Parasitol Res (2012) 110:389–394 DOI 10.1007/s00436-011-2503-4

ORIGINAL PAPER

Parasites of (Osteichthyes: Cichlidae) from Brazil

Marly de Fátima Carvalho de Melo & Everton Gustavo Nunes dos Santos & Elane Guerreiro Giese & Jeannie Nascimento dos Santos & Cláudia Portes Santos

Received: 4 March 2011 /Accepted: 21 June 2011 /Published online: 12 July 2011 # Springer-Verlag 2011

Abstract Satanoperca jurupari (Osteichthyes: Cichlidae) is Sciadicleithrum satanopercae Yamada et al. 2009, the larval reported for the first time to be parasitized by the nematodes cystidicolid nematode Pseudoproleptus sp. and the adult Procamallanus (Spirocamallanus) rarus Travassos, Artigas anisakid nematode Raphidascaris (Sprentascaris) lanfrediae and Pereira, 1928, Procamallanus (Spirocamallanus) Melo et al. 2011a, b (Yamada et al. 2009; Mendoza-Franco et sp., larvae of Raphidascaroides sp. and Anisakidae gen. al. 2010;Meloetal.2011a, b). In this article, new records of sp., and by the acanthocephalan Neoechinorhynchus nematode and acanthocephalan species recovered from this (Neoechinorhynchus) paraguayensis Machado Filho fish from the Guamá River, near the delta of the River (Rev Bras Biol 19:379–381, 1959). Amazon, in Brazil, are reported.

Introduction Material and methods

The helminth fauna of the fish Satanoperca jurupari Between March 2009 and October 2010, a total of 59 specimens (Heckel, 1840) includes previous reports of the monogenean of S. jurupari, collected in the Guamá River, Belém, Pará State, ′ ″ ′ ″ : : Brazil (01°27 21 S, 48°30 14 W), were examined using a M. F. C. Melo E. G. Giese J. N. dos Santos dissecting microscope. The nematodes recovered were placed “ Laboratório de Biologia Celular e Helmintologia Profa. Dra. in physiological saline and then fixed in hot AFA (ethanol, Reinalda Marisa Lanfredi”, Instituto de Ciências Biológicas, Universidade Federal do Pará, formaldehyde and acetic acid solution). The acanthocephalans Pará, Brazil were kept in physiological saline at low temperatures (4°C) and then fixed in AFA. For light microscopy (LM), nematodes M. F. C. Melo were cleared in glycerine and, after examination, stored in 70% Laboratório de Parasitologia Doenças Negligenciadas, Faculdade de Farmácia, Instituto de Ciências da Saúde, ethanol. Acanthocephalans were stained with alcoholic Universidade Federal do Pará, chloridic carmine, cleared in beechwood creosote and Cidade Universitária, Av Augusto Corrêa n°1, Bairro Guamá, mounted in Canada balsam. Illustrations were made with the Belém, Pará 66075-110, Brazil aid of a drawing attachment on an Olympus CX31 microscope. μ E. G. N. dos Santos : C. P. Santos (*) All measurements are in micrometres ( m) unless otherwise Laboratório de Avaliação e Promoção da Saúde Ambiental, indicated, with the means in parentheses. The specimens Instituto Oswaldo Cruz, studied are deposited at the Helminthological Collection of Fiocruz, Av. Brasil 4365, Manguinhos, the Instituto Oswaldo Cruz (CHIOC), Rio de Janeiro, Brazil. Rio de Janeiro 21040-360, Brazil e-mail: [email protected]

E. G. Giese Results Laboratório de Pesquisa Dr. Carlos Azevedo, Instituto de Saúde e Produção , Universidade Federal Rural da Amazônia, Av. Tancredo Neves, 2501, The parasites of S. jurupari studied here include the Belém, Pará 66077-530, Brazil adult nematode Procamallanus (Spirocamallanus) rarus 390 Parasitol Res (2012) 110:389–394

