Anisakidae Skrjabin & Karokhin, 1945 and Raphidascarididae Hartwich, 1954 nematodes in lutjanidae (pisces: perciformes) from the Brazilian Northeast Coast

Nematodas Anisakidae Skrjabin & Karokhin, 1945 e Raphidascarididae Hartwich, 1954 em Lutjanidae (Pisces: Perciformes) do litoral nordeste brasileiro

A. M. Alves G. T. R. Souza R. M. Takemoto C. M. Melo R. R. Madi V. L. S. Jeraldo About the authors

Abstract

The present study aimed at describing and evaluating the fauna of Anisakidae and Raphidacarididae nematodes of lutjanid fish (snappers) from the Brazilian northeastern coast unloaded at the city of Aracaju, capital of the State of Sergipe. A total of 186 lutjanids of 5 different species were analyzed including 69 Lutjanus analis, 51 L. vivanus , 29 Ocyurus chrysurus, 23 L. synagris, and 14 L. jocu. Nematode specimens found in the viscera of these fish were clarified with lactophenol. Illustrations of each of these specimens were prepared to help identify these samples and compose their taxonomic description and classification. At necropsy, 3,183 nematodes belonging to two families were collected from fish viscera which included the following: Anisakidae: Anisakis, Terranova , Contracaecum, and Goezia; Raphidascarididae: Raphidascaris (Ichthyascaris) and Hysterothylacium . A total of six genera of nematodes were found at postmortem examination of which adult worms of only three genera (Goezia, Raphidascaris and Hysterothylacium) were detected in the fish examined. Larvae of Terranova sp. were found only in the musculature of O. chrysurus . Most of the nematode larvae were present in the mesentery and organs of the fish necropsied. Therefore, the zoonotic potential of these nematodes cannot be ruled out. There was a significant negative correlation between the intensity of parasitism by anisakids and the total body length of O. chrysurus; the intensity of parasitism was greater in smaller and shortef fish. There was a significant positive correlation between the abundance of these parasites and the length of L. synagris; the presence of these parasites increased according to the fish’s body length. To the authors’ knowledge, these are the first records of Raphidascaris (Ichthyascaris ) sp. and Hysterothylacium sp. in L. vivanus , of Terranova sp. in O. chrysurus and L. jocu, and of Goezia sp. in L. analis. These novel findings add the Brazilian northeast coast and the State of Sergipe in the geographic distribution of these parasites in the country.

Keywords:
Anisakis; Goezia; fishes; Terranova

Resumo

O objetivo deste trabalho é descrever e avaliar a fauna de Anisakidae e Raphidacarididae de peixes lutjanídeos do litoral nordeste do Brasil desembarcados na cidade de Aracaju, capital do estado de Sergipe. Foram analisados 186 lutjanídeos das espécies Lutjanus analis 69, L. vivanus 51, Ocyurus chrysurus 29, L. synagris 23 e L. jocu 14. Exemplares dos nematodas encontrados nas vísceras foram clarificados em lactofenol e ilustrados para auxiliar na identificação e compor a descrição taxonõmica. Foram coletados 3.183 nematodas das vísceras dos peixes, pertencentes a duas famílias: Anisakidae: Anisakis, Terranova, Contracaecum e Goezia; e Raphidascarididae: Raphidascaris (Ichthyascaris) e Hysterothylacium. Totalizando seis gêneros encontrados, apenas nos três últimos gêneros foram encontrados vermes em estágio adulto. Apenas em O. chrysurus foram encontradas larvas de Terranova sp. na musculatura. A maioria das larvas estava restrita ao mesentério e órgãos dos peixes, e em grande intensidade não podendo se descartar o potencial zoonótico. Observou-se uma correlação significativa negativa entre a intensidade anisakídeos e o comprimento total de O. chrysurus, onde a intensidade dos parasitas é maior em peixes de menor comprimento e uma correlação significativa positiva entre a abundância desses mesmos parasitos com o comprimento de L. synagris, onde a presença dos parasitas aumenta conforme o comprimento do peixe. Esse é o primeiro registro de Raphidascaris ( Ichthyascaris) sp. e Hysterothylacium sp. em L. vivanus ; de Terranova sp. em O. chrysurus e L. jocu e Goezia sp. em L. analis, adicionando o litoral nordeste do Brasil e o estado de Sergipe na distribuição geográfica desses parasitos.

Palavras chave:
Anisakis; Goezia; peixes; Terranova

1. Introduction

The families Anisakidae Skrjabin & Karokhin, 1945 and Raphidascarididae Hartwich, 1954 are composed of nematodes that carry out their life cycle in aquatic environments using different intermediate or paratenic hosts such as invertebrates, fish, aquatic birds, and mammals. However, both larval and adult stages of species from the genera Goezia and Hysterothylacium parasitize fish. Anisakids are a major concern to public health issues since they may be accidentally transmitted to humans by the ingestion of raw or undercooked fish infected by L3 larvae ( Andrade-Porto et al., 2015 ANDRADE-PORTO, S.M., CÁRDENAS, M.Q., MARTINS, M.L., OLIVEIRA, J.K.Q., PEREIRA, J.N., ARAÚJO, C.S.O. and MALTA, J.C.O., 2015. First record of larvae of Hysterothylacium (Nematoda: Anisakidae) with zoonotic potential in the Pirarucu Arapaima gigas (Osteichthyes: Arapaimidae) from South America. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 75, no. 4, pp. 790-795. http://dx.doi.org/10.1590/1519-6984.22213. PMid:26675898.
http://dx.doi.org/10.1590/1519-6984.222...
; Eiras et al., 2015 EIRAS, J.C., PAVANELLI, G.C., TAKEMOTO, R.M., BERNUCI, M.P., ALVARENGA, F.M.S., PACHECO, G.G., KARLING, L.C. and CALÇA, V.O. 2015. Zoonoses Causadas por nematodas. In: Pavanelli, G.C., Eiras, J.C., Yamaguchi, M.U. and Takemoto, R.M. Zoonoses Humanas Transmissíveis por Peixes no Brasil. Maringá-PR: UniCesumar, pp. 61-112. ; Souza et al., 2016 SOUZA, M.E., CARDOSO, E.O., LEAL, L.A., LIMA, T.M.P. and TOLEDO, R.C.C., 2016. Anisakidose humana: zoonose com risco potencial para consumidores de pescado cru. Veterinária e Zootecnia, vol. 23, no. 1, pp. 25-37. ). In fish, these larvae may be found in the mesentery, body cavities, musculature, or attached to internal organs (viscera). The presence of these larvae in the fish’s skeletal muscle is characteristic of some genera of the family Anisakidae. Anisakid larvae may migrate naturally to fish muscle tissue as a result of postmortem changes that occur in the host or when fish are subjected to freezing ( Eiras et al., 2006 EIRAS, J.C., TAKEMOTO, R.M. and PAVANELLI, G.C., 2006. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. 2nd ed. Maringá: Eduem, 199 p. ; Saad and Luque, 2009 SAAD, C.D.R. and LUQUE, J.L., 2009. Larvas de Anisakidae na musculatura do pargo, Pagrus pagrus, no Estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária, vol. 18, no. 1, suppl. 1, pp. 71-73. http://dx.doi.org/10.4322/rbpv.018e1014. PMid:20040196.
http://dx.doi.org/10.4322/rbpv.018e1014...
; Andrade-Porto et al., 2015 ANDRADE-PORTO, S.M., CÁRDENAS, M.Q., MARTINS, M.L., OLIVEIRA, J.K.Q., PEREIRA, J.N., ARAÚJO, C.S.O. and MALTA, J.C.O., 2015. First record of larvae of Hysterothylacium (Nematoda: Anisakidae) with zoonotic potential in the Pirarucu Arapaima gigas (Osteichthyes: Arapaimidae) from South America. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 75, no. 4, pp. 790-795. http://dx.doi.org/10.1590/1519-6984.22213. PMid:26675898.
http://dx.doi.org/10.1590/1519-6984.222...
).

