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Memórias do Instituto Oswaldo Cruz
Fundação Oswaldo Cruz, Fiocruz
ISSN: 1678-8060 EISSN: 1678-8060
Vol. 90, Num. 3, 1995, pp. 389-393
Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 90(3): 389-393, may/jun. 1995

Nematode Parasites of Brazilian Ciconiiformes Birds: a General Survey with New Records for the Species

J Julio Vicente, Roberto Magalhaes Pinto , Dely Noronha, L Goncalves

Departamento de Helmintologia, Instituto Oswaldo Cruz, Av. Brasil 4365, 21045-900 Rio de Janeiro, RJ, Brasil

Code Number: OC95076 Size of Files: Text: 18K Graphics: Line Drawings (gif) 61K

This report deals with the identification of one hundred and fifty-nine samples of nematodes recovered from Brazilian egrets and herons. Contracaecum microcephalum, C. multipapillatum, C. plagiaticium, Desportesius invaginatus, D. longevaginatus, Desmidocercella ardeae, Eustrongylides ignotus, Portocaecum reticulatum, Tetrameres micropenis, Capillaria sp. Contracaecum sp. Portocaecum sp. Procymea sp., Tetrameres sp. and Viktorocara sp. were studied The genus Viktorocara and the species C. microcephalum, C. plagiaticium, D. invaginatus, D. ardeae and P. reticulatum are referred in Brazil for the first time.

Key words: nematodes - Ciconiifonnes - birds - new records - Brazil

The present investigation refers to the nematodes recovered from egrets and herons. These hosts generally inhabit tropical environments; some species have been listed among those endangered of extinction and were captured during early institutional scientific expeditions to the Brazilian hintherlands, mostly in the first half of this century, generally conducted by Dr Lauro Travassos and Dr JF Teixeira de Freitas.

MATERIALS AND METHODS

One hundred and fifty-nine samples recovered between 1921 and 1961 in Brazilian north, southeastern and mid-eastern regions and deposited in the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC) were studied. Specimens are kept in numbered vials, matched with respective numbered files that contain data on the unidentified samples, regarding host, site of infection, locality of capture, preservative soIntion, date of necropsy and name of the collector. The source of samples according to host family is: ARDEIDAE: 27 from Ardea cocoi L.; 21 from Butoricles s. striatus (L.); 7 from Casroeradius albus egreua (Gmelin); 9 from Egreua t. thula (Molina); 2 from Ixobrychus exilis erythromelas (Vieillot); 2 from Nyctanassa violacea cayennensis (Gmelin); 38 from Nycticorax nycticorax hoactli (Gmelin); 4 from Pilherodius pileatus (Boddaefi); 2 from Syrigma sibilatrix (Temminck); 14 from Tigrisoma lineatum marmoratum (Vieillot); 3 from Tigrisoma sp. CI-CONIIDAE: 13 from Euxenura maguari (Gmelin); 1 from Jabiru mycteria (Lichtenstein); 5 from Mycteria americana L.; COCHLEARIIDAE: 7 from Cochlearius C. cochlearius (L.); THRESKIORNITHIDAE: 1 from Phimosus infuscatus nudifrons (Spix); 3 from Theristicus c. caudatus (Boddaert).

Nematodes were preserved in Railliet & Henry solution, (0.85% NaCl solution: 93 ml; formaldehyde: 5 ml; glacial acetic acid: 2 ml) and were processed for study as described elsewhere (Vicente et al. 1993). NHR and NGD indicate New Host Record and New Geographical Distribution, respectively. Classification and common names of hosts follow Pinto (1978) and Sick (1984). Confirmation of the taxonomic status of the nematodes was based on Hartwich (1974), Chabaud (1975), Anderson and Bain (1976, 1982). Specific diagnosis was achieved by comparison of the morphometric data actually obtained with those referred in the original descriptions and/or redescriptions, as well as with deposited type specimens whenever available in the CHIOC.

RESULTS

Eustrongylides ignotus Jagerskiold, 1909 (Dioctophymatoidea, Dioctophymatidae, Eustrongylinae)

Host: Euxenura maguari - NHR

Other hosts were listed by Rego and Vicente (1988).

Site of infection: gizzard.

Locality: Bartanco Alto, State of Mato Grosso do Sul, Brazil.

Specimens studied: CHIOC no. 33180a-b, 33181 a-b (whole mounts).