Travassos, Artigas and Pereira, 1928 and Procamallanus Deposition of specimens: CHIOC No. 35.716. (Spirocamallanus)sp.,larvaeofRaphidascaroides sp. Raphidascaroides sp. (Fig. 2a–c) and Anisakidae gen. sp., and the acanthocephalan Neo- Female (based on two specimens). Body 8.9–9.1 mm; echinorhynchus (Neoechinorhynchus) paraguayensis maximum width 360–420. Lips 45–70 long; interlabia 14– Machado Filho 1959. 15 long (Fig. 2a). Oesophagus 910–920×150–160 (Fig. 2b). Nerve ring 340–360 and excretory pore 510 Nematoda from anterior extremity. Ventriculus 45–50×60–110; ven- tricular appendix 310–320×55–70. Vulva 1.5–1.52 mm Camallanidae Railliet and Henry, 1915 from anterior extremity. Vagina muscular, 340–345 long. Tail 300–390 (Fig. 2c). Eggs 60×50. P. (Spirocamallanus) rarus Travassos, Artigas and Pereira, Site of infection: Intestine 1928 (Fig. 1a–c) Prevalence (n=59): 1.7% (one fish with two specimens) Male (based on single specimen). Body 11.3 mm long; Deposition of specimens: CHIOC No. 35.719 maximum width 220. Cuticle striated. Buccal capsule barrel-shaped, 100×80, with four inner spiral thickenings Acanthocephala (Fig. 1a). Basal ring present. Muscular oesophagus 740× 70; glandular oesophagus 280×90. Nerve ring 290 and Neoechinorhynchidae Ward, 1917 excretory pore 437 from anterior extremity. Caudal alae 685 long. Caudal papillae pedunculate: four pairs pre-anal, four N. (Neoechinorhynchus) paraguayensis Machado Filho pairs postanal. Spicules unequal, dissimilar; large spicule 1959 (Fig. 2d–g) 585 long, distal part bifurcate with ventral outgrowth; small General. Trunk aspinose, cylindrical, enlarged at mid- spicule 212 long. Tail conical 112 long (Fig. 1b and c). body; giant hypodermal nuclei distinct (Fig. 2d and e). Site of infection: Intestine Proboscis short, slightly globular. Proboscis hooks arranged Prevalence (n=59):1.7%(onefishwithsinglespecimen) in two circles of six hooks each; anterior hooks massive, Deposition of specimens: CHIOC No. 35717 with heavy roots; middle and posterior hooks smaller, Procamallanus (Spirocamallanus) sp. (Fig. 1d–f) with discoid roots. Neck small. Single-walled proboscis Female (based on single specimen). Body 26.3 mm receptacle inserted at base of proboscis. Cephalic long; maximum width 460. Cuticle striated. Buccal ganglion at base of proboscis receptacle. Lemnisci long, capsule 100×60, with 15 inner spiral thickenings subequal. (Fig. 1d and e). Basal ring absent. Muscular oesophagus Male (based on two mature specimens). Trunk 970– 1,050×100; glandular oesophagus 1,210×100 (Fig. 1d). 1,080×360–700 (Fig. 2d and e). Dorsal and ventral Nerve ring 350 from anterior extremity. Excretory pore not tegument of equal thickness. Proboscis 80–100×80–130 observed. Vulva 10.5 mm from anterior extremity. Tail (Fig. 2f). Proboscis hooks length: largest hooks 50–83, root 238; digitiform process 35 (Fig. 1e). 33–48; middle hooks 23–25, root 3; basal hooks 18, root 3. Site of infection: Intestine Neck 38–50×70–130. Proboscis receptacle 300×80–100. Prevalence (n=59):1.7%(onefishwithsinglespecimen) Lemnisci 370×40. Testes 2, elliptical; anterior testis 230– Deposition of specimens: CHIOC No. 35.718 270×200–240; posterior testis 220–230×200–250. Synci- tial cement-gland 100–210×210–300; cement reservoir Anisakidae Railliet and Henry, 1912 140–170×100. Common seminal vesicle 150–200×75–80. Saefftigen’s pouch 225–275×60–75. Bursa 150×150. Anisakidae gen. sp. larva (Fig. 1g–i) Female (based on four gravid females). Trunk 1,032– Third-stage larvae (based on nine specimens). Body 1,586×336–656 (Fig. 2e). Proboscis 92–109×118. Probos- 6.44–11.07 (8.87) mm×200–260. Cuticle finely striated. cis hooks: largest hooks 87–92, root 18–46; middle hooks Head with cephalic tooth (Fig. 1g and h). Lips poorly 18–20, root 4–9; basal hooks 20–25, root 2–3. Neck 40– developed. Oesophagus 620–1,000×60–100 (825×84). 50×110–150. Proboscis receptacle 233–380×152–161. Ventriculus elongate, 250–380×90–120 (327×107), with Lemnisci 427–660×100–142. Uterine bell 138–141 long. oblique posterior end (Fig. 1g). Nerve ring 190–290 (225) Germinal balls 104–190×95–190. Ovejetor 103–142 from anterior extremity. Excretory pore ventral, closely long. Eggs elliptical, 29–40×9–12, with concentric shells posterior to cephalic tooth. Tail conical, 55–95 (65) long; (Fig. 2g). tip with small, 15–25 (18) μm (Fig. 1i). Site of infection: Intestine Site of infection: Intestine Prevalence (n=59): 13%, intensity of 1–10 (mean 5) Prevalence (n=59): 8.5% (five fish with 12 specimens), acanthocephalans per fish intensity 1–3 (mean 2) larvae per fish Deposition of specimens: CHIOC Nos. 37464, 37465 Parasitol Res (2012) 110:389–394 391