Human infections by anisakids are not common in Brazil. However, several authors have reported the presence of these parasites in marine fish, generally in greater prevalences in comparison with other helminths ( São Clemente et al., 1994 SÃO CLEMENTE, S.C., UCHOA, C.M.A. and SERRA-FREIRE, N.M., 1994. Larvas de anisakideos em Pagrus pagrus (L.) e seu controle através de baixas temperaturas. Revista Brasileira de Ciência Veterinária, vol. 1, no. 1, pp. 21-24. http://dx.doi.org/10.4322/rbcv.2015.006.
http://dx.doi.org/10.4322/rbcv.2015.006...
; Luque, 2004 LUQUE, J.L., 2004. Biologia, Epidemiologia e controle de parasitas de peixes. Revista Brasileira de Parasitologia Veterinária, vol. 13, no. 1, pp. 161-164. ; Knoff et al., 2007 KNOFF, M., SÃO CLEMENTE, S.C., FONSECA, M.C.G., ANDRADA, C.G., PADOVANI, R.E.S. and GOMES, D.R., 2007. Anisakidae parasitos de congro-rosa, Genypterus brasiliensis Regan, 1903 comercializados no estado do Rio de Janeiro, Brasil de interesse na saúde pública. Parasitología Latinoamericana , vol. 62, no. 3-4, pp. 127-133. http://dx.doi.org/10.4067/S0717-77122007000200005.
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, 2013 KNOFF, M., SÃO CLEMENTE, S.C., KARLING, L.C., GAZARINI, J. and GOMES, D.C. 2013. Helmintos de potencial zoonótico. In: G.C. PAVANELLI, R.M. TAKEMOTO and J.C. EIRAS org. Parasitologia de peixes de água doce do Brasil. Maringá: Eduem, pp. 17-35. ; Barros, 2012 BARROS, L.A., 2012. Parasitoses de peixes com potencial zoonótico. In: A.T. SILVA-SOUZA, M.A.P. LIZAMA and R.M. TAKEMOTO. Patologia e Sanidade de Organismos Aquáticos . Maringá: MASSONI, pp. 125-137. ). Anisakid larvae have been reported by several authors in species of fish of economic importance such as: Anchoa tricolor, Netuma barba, Brevoortia aurea, Pagrus pagrus, Prionotus punctatus, Genypterus brasiliensis, Aluterus monoceros, Paralichthysis isoceles, Rhamdia quellen, Lophius gastrophysus, Lutjanus analis, Sardinella brasiliensis, and Selene setapinnis ( Palm, 1997 PALM, H.W., 1997. Trypanorhynch Cestodes of commercial fishes from northeast brazilian coastal waters. Memorias do Instituto Oswaldo Cruz, vol. 92, no. 1, pp. 69-79. http://dx.doi.org/10.1590/S0074-02761997000100014.
http://dx.doi.org/10.1590/S0074-0276199...
; São Clemente et al., 1994 SÃO CLEMENTE, S.C., UCHOA, C.M.A. and SERRA-FREIRE, N.M., 1994. Larvas de anisakideos em Pagrus pagrus (L.) e seu controle através de baixas temperaturas. Revista Brasileira de Ciência Veterinária, vol. 1, no. 1, pp. 21-24. http://dx.doi.org/10.4322/rbcv.2015.006.
http://dx.doi.org/10.4322/rbcv.2015.006...
; Cordeiro and Luque, 2004 CORDEIRO, A.S. and LUQUE, J.L., 2004. Community ecology of the metazoan parasites of atlantic moonfish, Selene setapinnis (Osteichthyes: Carangidae) from the coastal zone of the state of Rio de Janeiro, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia , vol. 64, no. 3A, pp. 399-406. http://dx.doi.org/10.1590/S1519-69842004000300004. PMid:15622838.
http://dx.doi.org/10.1590/S1519-6984200...
; Tavares and Luque, 2004 TAVARES, L.E.R. and LUQUE, J.L., 2004. Community ecology of the metazoan parasites of white sea catfish, Netuma barba (Osteichthyes: Ariidae), from the coastal zone of the state of Rio de Janeiro, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 64, no. 1, pp. 169-176. http://dx.doi.org/10.1590/S1519-69842004000100019. PMid:15195376.
http://dx.doi.org/10.1590/S1519-6984200...
; Tavares et al., 2004 TAVARES, L.E.R., LUQUE, J.L. and BICUDO, A.J.A., 2004. Metazoan parasites of brazilian menhaden Brevoortia aurea (spix & agassiz, 1829) (Osteichthyes: Clupeidae) from the coastal zone of the state of Rio de Janeiro, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 64, no. 3, pp. 553-554. http://dx.doi.org/10.1590/S1519-69842004000300019. PMid:15622853.
http://dx.doi.org/10.1590/S1519-6984200...
; Tavares and Luque, 2004 TAVARES, L.E.R. and LUQUE, J.L., 2004. Community ecology of the metazoan parasites of white sea catfish, Netuma barba (Osteichthyes: Ariidae), from the coastal zone of the state of Rio de Janeiro, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 64, no. 1, pp. 169-176. http://dx.doi.org/10.1590/S1519-69842004000100019. PMid:15195376.
http://dx.doi.org/10.1590/S1519-6984200...
; Bicudo et al., 2005 BICUDO, A.J.A., TAVARES, L.E.R. and LUQUE, J.L., 2005. Larvas de Anisakidae (Nematoda: Ascaridoidea) parasitas da cabrinha Prionotus punctatus (Bloch, 1793) (Osteichthyes: Triglidae) do litoral do estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária, vol. 14, no. 3, pp. 109-118. PMid:16229755. ; Knoff et al., 2007 KNOFF, M., SÃO CLEMENTE, S.C., FONSECA, M.C.G., ANDRADA, C.G., PADOVANI, R.E.S. and GOMES, D.R., 2007. Anisakidae parasitos de congro-rosa, Genypterus brasiliensis Regan, 1903 comercializados no estado do Rio de Janeiro, Brasil de interesse na saúde pública. Parasitología Latinoamericana , vol. 62, no. 3-4, pp. 127-133. http://dx.doi.org/10.4067/S0717-77122007000200005.
http://dx.doi.org/10.4067/S0717-7712200...
; Saad and Luque, 2009 SAAD, C.D.R. and LUQUE, J.L., 2009. Larvas de Anisakidae na musculatura do pargo, Pagrus pagrus, no Estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária, vol. 18, no. 1, suppl. 1, pp. 71-73. http://dx.doi.org/10.4322/rbpv.018e1014. PMid:20040196.
http://dx.doi.org/10.4322/rbpv.018e1014...
; Dias et al., 2010 DIAS, F.J.E., SÃO CLEMENTE, S.C. and KNOFF, M., 2010. Nematoides anisaquídeos e cestoides Trypanorhyncha de importância em saúde pública em Aluterus monoceros (Linnaeus, 1758) no Estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária, vol. 19, no. 2, pp. 94-97. http://dx.doi.org/10.1590/S1984-29612010000200005. PMid:20624345.
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; Felizardo et al., 2009 FELIZARDO, N.N., KNOFF, M., PINTO, R.M. and GOMES, D.C., 2009. Larval Anisakid nematodes of the flounder, Paralichthys isosceles Jordan, 1890 (Pisces: Teleostei) from Brazil. Neotropical Helminthology, vol. 3, no. 2, pp. 57-64. ; La Rue et al., 2010 LA RUE, M.L., CEOLIN, L.V., GABRIEL, C.C., BALDISSEROTTO, B., BECKER, A.G., ALMEIDA, F.M. and PEREIRA-JUNIOR, J., 2010. Risco de zoonose por parasitos do trato digestório de jundiás (Rhamdia quellen) coletados em reservatório de água da região central do rio grande do sul. Revista Saúde (Santa Maria), vol. 36, no. 2, pp. 79-81. http://dx.doi.org/10.5902/223658342316.
http://dx.doi.org/10.5902/223658342316 ...
; Saad et al., 2012 SAAD, C.D.R., VIEIRA, F.M. and LUQUE, J.L., 2012. Larvae of Anisakidae Skrjabin & Karokhin, 1945 (Nematoda, Ascaridoidea) in Lophius gastrophysus Miranda-Ribeiro, 1915 (Actinopterygii, Lophiidae) from the coastal zone of the state of Rio de Janeiro, Brazil. Neotropical Helminthology, vol. 6, no. 2, pp. 159-177. ; Knoff et al., 2013 KNOFF, M., SÃO CLEMENTE, S.C., KARLING, L.C., GAZARINI, J. and GOMES, D.C. 2013. Helmintos de potencial zoonótico. In: G.C. PAVANELLI, R.M. TAKEMOTO and J.C. EIRAS org. Parasitologia de peixes de água doce do Brasil. Maringá: Eduem, pp. 17-35. ; Hermida et al., 2014 HERMIDA, M., CARVALHO, B.F.L., CRUZ, C. and SARAIVA, A., 2014. Parasites of the Mutton Snapper Lutjanus analis (Perciformes: Lutjanidae) in Alagoas, Brazil. Revista Brasileira de Parasitologia Veterinária, vol. 23, no. 2, pp. 241-243. http://dx.doi.org/10.1590/S1984-29612014023. PMid:25054505.
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; Moreira et al., 2015 MOREIRA, J., PASCHOAL, F., CEZAR, A.D. and LUQUE, J.L., 2015. Community ecology of the metazoan parasites of Brazilian sardinella, Sardinella brasiliensis (Steindachner, 1879) (Actinopterygii: Clupeidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 75, no. 3, pp. 736-741. http://dx.doi.org/10.1590/1519-6984.00114. PMid:26465733.
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; Fontenelle et al., 2015 FONTENELLE, G., KNOFF, M., FELIZARDO, N.N., TORRES, E.J., LOPES, L.M., GOMES, D.C. and CLEMENTE, S.C., 2015. Anisakidae and Raphidascarididae larvae parasitizing Selene setapinnis (Mitchill, 1815) in the State of Rio de Janeiro. Revista Brasileira de Parasitologia Veterinária, vol. 24, no. 1, pp. 72-77. http://dx.doi.org/10.1590/S1984-29612015010. PMid:25909256.
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).