Contracaecum microcephalum (Rudolphi, 1819) Baylis, 1920 (Ascaridoidea, Anisakidae, Anisakinae) (Fig. 1 k )

Hosts: Butorides s. striatus (L.); conh-non name: striated heron ("socozinho, maria-mole, anavelha, joao-manuel") - NHR; Casmerodius albus egretta (G-melin) (- Ardea egretta); common name: great egret ("garca branca grande, guiratinga") - NHR; Egretta t. thula (Molina) (- Leucophoyx t. thula); common name: snowy egret ("garca branca pequena") - NHR. Site of infection: intestine.

Localities: State of Amazonas, Angra dos Reis, State of Rio de Janeiro, Mara jo Island, State of Para, Porto Cabral, State of Sao Paulo, Salobra, State of Mato Grosso do Sul, Brazil - NGD. Specimens studied: CHIOC no. 33162a-f, 33163a-b (whole mounts); 9456, 11785, 14698, 14976, 15038, 18007, 21174 (wet material).

Although reported from a wide range of hosts, with a large geographical distribution (Cram 1927) this is the first record of C. microcephalum in South America.

Contracaecum multipapillatum (Drasche, 1882) Baylis, 1920

Hosts: Ardea cocoi L.; common name: whitenecked heron ("maguari, baguari, soco-grande") NHR; Cochlearius c. cochlearius (L.) (=Cancroma cochlearia); common name: boat-billed heron ("tamatia, tamatiao"); Nycticorax nycticorax hoactli (Gmelin); common name: heron ("guacuru, soco dorminhoco, taiacu, taquiri") NHR.

Site of infection: intestine.

Localities: State of Mato Grosso do Sul, Angra dos Reis, State of Rio de Janeiro, Brazil.

Specimens studied: CHIOC no. 33 157a-i, 33158a-b, 33159a-b (whole mounts); 8318, 12979, 13021, 13022, 14189, Ea.8, 14458, 15036, 15585 (wet material).

Contracaecum plagiaticium Lent & Freitas, 1948 (Fig. 1 c, d )

Hosts: Nycticorax nycticorax hoactli - NHR; Pil- herodigs pileatus (Boddaert); common name: capped heron ("garca real") - NHR. Site of infection: stomach (?).

Localities: States of Mato Grosso do Sul and Rio de Janeiro, Brazil - NGD.

Specimens studied: CHIOC no. 33160a-f, 33161 (whole mounts); 8636, 12635 (wet material).

Contracaecum plagiaticium was described from Uruguay, parasitizing Nycticorax nycticorax naevius (Boddaert) (Lent & Freitas 1948) and is referred for the first time in Brazil.Porrocaecum reticulatum (Linstow, 1899) Baylis & Daubney, 1922 (Ascaridoidea, Ascarididae, Toxocarinae) (Fig. 1 i, j )

Hosts: Ardea cocoi; Egretta t. thula - NHR; Casmerodigs albgs egretta - NHR; Nycticorax nycticorax hoactli; Tigrisoma lineatum marmoratum (Vieillot); common name: rulescent tiger heron ("soco-boi, taiacu") - NHR.

Localities: State of Mato Grosso do Sul, Marajo Island, State of Para, Brazil - NGD.

Specimens studied: CHIOC no. 33164, 33165, 33166a-d, 33167a-b, 33168 (whole mounts); 9462, 11786, 12985, 15037, 15047, 15263,18006, 26428 (wet material).

This is a very peculiar species, considering that the presence of an accessory piece in addition to the two spicules in an ascarid is highly remarkable (Baylis & Daubney 1922). This is the first report of P. reticulatum in South America.

Tetrameres micropenis Travassos, 1925 (Habronematoidea, Tetrameridae, Tetramerinae)

Host: Nyctanassa violacea cayennensis (Gmelin); common name: yellow-crowned night heron* ("sabacu, tamatiao, matirao").

Site of infection: gizzard.

Locality: Rio de Janeiro, State of Rio de Janeiro, Brazil.

Specimens studied: CHIOC no. 9860 (wet material).

Desportesius invaginatus (Linstow, 1901 ) Chabaud & Campana, 1949 (Acuarioidea, Acuariidae, Acuariinae) (Fig. 1 e, f )

Host: Egretta t. thula - NHR.

Site of infection: gizzard.

Localities: Manarts, State of Amazonas, Rio de Janeiro, State of Rio de Janeiro, Brazil - NGD.

Specimens studied: CHIOC no. 33170a-d, 3 3171 a-d (wholemounts).

D. invaginatus has been reported from several ciconiiform hosts from Europe, Asia, Africa and USA (Wong & Anderson 1986). This is the first record of the species in South America.

