Gobioides broussonnetii (Gobiidae): a new host forPterobothrium crassicolle (Trypanorhyncha) on Marajó Island, northern Brazil

Gobioides broussonnetii (Gobiidae): um novo hospedeiro paraPterobothrium crassicolle (Trypanorhyncha) na Ilha do Marajó, Brasil

Marcela Videira Michele Velasco Lilian Dias Patrícia Matos Henrique Diniz Ferreira de Almeida Marcondes Lima da Costa Sérgio Carmona de São Clemente Edilson Matos About the authors

Abstracts

In the present study, the cestoid Pterobothrium crassicolle Diesing, 1850 (Trypanorhyncha), was observed parasitizing specimens of the violet goby (Gobioides broussonnetii Lacepède, 1800) collected from the estuary of the Paracauarí River on Marajó Island in the north of the Brazilian state of Pará, between January 2009 and December 2010. Tissue samples were analyzed, which led to identification of blastocysts containing plerocercoid larvae. These larvae were processed for scanning electron microscopy. Sixty G. broussonnetii specimens were dissected, and P. crassicolle was found in 48 (80%) of them. The violet goby,G. broussonnetii, is a new host for P. crassicolle.

Violet goby; plerocercus; Pterobothriidea


No presente estudo, o cestóide Pterobothrium crassicolle Diesing, 1850 (Trypanorhyncha) é descrito parasitando espécimes do Peixe-dragão (Gobioides broussonnetii Lacepède, 1800), coletados no estuário do rio Paracauari na Ilha de Marajó no Norte do Estado do Pará, entre janeiro de 2009 e dezembro de 2010. Amostras de tecidos foram analisadas e blastocistos contendo larvas plerocercóides foram identificados. Estas larvas foram processadas para microscopia eletrônica de varredura. Sessenta espécimes de G. broussonnetii foram analisados, e P. crassicolle foi encontrado em 48 indivíduos (80%). Este é o primeiro registro de P. crassicolle parasitando o Peixe-dragão, G. broussonnetii.

Peixe-dragão; plerocercos; Pterobothriidea


Introduction

The waters of the Amazon estuary are inhabited by both marine and freshwater fish species, which constitute an important economic resource for the region (BARTHEM, 1985Barthem RB. Ocorrência, distribuição e biologia dos peixes da Baía de Marajó, estuário amazônico. Bol Mus Paraense Emílio Goeldi Zool 1985; 2(1): 49-69.). The violet goby or dragon fish, Gobioides broussonnetii Lacepède, 1800, is the largest member of the Gobiidae and forms an important link in the food chain of this estuary. It prefers muddy bays and freshwater estuaries, but is also found at sea on muddy bottoms, widely distributed around the southern USA, Central America, the Caribbean islands and northeastern South America (BRAGANÇA, 2005Bragança AJM. Pesca, alimentação, reprodução e crescimento do Amuré, Gobioides broussonnetii Lacepède, 1800 (Pisces: Gobiidae) no Estuário Amazônico, Município de Vigia – Pará [Dissertação]. Belém: Universidade Federal do Pará; 2005.).

Trypanorhyncha is characterized by the presence of a bothridium-like scolex, with reversible tentacles, with a larval, plerocercus or plerocercoid, or post-larval stage, which can be found in teleost fish, crustaceans and, occasionally, reptiles. The adults are found in the gastrointestinal tracts of elasmobranch fish (CAMPBELL; BEVERIDGE, 1994Campbell RA, Beveridge I. Order Trypanorhyncha Diesing, 1863. In: Khalil LF, Bray RA, Jones A. Keys to the cestode parasites of vertebrates. Cambridge: CAB International; 1994. p. 51-148. PMid:7988720.).

While these parasites are well known from studies in southern Brazil (PALM, 1997Palm H. Trypanorhynch cestodes of commercial fishes from northeast brazilian coastal waters. Mem Inst Oswaldo Cruz 1997; 92(1): 69-79. http://dx.doi.org/10.1590/S0074-02761997000100014
http://dx.doi.org/10.1590/S0074-02761997...
), few data are available on their occurrence in this country's northern (Amazon) region. The present study identifies G. broussonnetii as a host of Pterobothrium crassicolle in the region of Marajó Island, in the estuary of the Amazon River in northern Brazil.