Lutjanidae are cosmopolitan fish, live in coral reefs, and are general carnivores, feeding on crustaceans, smaller fish, and molluscs ( Allen, 1985 ALLEN, G.R. 1985. FAO species catalog. Snappers of the world: An annotated and illustrated catalogue of lutjanid species known to date. Rome: FAO. vol. 6, 208 p. ; Cavalcanti et al., 2013 CAVALCANTI, E.T.S., ALVES, L.C. and CHELLAPPA, S., 2013. Occurrence of endoparasites in the southern red snapper, Lutjanus purpureus (Osteichthyes: Lutjanidae) from the coastal waters of Rio Grande do Norte, Brazil. Animal Biology Journal , vol. 4, no. 2, pp. 129-136. ). In the northeastern region of Brazil, these fish are exploited due to the good quality of their meat, and are considered an important of human food source ( Frédou and Ferreira, 2005 FRÉDOU, T. and FERREIRA, B.P., 2005. Bathymetric trends of North eastern Brazilian snappers (Pisces, Lutjanidae): Implications for the reef fishery dynamic. Brazilian Archives of Biology and Technology, vol. 48, no. 5, pp. 787-800. http://dx.doi.org/10.1590/S1516-89132005000600015.
http://dx.doi.org/10.1590/S1516-8913200...
; Begossi et al., 2011 BEGOSSI, A., SALIVONCHYK, S.V., ARAUJO, L.G., ANDREOLI, T.B., CLAUZET, M., MARTINELLI, C.M., FERREIRA, A.G., OLIVEIRA, L.E. and SILVANO, R.A., 2011. Ethnobiology of snappers (Lutjanidae): target species and suggestions for management. Journal of Ethnobiology and Ethnomedicine , vol. 7, no. 11, pp. 1-22. http://dx.doi.org/10.1186/1746-4269-7-11. PMid:21410969.
http://dx.doi.org/10.1186/1746-4269-7-1...
; Cavalcante et al., 2012 CAVALCANTE, L.F.M., OLIVEIRA, M.R. and CHELLAPPA, S. 2012. Aspectos reprodutivos do ariacó, Lutjanus synagris nas águas costeiras do Rio Grande do Norte. Biota Amazônia , vol. 2, no. 1, pp. 45-50. ). Therefore, further research on the nematode fauna that affect this group of fish is needed. The present study aimed at describing and evaluating the fauna of nematodes from the families Anisakidae and Raphidacarididae in lutjanid fish from the northeastern coast of Brazil unloaded in the city of Aracaju, capital of the State of Sergipe.

2. Materials and Methods

Fish were purchsed between March 2015 and July 2016 directly from artisanal fishermen at a fishery unit located in the city of Aracaju, State of Sergipe (SE), northeast Brazil (10 ° 54'17 “S 37 ° 2'56” W) according to supply and availability. These fish originated from the Western Atlantic. They were captured along the Brazilian of northeast coast and unloaded at the fishing unit in Aracaju, SE. Specimens were packed in thermal insulated boxes and shipped to the Laboratory of Tropical Biology at the Institute of Technology and Research. Fish were identified to the species level according to the taxonomic keys published by Allen in 1985. Then each fish was measured - total length (ct) - and weighed - weight (p). Gender was determined by gross examination of the gonads at necropsy. Parasitological evaluation of these specimens was performed according to the guidelines provided by Eiras et al. (2006) EIRAS, J.C., TAKEMOTO, R.M. and PAVANELLI, G.C., 2006. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. 2nd ed. Maringá: Eduem, 199 p. .

Nematodes that were found in organs and tissues of the digestive system during postmortem examination were fixed in 70% alcohol for further taxonomic classification. Identification of nematodes was based on their morphological characters (ventriculus, intestinal cecum, presence or absence of ventricular appendage), presence/lack of cephalic tooth and cephalic tooth arrangement, and morphology of the caudal region (presence or lack of mucron). Specimens were taxonomically characterized and their morphology compared with previous published reports of nematodes of fish available in the literature. Specimens were clarified with lactophenol. Illustrations were drawn using an light microscope (Coleman Model: N-120) with a light chamber to aid the morphological description and taxonomic identification and classification. Illustrations were prepared and converted to vector images using the software Paint. Net. V4.0.9, Adobe Illustrator cc 2014 and Adobe Photoshop cc (64 bit). Biometry of the specimens was performed using a light microscope (Coleman Model: N-120 Fuse T2A) coupled to a camera (HDCE-X5 model) and to a computer with Scope Image 9.0 (X5) software. Values ​​were expressed in millimeters (mm).

The parasitological indices of prevalence (p%), intensity (I), mean intensity (im), and mean abundance (am) were calculated according to the formulas published by Bush et al. (1997) BUSH, A.O., LAFFERTY, K.D., LOTZ, J.M. and SHOSTAK, A.W., 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology , vol. 83, no. 4, pp. 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
http://dx.doi.org/10.2307/3284227 ...
. Species of the family Anisakidae were grouped into a single group - Anisakidae - in order to carry out the statistical analyses. The Spearman correlation coefficient (rs) was used to assess possible correlations between the intensity and abundance of anisakíds and fish body length. In this survey, we used the statistical software Bioestat 5.0, and a level of significance of p <0.05 was considered.

