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Memórias do Instituto Oswaldo Cruz
Fundação Oswaldo Cruz, Fiocruz
ISSN: 1678-8060 EISSN: 1678-8060
Vol. 96, Num. 1, 2001, pp. 81-87
Untitled Document

Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 96(1) Jan. 2001, pp. 81-87

Nematodes of Elasmobranch Fishes from the Southern Coast of Brazil

Marcelo Knoff/++, Sérgio Carmona de São Clemente/*/++, Roberto Magalhães Pinto/++, Delir Corrêa Gomes/+/++

Laboratório de Helmintos Parasitos de Vertebrados, Departamento de Helmintologia, Instituto Oswaldo Cruz, Av. Brasil 4365, 21045-900 Rio de Janeiro, RJ, Brasil *Faculdade de Veterinária, Universidade Federal Fluminense, Niterói, RJ, Brasil

+Corresponding author. Fax: +55-21-598.4363. E-mail:
++CNPq research fellows, Proc. no. 143277/97-9, 302459/88-0, 300374/80-1 and 303124/89-0, respectively.

Received 25 May 2000
Accepted 10 August 2000

Code Number: oc01009

New records for nematode species recovered from elasmobranch fishes in Brazil are established and new systematical arrangements proposed. Parascarophis sphyrnae Campana-Rouget, 1955 from the spiral valve of Sphyrna zygaena is referred for the first time in South America as a new host record. Procamallanus (S.) pereirai Annereaux, 1946, from the spiral valve of Raja castelnaui is reported parasitizing an elasmobranch host. Nematode larvae of the genera Anisakis, Contracaecum, Pseudoterranova and Raphidascaris are listed from the stomach and spiral valves of several hosts. Anisakidae larvae previously referred in Brazil in the genus Phocanema should be reallocated in Pseudoterranova. Nematodes of the genera Anisakis, Contracaecum, Pseudoterranova and Raphidascaris are reported for the first time parasitizing elasmobranchs in Brazil.

Key words: Nematoda - new records - elasmobranch fishes - Brazil

The present investigation adds new data to the study of helminth parasites of elasmobranch fishes from Brazilian marine waters. In Brazil, the only reports on parasites of these hosts are related to the cestodes of the orders Tetraphyllidea and Trypanorhyncha (Rego et al. 1974, Rego 1977, São Clemente & Gomes 1989a,b, 1992, São Clemente et al. 1991) and to the anisakid nematodes, represented by two species: Terranova trichiuri Chandler, 1935 and T. rochalimai (Pereira, 1935) Johnston and Mawson, 1945 (Vicente et al. 1985, Vicente & Pinto 1999).


In November 1984, June 1985 and July 1986, 217 elasmobranch fishes: 6 Notorynchus pectorosus (Garman, 1884) (90-130 cm of total lenght-tl), 14 Squalus megalops (Macllay, 1881) (45-59 cm tl), 37 Mustelus canis (Mitchill, 1815) (70.5-113 cm tl), 35 M. schmitti Springer, 1939 (56-98 cm tl), 37 Galeorhinus vitaminicus Buen, 1950 (86-146 cm tl), 7 Carcharhinus brachyurus (Günther, 1870) (80-108 cm tl), 16 Sphyrna zygaena (Linnaeus, 1758) (81-147 cm tl), 5 S. lewini (Linnaeus, 1758) (75-165 cm tl), 20 Squatina guggenheim (Marini, 1936) (64-87 cm tl), 20 Squatina sp. (81-125 cm tl), 12 Raja castelnaui Ribeiro, 1907 (70-103 cm tl), 1 Dasyatis say (Lesseur,1817) (58 cm tl) and 1 D. centroura (Mitchill, 1815) (103 cm tl) were captured in the coast of the State of Rio Grande do Sul (30°40'S-33°40'S and 50°40'W-53°20'W; 12-100 m depth), by professional fishermen of the oceanographic ship Atlântico Sul. In March 1998, 46 elasmobranch fishes: 1 Hexanchus griseus (Bonnaterre, 1788) (132 cm tl), 7 Heptranchias perlo (Bonnaterre,1788) (87-107.4 cm tl), 16 Squalus sp. (41-67 cm tl), 9 Scyliorhinus haeckeli (Ribeiro, 1907) (41.5-54.5 cm tl), 5 Carcharhinus signatus (Poey, 1868) (120-150 cm tl) and 8 Dipturus trachyderma (Krefft and Stehmann, 1975) (133.5-176 cm tl) were captured about 125 miles off the littoral of State of Paraná (25°50'S-25°52'S and 45°23'W-45°25'W; 200-500 m depth), by professional fishermen of the fishing boat Icanhema VI. Parasites were collected, fixed, stained and mounted following Amato et al. (1991). The classification of the nematode parasites considered herein is that of Yamaguti (1961), Chabaud (1975 a, b), Hartwich (1974), Anderson (1992). The prevalence, intensity and mean intensity of infection are indicated in accordance to Bush et al. (1997). The drawings were made with a camera lucida connected to an Olympus BH-2 microscope. All measurements are in millimeters; ranges of measurements are followed by mean values (when indicated) within parentheses. Voucher specimens were deposited in the Coleção Helmintológica do Instituto Oswaldo Cruz (CHIOC), Fiocruz, Rio de Janeiro, RJ, Brazil. Deposited anisakidid larvae refer to one sample from each host species. Host specimens collected between 1984 and 1986 were determined on board by Dr Carolus Maria Vooren and were not deposited. Host specimens collected in 1998 and 1999 were determined by Drs Alberto Ferreira Amorim and Carlos Arfelli and at least one specimen of each species of these fishes was deposited as voucher host in the Coleção Ictiológica do Instituto de Pesca, Santos, SP, Brazil: D. trachyderma no. IP1961; C. signatus no. IP1962; H. perlo no. IP1963; H. griseus no. IP1964; Squalus sp. no. IP1965; S. haeckeli no. IP 1966.