Fig. 1 Procamallanus (Spirocamallanus) rarus: a buccal capsule of female; f tail of female. Anisakidae gen. sp.: g, h anterior end of of male; b posterior end of male; c spicule. Procamallanus body; i posterior end of body. Scale bars: a 100 μm; b, c, f, h, i (Spirocamallanus)sp.:d anterior end of female; e buccal capsule 200 μm; d 1mm,e 250 μm, g 500 μm 392 Parasitol Res (2012) 110:389–394

Fig. 2 Raphidascaroides sp.: a anterior end with ventro-lateral lips paraguayensis: d adult male, general view; e proboscis; f adult and interlabium; b oesophagus and ventricular appendix; c caudal end female, general view; g eggs in different stages. Scale bars: a 400 μm, of female, lateral view. Neoechinorhynchus (Neoechinorhynchus) b 1 mm, c 25 μm

Discussion one feature enabled the identification of the single male found in S. jurupari. Previously, this parasite has been P. (Spirocamallanus) rarus is well characterized by the reported as occurring throughout much of the Neotropical shape of its large spicule with a bifurcate distal end. This region in freshwater fishes from Brazil, Paraguay, Argentina Parasitol Res (2012) 110:389–394 393 and Peru (Travassos and Kohn 1965; Vicente and Pinto specimens were relatively smaller than the types, i.e., trunk 1999; Vicente et al. 1985; Kohn and Fernandes 1987; of males 1.6–2.0×0.5– 0.7 mm and of females 2.9–3.8×1.1– Rodrigues et al. 1991; Thatcher 1991, 2006;Moravec1998; 1.4 mm. The specimens collected from the intestine of S. Giese et al. 2009; Eiras et al. 2010). However, this is the jurupari in the Guamá River, Pará, northern Brazil, although first record of this species parasitizing S. jurupari.The smaller (trunk of males 0.97–1.08×0.36–0.70 mm and of single adult female of Procamallanus (S.) sp. found in S. females 1.03–1.6×0.33–0.65 mm) present similar character- jurupari did not permit a specific identification. istics to N.(N.) paraguayensis, such as the general ovoid The only species of Raphidascaroides reported in the shape of the body, the male genital organs occupying ca. Neotropical region is Raphidascaroides brasiliensis 70% of the trunk, and the shape and size of the hooks. Moravec and Thatcher 1997, which was described from S. jurupari is considered a new host for the helminths the River Amazon (Moravec and Thatcher 1997), with recorded here, and N.(N.) paraguayens is reported from a juvenile specimens also being found in a siluriform fish new geographical region. from Paraguay (Moravec 1998). The females of R. brasiliensis were previously reported to have larger body Acknowledgements We are grateful to Dr David Gibson from the measurements (length 46–77 mm) than the specimens Natural History Museum, London, UK, for revision of the English. We – also thank