3. Results

A total of 186 lutjanids from 5 different species were analyzed as follows: Lutjanus analis (69 specimens), Lutjanus vivanus (51 specimens), Ocyurus chrysurus (29 specimens), Lutjanus synagris (23 specimens), and Lutjanus jocu (14 specimens). The mean total length and weight for each fish species is shown in Table 1 .

Table 1
Mean and standard deviation of length and weight of different species of lutjanid fish collected between March 2015 and July 2016 along the coast of Northeast Brazil. ml: mean length; mw: mean weight.

A total of 3.183 nematodes belonging to 2 families and 6 species were collected from viscera and musculature of fish: Anisakidae: Anisakis, Terranova , Contracaecum, and Goezia; Raphidascarididae: Raphidascaris (Ichthyascaris) and Hysterothylacium . In 4 genera (Contracaecum, Goezia; Raphidascaris , and Hysterothylacium), the parasitism intensity was low ( Table 2 ). Anisakis sp. was the most prevalent genus of nematode in the samples examined. A great parasitism intensity of the genus Terranova (1,362 larvae) was found in O. chrysurus. Only specimens from the genera Raphidascaris (Ichthyascaris), Hysterothylacium and Goezia were adults. High prevalence and intensity indices of nematode larval infestation were detected mainly in the intestinal mesentery of fish. Parasites were found in all organs. The site of infection was collectively referred to as “tissues” ( Table 2 ).

Table 2
Parasitological indices for nematode species of the host species of Lutjanus vivanus, Lutjanus synagris, Lutjanus jocu , Ocyurus chrysurus, collected in the period of March 2015 and July 2016 along the Brazilian Northeast coast in which: P% = Prevalence; I = Intensity; MI = Mean Intensity; MA = Mean Abundance.

The correlation between the length of parasitized fish and parasitic indices by anisakids did not show statistical significance, except for O. chrysurus and L. synagris in which there was a significant negative and positive correlation, respectively ( Table 3 ). Based on these data, we may infer that the number of these parasites does not increase proportionally according to the body size of this host species; the number of parasites is greater in smaller fish. The correlation between fish length and abundance of anisakids was not significant among species, except for L. synagris ( Table 3 ) in which there was a significant and positive correlation. This finding shows that for this particular species the Anisakidae fauna increases proportionally according to the fish’s body size.

Table 3
Correlation between fish body length of the Lutjanidae family and the intensity and abundance of anisakids, collected from March 2013 to July 2016 along the Brazilian Northeast coast.

All the fish analyzed had at least one Anisakidae larvae (prevalence of 100%) with the greatest intensities of Anisakis sp. in L. analis, L. jocu, L. synagris, and L. vivanus, and of Terranova sp. in O. chrysurus. Among all fish specimens evaluated for the presence of anisakids, only O. chrysurus presented larvae in the musculature (n = 34) which belonged to the genus Terranova ( Table 2 ).

The morphological description of the parasites found is given below:

Superfamily Ascaridoidea Baird, 1853

Family Anisakidae Railliet & Henry, 1912

Subfamily Anisakinae Chabaud, 1965

Genus Anisakis Dujardin, 1845

Hosts: L. analis, L. jocu, L. synagris,

L. vivanus, O. chrysurus.

Site of infection: viscera (intestinal mesentery).

Location: Northeastern Coast, Aracaju, SE, Brazil.

Material examined: 56 specimens of L3 larvae

Description ( Figure 1 ): 3rd stage larvae. Thin body (length: 20 ± 2) ( Figure 1 a). Cuticle with transverse striae, most noticeable in the anterior and posterior extremities, and also evident throughout the body. Anterior end with three slightly defined lips, one dorsal lip with a pair of labial papillae and two subventral lips, each with a single papilla, approximately of the same size (length: 0.06 ± 0.01), with the presence of a ventral cephalic tooth close to the oral aperture ( Figure 1 b). Thick cuticle; nerve ring located in the anterior region of the esophagus. Long esophagus (length: 1.5 ± 0.1), followed by a long ventriculus (length 0.5 ± 0.07) compressed agaisnt the intestine. Absence of ventricular appendix and intestinal cecum. Tail: conical, rounded and tapered with the rectum canal; mucron in the terminal region ( Figure 1 c).

Figure 1
Anisakis sp. a - Larva L3 (bar: 5mm). b - Anterior region (bar: 0.06mm), arrows indicate the cephalic tooth and the nerve ring. c - Posterior region (bar: 0.06mm), arrow indicates the micron.

Genus Terranova Leiper & Atkinson, 1914

Hosts: L. jocu, L. vivanus, O. chrysurus.

Infection site: viscera (intestinal mesentery) and musculature.

Location: Northeastern Coast, Aracaju, SE, Brazil.

Material examined: 5 specimens of L3 larvae

Description ( Figure 2 ): Larvae L3, thin body (length: 12 ± 8), cuticle with transverse striae most evident in the anterior and posterior regions (terminal portion of the tail) and some along the body. Anterior end with three underdeveloped lips, dorsal lip, and two subventral lips (length 0.07 ± 0.04). Cephalic tooth: pronounced, evident, located near the oral aperture of the larvae which lies between the subventral lips. Opening of the excretory pore near the ventro-lateral lips. Nervous ring at the anterior end of the esophagus ( Figure 2 b). Esophagus (length: 1.3 ± 0.5) and short ventriculus (length: 0.3 ± 0.1) without ventricular appendage. The intestinal cecum extends over the ventriculus, exceeding half of the esophagus. The posterior region has a robust, conical and transversely striated tail; mucron absent; two spherical rectal glands present ( Figure 2 c).

Figure 2
Terranova sp.; a- Larva L3 (bar: 3mm) collected from Lutjanus vivanus and Lutjanus jocu; b - Anterior region (bar: 0.04 mm); arrows indicate the cephalic tooth and opening of the excretory pore; c - Posterior region (bar: 0.04mm); arrow indicates the rectal glands.

Superfamily Ascaridoidea Baird, 1853

Family Raphidascarididae Hartwich, 1954

Subfamily Raphidascaridinae Hartwich, 1954

Genus Hysterothylacium Ward and Magath, 1917

Host: L. vivanus.

Infection Site: Intestine

Location: Northeastern Coast, Aracaju, SE, Brazil.

Material examined: 1 pregnant female.

Description ( Figure 3 ): Elongated body (length: 21), which becomes thinner in the anterior end ( Figure 3 a). The cuticle that lines the body is transversely striated. Whitish body. Lips: well developed; interlabium absent. It has three rounded lips with elliptical labial papillae and anterior lobes ( Figure 3 b). Subventral lips of the same size (length: 0.2) and slightly smaller dorsal lip (length: 0.1). Long esophagus (Length: 3) occupies 14% of body length. Oval and short ventriculus (Length: 0.2), present; short ventricular appendix (Length: 0.5). Intestinal cecum inverted and slightly longer than the ventriculus. The uterus extends posteriorly to the level of the rectum. Numerous elliptical eggs with delicate and thin membranes ( Figure 3 d). Mucron absent. Conical and tapered tail, with evident transverse striations, with numerous cuticular protrusions, similar to nodules in the terminal portion of the tail ( Figure 3 c). Caudal region has three spherical rectal glands.

