on pelagic fish that form shoals, with a 

maximum length of 37 cm. Plagioscion squamosissimus 

is the species most consumed by S. fluviatilis in 

Central Amazon and also appears among the most 

consumed in the Amazonian Estuary (Beltrán-

Pedreros & Pantoja, 2006; Rosas, Marigo, Laeta, & 

Rossi-Santos, 2010). In addition, Borobia and Barros 

(1989) mentioned fish of the genus Pellona among 

the species predated by the tucuxi. Inia geoffrensis

essentially fluvial, is the largest river dolphin, being 

endemic to the Amazon and Orinoco river basins. 
Adult females and pups occupy flooded areas, while 

adult males prefer to feed on the river channels. 

This piscivorous species uses dozens of fish species 

in their diet, although there are records of ingestion 

of crabs and turtles (Rocha-Campos, Câmara, & 

Pretto, 2010). Plagioscion spp. and Pellona spp. appear 

among the food items of the pink river dolphin 

(Best & da Silva, 1993). 

Anisakid L

3

 collected from P. castelnaeana were 

morphometrically similar to those collected by 

Fontenelle et al. (2016) in P. squamosissimus from the 

State of Pará (12.90 length x 0.33 width). 

Notwithstanding, they showed larger body size than 

the ones collected by Andrade-Porto et al. (2015) in 

Arapaima gigas from the State of Amazonas (2.53 

length x 0.10 width) and smaller than the ones 

collected by Felizardo, Knoff, Pinto, and Gomes 

(2009) in Paralichthys isosceles from the State of Rio de 

Janeiro (15.60 length x 0.36 width), Fontenelle et al. 

(2013) in Cynoscion guatucupa from the State of Rio 

de Janeiro (22.33 length x 0.44 width) and Moravec 

et al. (2016) in Sandelia capensis (32.48 length x 1.39 

width) from South Africa. These larvae may be 

different anisakid species. Besides that, according to 

Fontenelle et al. (2016), it is possible that these 
differences in length and width of Anisakidae larvae 

are also related to different hosts or the influences of 

the different ecoregions in which the fish examined 

were collected. 

Vanzolini (2004) reports that some species of the 

family Anisakidae were described from specimens 

collected in Sotalia fluviatilis and Inia geoffrensis from 

the Brazilian Amazon, yet in the 19

th

 century. 

Therefore, the life cycle of these nematodes can be 

completed in the Amazon basin, since their 

biodiversity houses cetaceans that participate as final 

hosts, as well as fish (Plagioscion squamosissimus and 

Pellona castelnaeana, in the present study) that can 

host larvae (L

3

) until they are predated by the 

dolphins. 

Conclusion 

We have now witnessed a rapid increase in the 

number of publications on the presence of anisakid 

larvae in various intermediate hosts in Brazil and in 

other parts of the world, so attention should be 

extended to human protection against anisakiasis. 

Members of the family Anisakidae find in Amazonia 

the necessary conditions to fully complete their 
heteroxenous life cycle. Among the possible 

intermediate hosts, Plagioscion squamosissimus and 

Pellona castelnaeana are presented. As far as we know, 

this is the first record of anisakid parasitizing Pellona 

castelnaeana

Acknowledgements 

The authors are grateful to the Laboratory of 

Scanning Electron Microscopy and Laboratory of 

Histology and Animal Embryology-LHEA/UFRA 

for putting at our disposal the scanning electron 

microscope (VEGA 3). 

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Anisakid in Plagioscion squamosissimus and Pellona castelnaeana 395 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 389-395, July-Sept., 2017 

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Received on February 24, 2017. 

Accepted on May 16, 2017. 

 

 

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and reproduction in any medium, provided the original work is properly cited. 

 

 

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