Cystidicolidae Skrjabin,1945
Parascarophis sphyrnae Campana-Rouget, 1955
(Figs 1-3)

Description of specimen (based on one female). Female: body 30.0 long, maximum width 0.144. Head with a cap-like cuticular expansion which extends backwards rather dorsally than ventrally, dorsal face 0.050 long and ventral face 0.020 long. Buccal capsule 0.220 long. Esophagus 4.0 long without a clear distinction between muscular and glandular portions. Nerve ring 0.216 from anterior extremity. Vulva at the mid anterior portion of the body, 19.7 from anterior extremity. Ovijector directed upwards and then turning downwards, near its connection with the opposed uterus. Eggs thin-shelled, embryonated, 0.025-0.029 long by 0.011-0.014 wide, without polar filaments. Anus 0.160 from posterior extremity. Excretory pore not observed.

Host: Sphyrna zygaena (Sphyrnidae)
Site of infection: spiral valve
Locality: littoral of the State of Rio Grande do Sul, Brazil
Prevalence (P) = 6.2%
Intensity of infection (I) = 1
Number of specimens recovered: 1 female
Specimen deposited: CHIOC No. 34263 (voucher) - whole mount.

Camallanidae Railliet & Henry, 1915
Procamallanus (S.) pereirai Annereaux, 1946
(Figs 4-7)

Description of specimens (based on one male and five females). Male: body 10.67 long, maximum width near midlength 0.158. Buccal capsule 0.090 long by 0.061 wide, 14 spiral bands. Esophagus 1.09 long, muscular anterior portion of esophagus 0.489 long and glandular posterior portion 0.604 long. Nerve ring 0.226 from anterior extremity. Caudal alae wide, continuous anteriorly with symetrical pair of pedunculated papillae; precloacal pairs three, postcloacal six pairs. Spicules unequal and similar. Longer spicule 0.420 and shorter spicule 0.220 long. Cloaca 0.144 from posterior extremity. Tail possessing two small spines. Female: body 13.3 - 17.8 long, maximum width at its middle, 0.273-0.360. Buccal capsule 0.100 - 0.108 long by 0.086 - 0.090 wide, with 14 spiral bands. Muscular anterior portion of esophagus 0.518 - 0.576 long and glandular posterior portion 0.763 - 0.864 long. Nerve ring 0.237 - 0.316 from anterior extremity. Vulva 6.99 from anterior extremity. Ovijector long directed downwards. Rectum 0.108 - 0.144 long. Anus 0.140 - 0.180 from posterior extremity. Tail with two spines.

Host: Raja castelnaui (Rajidae)
Site of infection: spiral valve
Locality: coast of the State of Rio Grande do Sul, Brazil
Prevalence (P) = 25%
Mean intensity of infection (MI) = 2
Number of specimens recovered: 1 male, 5 females
Specimens deposited: CHIOC No. 34264, 34265a, b, c and 34266 (vouchers) - whole mounts.

Anisakidae Skrjabin & Karokhin,1945

Data on the number of specimens of Anisakidae nematode larvae (infrapopulation) in elasmobranch hosts collected between 1984 and 1986 (State of Rio Grande do Sul) and 1998 (State of Paraná) in the Southern Brazil and their number of deposit in the CHIOC are presented in Table I. Prevalence, intensity or mean intensity of infection in elasmobranch hosts are on the Tables II and III for those necropsies performed in 1984-1986 and 1998, respectively. Fishes collected in March 1999 from State of Santa Catarina were negative to Anisakidae nematode larvae.