Figure 3
Hysterothylacium sp. a - Adult female (esophagus scale: 3mm). b - Anterior region and detail of the lips (scale: 0.2mm); arrows indicate anterior lobes; c - Caudal region; arrows indicate the rectal glands and cuticular spines at the end of the tail; d - Egg (scale: 0.01mm).

Super family Ascaridoidea Baird, 1853

Family Raphidascarididae Hartwich, 1954

Subfamily Raphidascaridinae Hartwich, 1954

Genus Raphidascaris Railliet & Henry, 1915

Species Raphidascaris (Ichthyascaris) sp.

Host: L. vivanus.

Infection Site: Intestine

Location: Northeastern Coast, Aracaju, SE, Brazil.

Material examined: 4 specimens (3 pregnant females and 1 male).

Description ( Figure 4 ): Female ( Figure 4 2): Elongated body (length: 10; width: 0.67).

Figure 4
a1 and a2 - Female and male of Raphidascaris (Ichthyascaris ) sp. (bar: 1mm); b - Anterior region (bar: 0.5mm); c1 and c2 - Posterior of female and male (bar: 0.5mm); d - Egg (0.01mm); e - Spikes of the core (bar: 0.1mm).

The cuticle of the body is also transversely striated. Relatively opaque/not very transparent body. It has three well-developed lips (length: 0.06; width: 0.07). In each lip there are anterior lobes and elliptic labial papillae, a pair of papillae in the dorsal lobe and a papilla in each subventral libe, and also presents narrow lateral wings that join in one side of the body near the base of the lips ( Figure 4 b). Short esophagus (length: 1; width: 0.2) occupying 11% of the body. Flat, oval and short ventriculus (length: 0.1; width: 0.2); ventricular appendage present (length: 0.5; width: 0.1). The vulva opens shortly before the terminal region of the ventricular appendage. Uterus extends posterior to the level of the rectum. Numerous eggs occupy a large area in the central region of the body; these eggs are elliptical, and have delicate and thin membranes ( Figure 4 d). Conical and tapered tail, with transverse striations evident; there are small lumps similar to nodules in the terminal portion. Mucron: absent. The caudal region has three spherical rectal glands ( Figure 4 1).

Male ( Figure 4 1): Elongated body, same length and width of female (length: 10; width: 0.6). It also has three well-developed lips of approximately the same size. Lips with anterior lobes and elliptical labial papillae, a pair of papillae on the dorsalis and a papilla in each subventral. Short esophagus, of equal length to the female (length: 1mm; width: 0.2). Flat, oval and short ventriculus, as well as in female (length: 0.1; width: 0.2); ventricular appendage present, slightly larger than that of female (length: 0.6). Conical and tapered tail; mucron absent. The caudal region has three spherical rectal glands ( Fig 4 2). Ventrally curved posterior region with 36 pairs of subventral papillae. Spikes equal in length (Length: 0.3), pointed and without ornamentation, corresponding to 3% of the body length ( Figure 4 e).

Superfamily Ascaridoidea Baird, 1853

Family Anisakidae Skrjabin & Karokhin, 1945

Genus Goezia Zeder, 1800

Host: L. analis.

Infection Site: Intestine

Location: Northeastern coast, Aracaju, SE, Brazil

Material examined: 3 specimens.

Description ( Figure 5 ): Medium-sized nematodes, Elongated body, male smaller (length: 7.5; width: 0.7) than female (length: 9.7mm; width: 0.7) with very thick cuticle, transversely striated body with several transverse rows of posteriorly oriented spines around the body ( Figure 5 a, b). The rows of thorns begin just after the lips. The lines gradually become more separate, becoming less spaced as they approach the tail. Lips nearly identical morphologically; inner part of each lip with two distinct lobes oriented towards the oral aperture ( Figure 5 c). Dorsal lip with two double papillae; ventro-lateral lips each with a single papilla and a double papilla. Interlabium absent. Triangular oral aperture. Esophagus occupies 9.2% of body length in females (Length: 0.9; width: 0.1) and 10.6% in males (length: 0.8; width: 0.1). Elliptical and small ventriculus (Length: 0.04; width: 0.1). Ventricular appendage of the female (length: 1.4; width: 0.05) is larger than the ventricular appendage of the male (length: 0.4; width: 0.04). Intestinal cecum inverted, reaching part of the esophagus ( Figure 5 f). Conical tail with the digitiform process ( Figure 5 d). In the terminal portion of the male tail, there are cuticular spines and a pair of similar spicules (length: 0.8) ( Figure 5 e). In the female, there is a mucron with 20 small spines. Spherical eggs with thin, smooth shell, and non-cleaved contents ( Figure 5 f).

Figure 5
a and b - Male and female adults of Goezia sp. (bar: 1mm); c - Anterior region, with prominence of the lips (bar: 0.5mm); d- Posterior Region: 1 - terminal portion of the male; 2 - terminal portion of the female (bar: 0.5mm); e - Spicule of the male (bar: 0.6mm); f - arrangement of internal organs: esoph - esophagus vent – ventriculus; apv - ventricular appendage; inc - intestinal cecum; ut - coiled uterus g - Egg (bar: 0.01).

In the present survey, the presence of nematodes of the family Anisakidae was high in the fish samples examined. The non-significant correlation between the fish body length and the parasite intensity of 4 of the 5 fish species of this study allows us to infer that the parasitism by anisakids is neither determined nor influenced by the length of the host, and that fish of varying sizes may be infected and have zoonotic potential. O. chrysurus was the only species that presented negative and significant correlation between host’s body length and intensity of anisakids. The same was observed between the abundance of Anisakis sp. and the body length of L. synagris.

Infection by these parasites involves aquatic invertebrates and fish as intermediary hosts through the food chain, which explains how fish acquire these parasites. On the other hand, the fish could play a role as paratenic hosts helping to disseminate and spread the parasites until reaching a definitive host ( Bicudo et al., 2005 BICUDO, A.J.A., TAVARES, L.E.R. and LUQUE, J.L., 2005. Larvas de Anisakidae (Nematoda: Ascaridoidea) parasitas da cabrinha Prionotus punctatus (Bloch, 1793) (Osteichthyes: Triglidae) do litoral do estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária, vol. 14, no. 3, pp. 109-118. PMid:16229755. ; Saad et al., 2012 SAAD, C.D.R., VIEIRA, F.M. and LUQUE, J.L., 2012. Larvae of Anisakidae Skrjabin & Karokhin, 1945 (Nematoda, Ascaridoidea) in Lophius gastrophysus Miranda-Ribeiro, 1915 (Actinopterygii, Lophiidae) from the coastal zone of the state of Rio de Janeiro, Brazil. Neotropical Helminthology, vol. 6, no. 2, pp. 159-177. ).

The larvae of anisakids showed high prevalence and intensity rates in fish tissues, in particular in the intestinal mesentery, with the highest indexes represented by Anisakis sp. However, larvae of Contracaecum sp. and Terranova sp. were found at lower intensities. According to Azevedo et al. (2007) AZEVEDO, R.K., ABDALLAH, V.D. and LUQUE, J.L., 2007. Aspectos quantitativos da comunidade de metazoários parasitos do gordinho Peprilus paru (Linnaeus,1758) (Perciformes: Stromateidae), do litoral do estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária, vol. 16, no. 1, pp. 10-14. PMid:17588316. , the presence of these larvae in the mesentery represents a low zoonotic potential. However, due to the high intensity of anisakids collected, the zoonotic risk cannot be ruled out since these parasites may migrate to the musculature of barely live or freshly caught fish. Evidence indicates that the presence of anisakid larvae in tissues of economically important fish negatively affects fish industrialization in addition to its implications for public health ( Knoff et al., 2013 KNOFF, M., SÃO CLEMENTE, S.C., KARLING, L.C., GAZARINI, J. and GOMES, D.C. 2013. Helmintos de potencial zoonótico. In: G.C. PAVANELLI, R.M. TAKEMOTO and J.C. EIRAS org. Parasitologia de peixes de água doce do Brasil. Maringá: Eduem, pp. 17-35. ).