Desportesius longevaginatus (Molin, 1860) Wong & Anderson, 1986

Hosts: Euxenura maguari (Gmelin); common name: maguari stork ("baguari, cauaua, jaburu moleque, cegonha"); Mycteria americana L.; common name: stork ("passarao, cabeca seca, cabeca de pedra")-NHR.

Site of infection: gizzard.

Localities: Barranco Alto and Salobra, State of Mato Grosso do Sul, Brazil.

Specimens studied: CHIOC no. 33172a-i (whole mounts); 14471, 14484, 14591, 14594, 15009, 15606 (wet material).

Desmidocercella ardeae (Na wrotzky, 1914) Yorke & Maplestone, 1926 (Aproctoidea, Desmidocercidae) (Fig. 1 a,b)

Host: Ardea cocoi - NHR.

Site of infection: body cavity (extemal intestinal surface).

Localities: Maraj6 Island, State of Para, State of Mato Grosso do Sul, Brazil - NGD.

Specimens studied: CHIOC no. 33169a-d (whole mounts), 13503 (wet material).

The occurrence of the genus Desmidocercella Yorke and Maplestone, 1926 is assigned for the .first time in a Brazilian host. The species has been included in Pharyngosetaria Lubimov, 1937, which is, actually, considered a synonym of the former genus, according to Chabaud and Anderson (1959).

Specimens which could not be identified to the already referred species, due to their poor state of preservation, are distributed in the following genera.

Capillaria sp.

(Trichinelloidea, Trichuridae, Capillariinae)

Host: Theristicus c. caudatus (Boddaezt); common name: buff-necked ibis ("curicaca").

Site of infection: stomach.

Locality: Salobra, State of Mato Grosso do Sul, Brazil.

Specimens studied: CHIOC no. 11770 (wet material).

Contracaecum sp.

Hosts: Ardea cocoi, Butorides s. striatus, Casmerodius albus egretta, Cochlearius c. cochlearius, Egretta t. thula, Euxenura maguari, Jabiru mycteria (Lichtenstein); common name: jabiru stork ("tuiuiu, jaburu"), Nyctanassa violacea cayennensis, Nycticorax nycticorax hoactli, Pilherodius pileatus, Tigrisoma lineatum nrtttoratun Tigrisoma sp.; common name: heron ("soco").

Sites of infection: intestine, stomach (?).

Localities: States of Mato Grosso do Sul, Para,

Rio de Janeiro, Sao Paulo, Brazil.

Specimens studied: CHIOC no. 33176a-b, 33177a-b, 33178a-d, 33179 (whole mounts); 84, 2723, 2724, 3219, 4975, 5983, 6174, 7411, 7985, 8239, 8242, 8243, 8248, 8633, 8635, 8679, 8684, 8688, 8693, 8706, 8707, 8712, 8715, 8716, 8718, 8720, 8760, 8771, 8822, 9477, 9674, 9795, 11721, 11769, 11771, 11778, 11780-11782,12775, 13075, 13152, 13244, 13480, 13482, 14191, 14194, 14195, 14202, 14468, 14484, 14555, 14576, 14579, 14604, 14653, 14966, 14970, 14972, 14975, 15039, 15042, 15516, 15592, 17996, 20459, 29158*, 30145 ( wet material); * from the Zoological Garden of Rio de Janeiro.

Porrocaecum sp.

Hosts: Ardea cocoi, Cochlearius c. cochlearius, Egretta t. thula, Ixobrychus exilis erytromelas (Vieillot) (= Ardetta erytromelas); common name: least bittem ("soco-mirim vermelho").

Sites of infection: intestine, stomach (?).

Locality: State of Mato Grosso do Sul, Brazil.

Specimens studied: CHIOC no. 6676, 6677, 8102, 8144, 8638, 11352, 12448, 12636, 12980, 13074, 13257, 13258, 15531, 15533 ( wet material ).

Procyrnea sp. (Habronematoidea, Habronematidae, Habronematinae)

Hosts: Euxenura maguari, Euxenura sp.

Site of infection: gizzard.

Localities: Bartanco Alto and Salobra, State of Mato Grosso do Sul, Brazil.

Specimens studied: CHIOC no. 33174a-d (whole mounts); 9461, 14468, 14471, 14484, 14591 (wet material).

Tetrameres sp.

Hosts: Phimosus infuscatus nudifrons (Spix) ('Ibis nudifrons); common name: bare-faced ibis ("coro-coro"); Syrigma sibilatrix (Temminck); common name: whistling heron ("maria faceira"), Theristicus c. caudatus.

Site of infection: gizzard.

Locality: State of Mato Grosso do Sul, Brazil.

Specimens studied: CHIOC no. 8699, 11501, 13098 (wet material).