Anisakinae Railliet & Henry, 1912
Anisakis Dujardin, 1845
Anisakis sp.

Hosts: Hexanchus griseus (Hexanchidae); Heptranchias perlo (Heptranchidae); Squalus megalops (Squalidae); Mustelus canis (Triakidae); Galeorhinus vitaminicus (Triakidae); Carchar-hinus signatus (Carcharhinidae); Dipturus trachyderma (Rajidae); Squatina sp. (Squatinidae).

Contracaecum Railiet & Henry, 1912
Contracaecum sp.

Hosts: Hexanchus griseus (Hexanchidae); Heptranchias perlo (Heptranchidae); Scyliorhinus haeckeli (Scyliorhynidae); Mustelus canis (Triakidae); Mustelus schmitti (Triakidae); Galeorhinus vitaminicus (Triakidae); Carchar-hinus brachyurus (Carcharhinidae); Carcharhinus signatus (Carcharhinidae); Sphyrna zygaena (Sphyrnidae); Dipturus trachyderma (Rajidae); Squatina sp. (Squatinidae).

Pseudoterranova Mosgovoy, 1950
Pseudoterranova sp.

Hosts: Squalus megalops (Squalidae); Mustelus canis (Triakidae); Mustelus schmitti (Triakidae); Galeorhinus vitaminicus (Triakidae).

Raphidascarinae Hartwich,1954
Raphidascaridinea Chabaud, 1965
Rhaphidascaris Railiet & Henry, 1915
Rhaphidascaris sp.

Hosts: Scyliorhinus haeckeli (Scyliorhynidae); Galeorhinus vitaminicus (Triakidae); Raja castelnaui (Rajidae); Dipturus trachyderma (Rajidae).


Description of P. sphyrnae was based on female specimens parasitizing the spiral valve of S. diplana from the coast of Senegal (Campana-Rouget 1955a, b). Our specimen from the spiral valve of S. zygaena is 2.5 times longer than those from Senegal, but in accordance to established morphological parameters for the species. This is the first report of P. sphyrnae in South America and in the new host species. Procamallanus (S.) pereirai has been reported from a variety of hosts and different geographical localities (Annereaux 1946, Sogandares-Bernal 1955, Noble & King 1960, Hutton 1964, Joy 1971, 1974, Yin 1983, Sood 1989, Frost & Dailey 1994). In Brazil this nematode was referred parasitizing Paralonchurus brasiliensis (Pinto et al. 1984, Vicente et al. 1985). Larval stages of P. (S.) pereirai have been reported in Brazil for the teleosts Stellifer brasiliensis, Nebris microps, Porichthys porosissimus, Symphurus tesselatus and Menticirrus americanus (Santos et al.1999). Procamallanus (S.) pereirai is here referred for the first time from an elasmobranch host. The Anisakidae larvae reported herein represent the genera Anisakis, Contracaecum, Pseudo-terranova and Raphidascaris. Considering the life-cycle of these nematodes (Anderson 1992) it is possible to suppose that the third-stage larvae are ingested with the intermediate fish hosts. Several anisakid species have been referred from freshwater and marine fishes in Brazil (Vicente et al. 1985, Barros & Amato 1993, São Clemente et al. 1994, 1995a, b, 1996, Vicente & Pinto 1999). According to Gibson (1983), Pseudoterranova must be recognized as the oldest available name for Phocanema and based on this fact, species previously referred to the genus Phocanema should be reallocated in Pseudoterranova. This is the first report of anisakid nematodes of the genera Anisakis, Contracaecum, Pseudoterranova and Raphidascaris parasitizing elasmobranchs in Brazil, considering that only T. trichuri Chandler, 1935 and T. rochalimai (Pereira, 1935) Johnston and Mawson, 1945 were previously referred from these hosts (Vicente et al. 1985). Thus, the occurrence of the larvae studied herein, represents new records for Brazilian hosts.


To Dr Carolus Maria Vooren from the Universidade do Rio Grande, State of Rio Grande do Sul, for the identification of fishes captured between the years 1984-1986, to Drs Alberto Ferreira Amorim and Carlos Arfelli from the Instituto de Pesca, Santos, State of São Paulo, for the identification of fishes captured between the years 1998-1999 and to the fishermen of the research ship Atlântico Sul of the Fundação Universidade do Rio Grande and of the fishing boat Icanhema VI from Santos, both for helping during capture of hosts.


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Financial support: CNPq Proc. no. 571491/97-9
The authors dedicate this paper in honor of the Oswaldo Cruz Institute, on the occasion of the centenary of its foundation, May 25th 1900.

Copyright 2001 Fundacao Oswaldo Cruz Fiocruz

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