Materials and Methods

Violet goby (G. broussonnetii) specimens (n = 60) were collected monthly between January 2009 and December 2010 in the area of the estuary of the Paracauarí River in the municipality of Salvaterra, which is located on Marajó Island, in the north of the Brazilian state of Pará (0° 58′ S and 49° 34′ W) (MMA/SISBIO authorization no. 27119-1). The specimens were kept in an oxygenated aquarium filled with water from the capture site, and were subsequently transported in aerated plastic bags to the Edilson Matos Research Laboratory at the Federal University of Pará (FUPA) in the mainland city of Belém. The specimens were anesthetized with MS 222 (Sandoz Laboratories) for measurement of biometric parameters and subsequent dissection.

Tissues from host samples were analyzed using a stereomicroscope, which led to identification of blastocysts containing plerocercus larvae. These larvae were processed following the procedures recommended by Eiras (1994)Eiras JC. Elementos de Ictioparasitologia. Porto: Ed. Fundação Eng. Antônio de Almeida; 1994.. The taxonomic classification of the trypanorhynch helminths was based on the studies of Rego et al. (1974)Rego AA, Santos JC, Silva PP. Estudo de cestóides de peixes do Brasil. Mem Inst Oswaldo Cruz 1974; 72(3-4): 187-204. http://dx.doi.org/10.1590/S0074-02761974000200004
http://dx.doi.org/10.1590/S0074-02761974...
, Campbell and Beveridge (1994)Campbell RA, Beveridge I. Order Trypanorhyncha Diesing, 1863. In: Khalil LF, Bray RA, Jones A. Keys to the cestode parasites of vertebrates. Cambridge: CAB International; 1994. p. 51-148. PMid:7988720. and Palm (1997)Palm H. Trypanorhynch cestodes of commercial fishes from northeast brazilian coastal waters. Mem Inst Oswaldo Cruz 1997; 92(1): 69-79. http://dx.doi.org/10.1590/S0074-02761997000100014
http://dx.doi.org/10.1590/S0074-02761997...
. The prevalence of the parasites and the mean intensity of infection were calculated in accordance with Bush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak W. Parasitology meets ecology on its own terms: Margolis et al. Revisited. J. Parasitol 1997; 83(4): 575-583. PMid:9267395. http://dx.doi.org/10.2307/3284227
http://dx.doi.org/10.2307/3284227...
.

For scanning electron microscopy (SEM), the larvae were fixed in 5% glutaraldehyde buffered with sodium cacodylate (pH 7.2) for 12 hours at 4 °C, and then washed overnight in the same buffer solution and post-fixed in 2% OsO4 buffered with the same solution for 3 hours at 4 °C. The samples were then dehydrated in an increasing series of ethanol concentrations. The larvae were dried to the critical point, metalized with a fine (20 nm) layer of gold, and photographed in a LEO 1459 VP SEM operated at 80 kV. The specimens were also photographed in a Hitachi TM 3000 Tabletop electron microscope (Hitachi TM 3000), for which they were prepared following the same procedure, except for the metalization, which was not carried out in this case. Representative specimens of the species found were deposited in the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC no. 37845 a-b), Rio de Janeiro, RJ, Brazil.

Results and Discussion

The 60 G. broussonnetii specimens analyzed in the present study had a mean total length of 21.7 ± 4.5 cm, and 48 (80.0%) were found to be parasitized by at least one blastocyst, with mean intensity of 1.04. Fifty blastocysts were collected and processed, and all were identified as P. crassicolle, and no infections by any other helminth species were recorded. All the specimens were found in the mesentery of the fish, and it seemed that these parasites did not show any preference regarding host gender.

Taxonomy:

Superfamily Otobothrioidea Dollfus, 1942

Family Pterobothriidea Pintner, 1931

Pterobothrium crassicolle Diesing, 1850 (Figure 1a-f)

Figure 1.
Pterobothrium crassicolle. (a) Optical microscopy showing the scolex with bothria (arrows) and tentacles (arrowheads). Scale bar: 500 µm. (b) Scolex presenting pars bulbosa (*) and tentacle sheath (arrowhead). Scale bar: 500 µm.(c) Tabletop electron microscopy, showing oncotaxis of the basal area of the tentacles (*) and the beginning of the metabasal area (double arrows). Scale bar: 40 µm. (d)Oncotaxis of the basal region (*) with hooks characteristic of the species (arrowhead). Scale bar: 30 µm. (e) SEM, showing oncotaxis of the metabasal region of the tentacles. Scale bar: 25 µm. (f) Oncotaxis of the apical region of the tentacles. Scale bar: 25 µm.