Francisco Tiago Melo and Djane Clarys Baía from the studied here (length 8.9 9.1 mm); therefore, it is not Universidade Federal do Pará for their valuable assistance. Financial possible to ascribe a specific identification. support for the study was obtained from the PROCAD/2005, The ventriculus of Anisakidae gen. sp. larvae has an PROCAD NF/2009 programmes of the Brazilian Graduate Training oblique end, which suggests a relationship with species Council (CAPES), PROEP IOC/FIOCRUZ/CNPq and Programa Estratégico de Apoio à Pesquisa em Saúde (PAPES V), FIOCRUZ/ of Anisakis Dujardin, 1845 or Terranova Leiper and CNPq. This study is part of the doctoral thesis of the first author from Atkinson, 1914. In the former case, the ventriculus may the Programa de Pós-Graduação em Biologia de Agentes Infecciosos e be oblique and in the latter, a small dorsal caecum could be Parasitários/ICB-UFPA. growing, as pointed out by Moravec et al. (1997)incichlid fish from Venezuela. Both genera are related to marine and freshwater environments. The fish host, S. jurupari,was References collected in freshwater but in an area influenced by the tides. Brasil-Sato MC, Santos MD (2005) Metazoan parasites of Conorhyn- Anisakidae gen. sp. larvae have previously been reported chus conirostris (Valenciennes, 1840), an endemic siluriform fish from Brazil parasitising the freshwater fishes Acestrorhyn- of the São Francisco Basin, Brazil. Rev Bras Parasitol Vet chus lacustris, Auchenipterus nigripinnis, Brycon orbignya- 14:160–166 Eiras JC, Takemoto RM, Pavanelli GC (2010) Diversidade dos nus, Conorynchus conirostris, Prochilodus lineatus, parasitas de peixes de água doce do Brasil. 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Consid- Machado Filho DA (1959) Uma nova espécie do gênero “Neo- echinorhynchus” Hamman, 1892 parasita de “peixe-martim” do ering the absence of morphological characters needed to Paraguai (Neoechinorhynchidae, Archiacanthocephala). Rev Bras determine the generic identity of these larvae, we refer to Biol 19:379–381 them as Anisakidae gen. sp. Melo MFC, Giese EG, Santos JN, Portes Santos C (2011a) First The acanthocephalans species of Neoechinorhynchus record of larval Pseudoproleptus sp. (Nematoda: Cystidicolidae) in fish host. Acta Trop 117:212–215 (Neoechinorhynchus) previously reported from Brazil are: Melo, MFC, Santos, JN, Giese EG, Nunes EG, Portes Santos, C N.(N.) curemai Noronha, 1973, N.(N.) macronucleatus (2011b) Raphidascaris (Sprentascaris) lanfrediae n. sp. Machado Filho, 1954, N.(N.) paraguayensis Machado Filho (Nematoda: Anisakidae) from the fish Satanoperca jurupari 1959, N.(N.) pimelodi Brasil-Sato and Pavanelli, 1998, N. (Osteichthyes: Cichlidae). 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