Montoya-Mendoza et al. (2014) MONTOYA-MENDOZA, J., JIMÉNEZ-BADILLO, M.L. and SALGADO-MALDONADO, G., 2014. Helminths of Ocyurus chrysurus from coastal reefs in Veracruz, Mexico. Revista Mexicana de Biodiversidad, vol. 85, no. 3, pp. 957-960. http://dx.doi.org/10.7550/rmb.43343.
http://dx.doi.org/10.7550/rmb.43343 ...
demonstrated that O. chrysurus shared a rich parasitic community. The authors found larvae of the genus Contracaecum in the viscera of fish. In the present study, larvae of Terranova were found were found in O. chrysurus with high prevalences (more than 50%), and different from the authors regarding the site of infection (the musculature), demonstrating that larvae ability to migrate and the possibility of zoonotic transmission. To the authors’ knowledge, this is the first report of Terranova sp. in O. chrysurus and L. jocu. Larvae of Terranova have been previously reported in other fish by other authors including Cordeiro and Luque (2004) CORDEIRO, A.S. and LUQUE, J.L., 2004. Community ecology of the metazoan parasites of atlantic moonfish, Selene setapinnis (Osteichthyes: Carangidae) from the coastal zone of the state of Rio de Janeiro, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia , vol. 64, no. 3A, pp. 399-406. http://dx.doi.org/10.1590/S1519-69842004000300004. PMid:15622838.
http://dx.doi.org/10.1590/S1519-6984200...
, Tavares and Luque (2004) TAVARES, L.E.R. and LUQUE, J.L., 2004. Community ecology of the metazoan parasites of white sea catfish, Netuma barba (Osteichthyes: Ariidae), from the coastal zone of the state of Rio de Janeiro, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 64, no. 1, pp. 169-176. http://dx.doi.org/10.1590/S1519-69842004000100019. PMid:15195376.
http://dx.doi.org/10.1590/S1519-6984200...
, Tavares et al. (2005) TAVARES, L.E.R., LUQUE, J.L. and BICUDO, A.J.A., 2005. Community ecology of metazoan parasites of the anchovy Anchoa tricolor (Osteichthyes: Engraulidae) from the coastal zone of the state of Rio de Janeiro, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia , vol. 65, no. 3, pp. 533-540. http://dx.doi.org/10.1590/S1519-69842005000300019. PMid:16341432.
http://dx.doi.org/10.1590/S1519-6984200...
and Luque et al. (2008) LUQUE, J.L., FELIZARDO, N.N. and TAVARES, L.E.R., 2008. Community ecology of the metazoan parasites of namorado sandperches, Pseudopercis numida Miranda-Ribeiro, 1903 and P. semifasciata Cuvier, 1829 (Perciformes: Pinguipedidae), from the coastal zone of the State of Rio de Janeiro, Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 68, no. 2, pp. 269-278. http://dx.doi.org/10.1590/S1519-69842008000200007. PMid:18660954.
http://dx.doi.org/10.1590/S1519-6984200...
in Selene setapinnis, Netuma barba, Anchoa tricolor (Spix & Agassiz, 1829), Pseudopercis numida Miranda-Ribeiro, 1903, and P. semifasciata Cuvier, 1829, respectively.

Cortes et al. (2009) CORTÉS, J., VALBUENA, J. and MANRIQUE, G., 2009. Nemátodos parásitos de Lutjanus synagris (Linneaus, 1758) y Lutjanus analis (Cuvier, 1828) (Perciformes, Lutjanidae) en las zonas de Santa Marta y Neguanje, Caribe Colombiano. Revista de la Facultad de Medicina Veterinaria y Zootecnia, vol. 56, no. 1, pp. 23-31. reported the genera Contracaecum sp. and Raphidascaris sp. in L. analis and L. synagris in which Raphidascaris sp. presented the highest prevalence for both species of fish. However, the findings published of the authors may not be accurate. These authors described adults of Contracaecum sp. in L. analis. These parasites reach the adult stage only in the digestive tract of piscivorous birds and mammals which are their definitive hosts ( Saad et al., 2012 SAAD, C.D.R., VIEIRA, F.M. and LUQUE, J.L., 2012. Larvae of Anisakidae Skrjabin & Karokhin, 1945 (Nematoda, Ascaridoidea) in Lophius gastrophysus Miranda-Ribeiro, 1915 (Actinopterygii, Lophiidae) from the coastal zone of the state of Rio de Janeiro, Brazil. Neotropical Helminthology, vol. 6, no. 2, pp. 159-177. ). The present survey also documented the occurrence of the genus Contracaecum and the species L. analis with a low intensity (n = 1 larva) which was considered an incidental finding.

Hermida et al. (2014) HERMIDA, M., CARVALHO, B.F.L., CRUZ, C. and SARAIVA, A., 2014. Parasites of the Mutton Snapper Lutjanus analis (Perciformes: Lutjanidae) in Alagoas, Brazil. Revista Brasileira de Parasitologia Veterinária, vol. 23, no. 2, pp. 241-243. http://dx.doi.org/10.1590/S1984-29612014023. PMid:25054505.
http://dx.doi.org/10.1590/S1984-2961201...
analyzed specimens of L. analis, and recorded the presence of nematodes of the genus Hysterothylacium (P= 3,3%; IM= 3,00±2,83; AM= 0,10±0,66), different from the present study which reported the presence of Anisakis sp. with higher prevalence, intensity, and abundance indices (P= 20,28%; IM= 15,28±36,27; AM= 3,10±17,15). The morphological analysis of Anisakis larvae in relation to the tail does not match the one described by Bicudo et al. (2005) BICUDO, A.J.A., TAVARES, L.E.R. and LUQUE, J.L., 2005. Larvas de Anisakidae (Nematoda: Ascaridoidea) parasitas da cabrinha Prionotus punctatus (Bloch, 1793) (Osteichthyes: Triglidae) do litoral do estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária, vol. 14, no. 3, pp. 109-118. PMid:16229755. in Rio de Janeiro, southeast Brazil, being less sharp and more rounded and conical, with mucron and transverse striations evident in the terminal region, having the morphology and length similar to those described by Felizardo et al. (2009) FELIZARDO, N.N., KNOFF, M., PINTO, R.M. and GOMES, D.C., 2009. Larval Anisakid nematodes of the flounder, Paralichthys isosceles Jordan, 1890 (Pisces: Teleostei) from Brazil. Neotropical Helminthology, vol. 3, no. 2, pp. 57-64. and Saad et al. (2012) SAAD, C.D.R., VIEIRA, F.M. and LUQUE, J.L., 2012. Larvae of Anisakidae Skrjabin & Karokhin, 1945 (Nematoda, Ascaridoidea) in Lophius gastrophysus Miranda-Ribeiro, 1915 (Actinopterygii, Lophiidae) from the coastal zone of the state of Rio de Janeiro, Brazil. Neotropical Helminthology, vol. 6, no. 2, pp. 159-177. . Larvae of Terranova were larger in relation to other larvae of Terranova spp. reported by other authors; the excretory pore located near the ventrolateral base of the lips and the short intestinal cecum were morphological characters that corroborated with previous findings published by Tavares et al. (2007) TAVARES, L.E.R., SAAD, C.D.R., CEPEDA, P.B. and LUQUE, J.L., 2007. Larvals of Terranova sp. (Nematoda: Anisakidae) Parasitic in Plagioscion squamosissimus (Perciformes: Sciaenidae) from Araguaia river, State of Tocantins, Brasil. Revista Brasileira de Parasitologia Veterinária, vol. 16, no. 2, pp. 110-115. PMid:17706015. , Saad et al. (2012) SAAD, C.D.R., VIEIRA, F.M. and LUQUE, J.L., 2012. Larvae of Anisakidae Skrjabin & Karokhin, 1945 (Nematoda, Ascaridoidea) in Lophius gastrophysus Miranda-Ribeiro, 1915 (Actinopterygii, Lophiidae) from the coastal zone of the state of Rio de Janeiro, Brazil. Neotropical Helminthology, vol. 6, no. 2, pp. 159-177. , and Fonseca et al. (2016) FONSECA, M.C.G., KNOFF, M., FELIZARDO, N.N., DI AZEVEDO, N.I.N., TORRES, E.J.L., GOMES, D.C., IÑIGUEZ, A.M. and SÃO CLEMENTE, S.C., 2016. Integrative taxonomy of Anisakidae and Raphidascarididae (Nematoda) in Paralichthys patagonicus and Xystreurys rasile (Pisces: Teleostei) from Brazil. International Journal of Food Microbiology, vol. 235, pp. 113-124. http://dx.doi.org/10.1016/j.ijfoodmicro.2016.07.026. PMid:27491056.
http://dx.doi.org/10.1016/j.ijfoodmicro...
.