Principal morphological traits of P. crassicolle based on 30 plerocerci collected from G. broussonnetii: Plerocercus with blastocyst. Scolex elongated, acraspedote, subcylindrical and narrower than the pars bothridialis. Pars bothridialis with four piriform bothria on mobile pedicles with rounded edges (Figure 1a). Pars vaginalis is long, corresponding to more than half the length of the scolex. The tentacle sheath is initially relatively smooth, with elongated bulbs. Pars postbulbosa does not overlap the pars bothridialis. Distinctive basal armature and swelling present on bothridial and antibothridial faces of tentacle; macrohooks present on antibothridial face; asymmetrical basal swelling of tentacle present. Hook files 1 (1′) widely separated, falciform; intercalary row(s) present proximally to each principal row; intercalary rows extend onto bothridial surface to merge with band of hooks occupying midline of bothridial surface of tentacle. Hooks in row 1 (1′) widely spaced, falciform; hook rows interspersed with each principal hook row, the interspersed row extending along the bothridial surface bordered with the group of hooks, occupying the median line of the bothridial surface of the tentacle (Figure 1b-d). Metabasal and apical shielding formed by the principal rows of large hooks in an alternating half-spiral arrangement, heteromorphic and hollow. Small hooks interspersed between the principal rows on both the bothrial and antibothrial surfaces (Figure 1e, f).

The morphology of the P. crassicolle specimens collected in the present study was consistent with the descriptions provided for the species by São Clemente (1986a), Rego (1987)Rego AA. Redescrição de Pterobothrium crassicolle Diesing, 1850 (Cestoda: Trypanorhyncha) e revalidação de espécie. Mem Inst Oswaldo Cruz 1987; 82(1): 51-53. http://dx.doi.org/10.1590/S0074-02761987000100008
http://dx.doi.org/10.1590/S0074-02761987...
andCampbell and Beveridge (1996)Campbell RA, Beveridge I. Revision of the family Pterobothriidae Pintner, 1931 (Cestoda: Trypanorhyncha). Invertebrate Taxonomy 1996; 10(3): 617-662. http://dx.doi.org/10.1071/IT9960617
http://dx.doi.org/10.1071/IT9960617...
. The larvae of P. crassicolle are not host-specific (PORTO et al., 2009Porto CJS, São Clemente SC, Freitas MQ, São Clemente RRB, Knoff M, Matos E. Pterobothrium crassicolle (Eucestoda: Trypanorhyncha) em corvinas, Micropogonias furnieri, comercializadas no município de Niterói, Rio de Janeiro, Brasil. Rev Bras Cien Vet 2009; 16(3): 133-135.), and have been recorded in siluriform and other estuarine and marine fish species in Brazil (DIAS et al. 2011Dias LNS, Paiva RS, São Clemente SC, Rodrigues AP, Peralta ASL, Matos E. Cestóides Trypanorhyncha parasitos de Scianideos de importância comercial, capturados no litoral amazônico, Brasil. Rev Bras Cienc Vet 2011; 18(1): 3-5.; PEREIRA Jr; BOEGER, 2005; PORTO et al., 2009Porto CJS, São Clemente SC, Freitas MQ, São Clemente RRB, Knoff M, Matos E. Pterobothrium crassicolle (Eucestoda: Trypanorhyncha) em corvinas, Micropogonias furnieri, comercializadas no município de Niterói, Rio de Janeiro, Brasil. Rev Bras Cien Vet 2009; 16(3): 133-135.; REGO, 1987Rego AA. Redescrição de Pterobothrium crassicolle Diesing, 1850 (Cestoda: Trypanorhyncha) e revalidação de espécie. Mem Inst Oswaldo Cruz 1987; 82(1): 51-53. http://dx.doi.org/10.1590/S0074-02761987000100008
http://dx.doi.org/10.1590/S0074-02761987...
; SÃO CLEMENTE, 1986a, b; SÃO CLEMENTE et al., 1997; TAKEMOTO et al., 1996Takemoto RM, Amato JFR, Luque JL. Comparative analysis of the metazoan parasite communities of leatherjackets, Oligoplites palometa, O. saurus and O. saliens (Osteichthyes: Carangidae) from Sepetiba Bay, Rio de Janeiro, Brazil. Rev Bras Biol 1996; 56(4): 639-650.).

A number of studies have recorded the presence of plerocerci ofP. crassicolle in fish collected off the coast of Brazil. In the north of the Brazilian state of Pará, this species was recorded for the first time by Diesing (1850) (reference unexamined, apud Rego, 1987Rego AA. Redescrição de Pterobothrium crassicolle Diesing, 1850 (Cestoda: Trypanorhyncha) e revalidação de espécie. Mem Inst Oswaldo Cruz 1987; 82(1): 51-53. http://dx.doi.org/10.1590/S0074-02761987000100008
http://dx.doi.org/10.1590/S0074-02761987...
) in Bagrus marinus, and Rego (1987)Rego AA. Redescrição de Pterobothrium crassicolle Diesing, 1850 (Cestoda: Trypanorhyncha) e revalidação de espécie. Mem Inst Oswaldo Cruz 1987; 82(1): 51-53. http://dx.doi.org/10.1590/S0074-02761987000100008
http://dx.doi.org/10.1590/S0074-02761987...
provided a redescription of the species in Brachyplatystoma flavicans, B. vaillantii and B. marinus. The prevalence of infection recorded in G. broussonnetii was relatively high in comparison with previous studies in southern Brazil, while the intensity was comparatively low. São Clemente (1986a, b) recorded a prevalence of 11% and mean intensity of 1.52 in whitemouth croakers (Micropogonias furnieri) from Rio de Janeiro, for example, and Porto et al. (2009)Porto CJS, São Clemente SC, Freitas MQ, São Clemente RRB, Knoff M, Matos E. Pterobothrium crassicolle (Eucestoda: Trypanorhyncha) em corvinas, Micropogonias furnieri, comercializadas no município de Niterói, Rio de Janeiro, Brasil. Rev Bras Cien Vet 2009; 16(3): 133-135. recorded values of 26.7% and 2.25, respectively, for this species from the same region (Niterói). At the southern extremity of this country, in Rio Grande, Pereira Jr. and Boeger (2005) recorded a prevalence of 66.7% and a mean intensity of infection of 5.2 in some species of sciaenid fish. The present report is the first record ofP. crassicolle infecting the violet goby, G. broussonnetii.

We are grateful to the Federal Rural University of Amazonia, Federal University of Pará, CAPES, CNPq (Edital Universal 2011), IBAMA/ SISBIO/ICMBIO and FAPESPA, and to Dr. Stephen Ferrari for translation and revision of the manuscript. The helpful suggestions and comments of the Associate Editor and reviewers are greatly appreciated.

References

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  • Bush AO, Lafferty KD, Lotz JM, Shostak W. Parasitology meets ecology on its own terms: Margolis et al. Revisited. J. Parasitol 1997; 83(4): 575-583. PMid:9267395. http://dx.doi.org/10.2307/3284227
    » http://dx.doi.org/10.2307/3284227
  • Campbell RA, Beveridge I. Order Trypanorhyncha Diesing, 1863. In: Khalil LF, Bray RA, Jones A. Keys to the cestode parasites of vertebrates. Cambridge: CAB International; 1994. p. 51-148. PMid:7988720.
  • Campbell RA, Beveridge I. Revision of the family Pterobothriidae Pintner, 1931 (Cestoda: Trypanorhyncha). Invertebrate Taxonomy 1996; 10(3): 617-662. http://dx.doi.org/10.1071/IT9960617
    » http://dx.doi.org/10.1071/IT9960617
  • Dias LNS, Paiva RS, São Clemente SC, Rodrigues AP, Peralta ASL, Matos E. Cestóides Trypanorhyncha parasitos de Scianideos de importância comercial, capturados no litoral amazônico, Brasil. Rev Bras Cienc Vet 2011; 18(1): 3-5.
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    » http://dx.doi.org/10.1590/S0074-02761997000100014
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    » http://dx.doi.org/10.1590/S0074-02761974000200004
  • Rego AA. Redescrição de Pterobothrium crassicolle Diesing, 1850 (Cestoda: Trypanorhyncha) e revalidação de espécie. Mem Inst Oswaldo Cruz 1987; 82(1): 51-53. http://dx.doi.org/10.1590/S0074-02761987000100008
    » http://dx.doi.org/10.1590/S0074-02761987000100008
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  • Takemoto RM, Amato JFR, Luque JL. Comparative analysis of the metazoan parasite communities of leatherjackets, Oligoplites palometa, O. saurus and O. saliens (Osteichthyes: Carangidae) from Sepetiba Bay, Rio de Janeiro, Brazil. Rev Bras Biol 1996; 56(4): 639-650.

Publication Dates

  • Publication in this collection
    Jul-Sep 2013

History

  • Received
    13 Apr 2013
  • Accepted
    12 June 2013
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