The genus Goezia is known for presenting general morphological characters such as three radial lips and thick striated cuticle with several crowns of spines projected from the back of each segment. Its life cycle is not yet fully known and warrants further research ( Deardorff and Overstreet, 1980 DEARDORFF, T.L. and OVERSTREET, R.M., 1980. Taxonomy and Biology of North American Species of Goezia (Nematoda: Anisakidae) from Fishes, including Three New Species. Proceedings of the Helminthological Society of Washington, vol. 47, no. 2, pp. 192-217. ). Goezia species have been reported in several species of fish including Rhaphiodon vulpinus, Serrasalmus marginatus, Ageneiosus valenciennes, Hoplosternum littorale, Arapaima gigas, Hemisorubim platyrhynchos, Mylossoma orbignyanus, Parauchenipterus galeatus, Pimelodus maculatus, Leporinus friderici, Ageneiosus militaris, Trachelyopterus galeatus, Brycon orbignyanus, Piacactus mesopotamicus, Oxydoras knerii, Iheringichthys labrosus, and Macrodon ancylodon, ( Moravec et al., 1993 MORAVEC, F., KOHN, A. and FERNANDES, B.M.M., 1993. Nematode parasites of fishes of the Paraná River, Brazil. Part 2. Seuratoidea, Ascaridoidea, Habronematoidea and Acuarioidea. Folia Parasitologica, vol. 40, pp. 115-134. ; Vicente and Pinto, 1999 VICENTE, J.J. and PINTO, R.M., 1999. Nematóides do Brasil. Nematóides de peixes Atualização: 1985-1998. Revista Brasileira de Zoologia , vol. 16, no. 3, pp. 561-610. http://dx.doi.org/10.1590/S0101-81751999000300001.
http://dx.doi.org/10.1590/S0101-8175199...
; Abdallah et al., 2006 ABDALLAH, V.D., AZEVEDO, R.K. and LUQUE, J.L., 2006. Ecologia da comunidade de metazoários parasitos do tamboatá Hoplosternum littorale (Hancock, 1828) (Siluriformes: Callichthyidae) do rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Scientiarum. Biological Sciences, vol. 28, no. 4, pp. 413-419. http://dx.doi.org/10.4025/actascibiolsci.407.
http://dx.doi.org/10.4025/actascibiolsc...
; Santos and Moravec, 2009 SANTOS, C.P. and MORAVEC, F., 2009. Goezia spinulosa (Nematoda: Raphidascarididae), a pathogenic parasite of the Arapaima gigas (Osteichthyes). Folia Parasitologica, vol. 56, no. 1, pp. 55-63. http://dx.doi.org/10.14411/fp.2009.009. PMid:19391331.
http://dx.doi.org/10.14411/fp.2009.009 ...
; Azevedo et al., 2010 AZEVEDO, R.K., ABDALLAH, V.D. and LUQUE, J.L., 2010. Acanthocephala, Annelida, Arthropoda, Myxozoa, Nematoda and Platyhelminthes parasites of fishes from the Guandu river, Rio de Janeiro, Brazil. Check List, vol. 6, no. 4, pp. 659-667. http://dx.doi.org/10.15560/6.4.659.
http://dx.doi.org/10.15560/6.4.659 ...
; Eiras et al., 2010 EIRAS, J.C., TAKEMOTO, R.M. and PAVANELLI, G.C., 2010. Diversidade dos parasitas de peixes de água doce do Brasil. Maringá: Cliche Tec, 333 p. ; Kohn et al., 2011 KOHN, A., MORAVEC, F., COHEN, S.C., CANZI, C., TAKEMOTO, R.M. and FERNANDES, B.M.M., 2011. Helminths of freshwater fishes in the reservoir of the Hydroelectric Power Station of Itaipu, Paraná, Brazil. Check List, vol. 7, no. 5, pp. 681-690. http://dx.doi.org/10.15560/7.5.681.
http://dx.doi.org/10.15560/7.5.681 ...
; Fujimoto et al., 2012 FUJIMOTO, R.Y., SARMENTO, A.M.B., DINIZ, D.G. and EIRAS, J.C., 2012. Nematode Parasites of Pescada Gó, Macrodon ancylodon Bloch and Schneider, 1801 (Osteichthyes, Sciaenidae), from Vila dos Pescadores, Bragança-PA, Brazil. Brazilian Archives of Biology and Technology, vol. 55, no. 6, pp. 865-870. http://dx.doi.org/10.1590/S1516-89132012000600009.
http://dx.doi.org/10.1590/S1516-8913201...
).

The majority of the studies on Goezia include freshwater fish. Studies of this genus of nematode in marine fish, especially in Lutjanidae, are scarce. In the present study, Goezia sp. was found in the intestinal lumen of the gut at low intensity. These were adult specimens/pregnant females which suggests that Lutjanus analis was playing the role of the definitive host for this parasite. Records of this parasitic group in lutjanids are rare. There are only one other case published by Rizwana et al. (2000) RIZWANA, A.G., GHAZI, R.R., KHATOON, N. and BILQEES, F.M., 2000. Goezia argentimaculatii sp. n. (Heterocheilidae) from fish Lutjanus argentimaculatus (Fork, 1775) of Karachi coast. Proceedings of Parasitology, vol. 30, pp. 33-40. describing Goezia argentimaculati in Lutjanus argentimaculatus. All species of Goezia are parasites of freshwater fish. Thus, parasitic infestations of L. analis by nematodes may be explained by the estuarine behavior of fish which may have acquired the parasites through the trophic chain. The presence of adult specimens of Goezia sp. in the intestine in L. analis is considered a novel finding.

Raphidascaris and Hysterothylacium are parasites that have teleost fish as intermediate, paratenic, or definitive hosts. These were the only genera found as adults in L. vivanus (Raphidascaris (Icthyascaris) as follows: 3 pregnant females and 1 male; Hysterothylacium: 1 pregnant female) being considered as new occurrences of these parasites in this species of fish and demonstrating that this species of fish is playing a role as the definitive hosts in the life cycle of these parasites, unlike other studies published elsewhere that reported only larvae of this group of nematodes parasitizing fish. Raphidascaris (Ichthyascaris ) sp. presented lower body and esophagus length and esophagus size in relation to the larger body when compared to the parameters described for R. (I.) etelidis in Etelis coruscans (Lutjanidae) by Moravec and Justine (2012) MORAVEC, F. and JUSTINE, J.L., 2012. Raphidascaris (Ichthyascaris ) etelidis n. sp. (Nematoda, Anisakidae), a new ascaridoid nematode from lutjanid fishes off New Caledonia. Zoosystema, vol. 34, no. 1, pp. 113-121. http://dx.doi.org/10.5252/z2012n1a4.
http://dx.doi.org/10.5252/z2012n1a4 ...
(10mm, 1mm and 11% x 26.63mm, 2.30, 8.1%, respectively). Two other species of the same subgenus, one in New Caledonia ( Moravec and Justine, 2005 MORAVEC, F. and JUSTINE, J.L., 2005. Two anisakid nematodes from marine fishes off New Caledonia, including Raphidascaris (Ichthyascaris) nemipteri n. sp. from Nemipterus furcosus. Systematic Parasitology, vol. 62, no. 2, pp. 101-110. http://dx.doi.org/10.1007/s11230-005-5484-9. PMid:16167119.
http://dx.doi.org/10.1007/s11230-005-54...
) and one in China ( Xu et al., 2012 XU, Z., ZHANG, L.P., LIU, B.C. and LI, L., 2012. Morphological and molecular characterization of Raphidascaris (Ichthyascaris) lophii (Wu, 1949) (Nematoda, Anisakidae) from marine fishes from China, with a key to the species of the subgenus Ichthyascaris. Acta Parasitologica, vol. 57, no. 3, pp. 316-322. http://dx.doi.org/10.2478/s11686-012-0037-2. PMid:22875681.
http://dx.doi.org/10.2478/s11686-012-00...
) have also been described. The number of subventral papillae and the size of the spicules in relation to the body were within the average of the parameters of species such as R. (I.) nemipteriMoravec and Justine (2005) MORAVEC, F. and JUSTINE, J.L., 2005. Two anisakid nematodes from marine fishes off New Caledonia, including Raphidascaris (Ichthyascaris) nemipteri n. sp. from Nemipterus furcosus. Systematic Parasitology, vol. 62, no. 2, pp. 101-110. http://dx.doi.org/10.1007/s11230-005-5484-9. PMid:16167119.
http://dx.doi.org/10.1007/s11230-005-54...
; R. (I.) arii Yooyen et al. (2011) YOOYEN, T., MORAVEC, F. and WONGSAWAD, C., 2011. Raphidascaris ( Ichthyascaris) arii sp. n. (Nematoda: Anisakidae), a new ascaridoid nematode from marine catfishes in the Gulf of Thailand. Helminthologia , vol. 48, no. 4, pp. 262-267. http://dx.doi.org/10.2478/s11687-011-0037-z.
http://dx.doi.org/10.2478/s11687-011-00...
; R. (I.) longispicula L, Li et al. (2012) LI, L., LIU, Y.Y., LIU, B.C. and ZHANG, L.P., 2012. Morphological and molecular evidence for a new species of the genus Raphidascaris (Nematoda: Anisakidae) from marine fishes from the South China Sea. Parasitology Research, vol. 110, no. 4, pp. 1473-1479. http://dx.doi.org/10.1007/s00436-011-2650-7. PMid:21987101.
http://dx.doi.org/10.1007/s00436-011-26...
, and R. (I.) lophii (Wu, 1949).

The genus Hysterothylacium was initially included in the family Anisakidae, but was then moved into the family Raphidascarididae ( Eiras et al., 2015 EIRAS, J.C., PAVANELLI, G.C., TAKEMOTO, R.M., BERNUCI, M.P., ALVARENGA, F.M.S., PACHECO, G.G., KARLING, L.C. and CALÇA, V.O. 2015. Zoonoses Causadas por nematodas. In: Pavanelli, G.C., Eiras, J.C., Yamaguchi, M.U. and Takemoto, R.M. Zoonoses Humanas Transmissíveis por Peixes no Brasil. Maringá-PR: UniCesumar, pp. 61-112. ) composing the family together with Raphidascaris. In the present study, the specimen of Hysterothylacium sp. found in L. vivanus was an adult female with eggs. It had a long esophagus and an inverted intestinal cecum slightly longer than the ventriculum which is a morphological feature shared by three other species: H. longilabrum Li, Liu & Zhang, 2012; H. anguillae Moravec et al. (2012), and H. gibsoniXu et al. (2014) XU, Z., LI, L. and ZHANG, L.P., 2014. Hysterothylacium gibsoni sp. nov. and H. tetrapteri (Bruce et Cannon, 1989) (Nematoda: Ascaridida) from the Chinese marine fishes. Acta Parasitologica, vol. 59, no. 2, pp. 323-330. http://dx.doi.org/10.2478/s11686-014-0250-2. PMid:24827106.
http://dx.doi.org/10.2478/s11686-014-02...
. However, the second species was found in rivers whereas the others occur in marine environments. In Brazil, the genus has been reported in several marine and freshwater fish ( Eiras et al., 2015 EIRAS, J.C., PAVANELLI, G.C., TAKEMOTO, R.M., BERNUCI, M.P., ALVARENGA, F.M.S., PACHECO, G.G., KARLING, L.C. and CALÇA, V.O. 2015. Zoonoses Causadas por nematodas. In: Pavanelli, G.C., Eiras, J.C., Yamaguchi, M.U. and Takemoto, R.M. Zoonoses Humanas Transmissíveis por Peixes no Brasil. Maringá-PR: UniCesumar, pp. 61-112. ). We believe that this is the first record of Hysterothylacium sp. in L. vivanus.

Anisakids reach adulthood in the digestive tract of birds and marine mammals which are definitive hosts of these nematodes, and have aquatic invertebrates and fish as intermediary or paratenic hosts during their larval stages (L1, L2, L3, and L4) ( Eiras et al., 2015 EIRAS, J.C., PAVANELLI, G.C., TAKEMOTO, R.M., BERNUCI, M.P., ALVARENGA, F.M.S., PACHECO, G.G., KARLING, L.C. and CALÇA, V.O. 2015. Zoonoses Causadas por nematodas. In: Pavanelli, G.C., Eiras, J.C., Yamaguchi, M.U. and Takemoto, R.M. Zoonoses Humanas Transmissíveis por Peixes no Brasil. Maringá-PR: UniCesumar, pp. 61-112. ). Therefore, identification at the species level is only possible using molecular tools. For Raphidascaris (Ichthyascaris) sp., only one male specimen was found, which made it difficult to accurately identify the species. Only one gravid female of Hysterothylacium was detected.

Azevedo et al. (2007) AZEVEDO, R.K., ABDALLAH, V.D. and LUQUE, J.L., 2007. Aspectos quantitativos da comunidade de metazoários parasitos do gordinho Peprilus paru (Linnaeus,1758) (Perciformes: Stromateidae), do litoral do estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária, vol. 16, no. 1, pp. 10-14. PMid:17588316. states that due to the complexity of marine environments, life cycle adaptations of parasites may occur. This may explain the occurrence of Hysterotylacium sp, Raphidascaris (Ichthyascaris) sp. and Goezia sp. in adult stage in lutjanids.

In conclusion, this is the first records of Raphidascaris (Ichthyascaris ) sp. and Hysterothylacium sp. in L. vivanus , of Terranova sp. in O. chrysurus, and of L. jocu and Goezia sp. in L. analis. Based on the findings of the present survey, the Brazilian northeast coast and the state of Sergipe are now included in the geographic distribution of these nematodes of fish in the country. Significant correlations between host body length and parasitic fauna for Ocyurus chrysurus and Lutjanus synagris are new data for these species.

  • (With 5 figures)

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Publication Dates

  • Publication in this collection
    18 Apr 2019
  • Date of issue
    Apr-Jun 2020

History

  • Received
    18 Jan 2018
  • Accepted
    21 Aug 2018
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