Viktorocara sp. (Acuarioidea, Acuariidae, Schistorophinae) (Fig. 1 g, h )

Host: Syrigma sibilatrix - NHR.

Site of infection: gizzard.

Locality: State of Mato Grosso do Sul, Brazil -NGD.

Specimen studied: CHIOC no. 33175 (whole mount)

    Fig. 1: Desmidocercella ardeae. a: anterior potion of female, lateral view. b: posterior portion of male, lateral view. Contracaecum plagiaticium. c: posterior potion of male, lateral view. d: anterior portion of male, lateral view. Desportesius invaginatus. e: anterior extremity of male, lateral view. f: posterior portion of male, lateral view. Viktorocara sp. g: anterior extremity of female, lateral view. h: posterior extremity of female, lateral view. Porrocaecum reticulatum. i: posterior extremity of male, lateral view. j: anterior portion of male, lateral view. Contracaecum microcephalum. k: posterior portion of male, lateral view. (Bars-in mm: 0.05 in fig. h; 0.1 in figs b, g; 0.2, in figs a, c, e, f; 0.5 in firs d.i. k: 1 in fig. j.

The genus Viktorocara Guschanskaya, 1950 has been reported from birds representing the families Charadriidae, Icteridae and Scolopacidae from Europe, Cuba, USA and Canada ( Wong & Lankester 1984). This is the first report of the genus in South America.

Other nematode species reported from Ciconiiformes in Brazil and not found during the present study:

Capillaria brasiliana Freitas, 1933, from Nycticorax nycticorax hoactli; C. venteli Freitas & Almeida, 1935, Dispharynx magnilabiata (Molin, 1860) Gendre, 1920 from Ajaia ajaja (L.) (=Platalea ajaja); common name: roseate spoonbill ("colhereiro, ajaja"); Euslrongylides perpapillalus Jagerskiold, 1909 from Ardea leuca (?), Casmerodius albus egretla; Hystrichis acantocephalicus Molin, 1861 from Phimosus i. infuscatus (Lichentenstein); common name: green ibis ("tapicuru, macarico preto"), Phimosus infuscatus nudifrons ( Cram 1927, Freitas 1933, Freitas & Almeida 1935, Rego & Vicente 1988).

REFERENCES

Anderson RC, Bain O 1976. Keys to the genera of the order Spirurida. Diplotriaenoidea, Aproctoidea and Filarioidea. p. 59-116. In RC Anderson, AG Chabaud, S Willmort (eds). CIH Keys to the nematode parasites of vertebrates. Part 3. Commonwealth Agricultural Bureaux, England.

Anderson RC, Bain O 1982. Keys to genera of the superfamilies Rhabditoidea, Dioctophymatoidea, Trichinelloidea and Muspiceoidea. p. 1-26. In RC Anderson, AG Chabaud, S Willmott (eds). CIH Keys to the nematode parasites of vertebrates. Part 9. Commonwealth Agricultural Bureaux, England.

Baylis HA, Daubney R 1922. Report on the parasitic nematodes in the collection of the zoological survey of India. Mem Indian Mus 7: 263-347.

Chabaud AG 1975. Keys to the genera of the order Spimrida. Spiruroidea, Habronematoidea and Acuanoidea. p. 29-58. In RC Anderson, AG Chabaud, S Willmott (eds). CIH Keys to the nematode parasites of vertebrates. Part 3. Commonwealth Agricultural Bureaux, England.

Chabaud AG, Anderson RC 1959. Nouvel essai de classification des Filaires (Superfamille des Filarioidea) II. Ann Par hum comp 34: 64-87.

Cram EB 1927. Bird parasites of the suborder Strongylata, Ascaridata and Spirerata. US Nat Mas Bull 140: 1-465.

Freitas JlTr 1933. Nouvelles especes du genre Capillaria Zeder, 1800. CRSB Rio de Janeiro 114:1195-1196.

Freitas JFT, Almeida JL 1935. Sobre os nematoda parasitas de esofago e papo de aves. Mem Inst Oswaldo Cruz 30:. 123-156.

Hartwich G 1974. Keys to the genera of the Ascaridoides. p. 1-15. In RC Anderson, AG Chabaud, S Willmott (eds). CIH Keys to the nematode parasites of vertebrates. Part 2. Commonwealth Agricultural Bureaux, England.

Lent H, Freitas JFT 1948. Uma colecao de nematodeos parasitas de vertebrados do Museu de Historia Natural de Montevideo. Mem Inst Oswaldo Cruz 46: 1-71.

Pinto OMO 1978. Novo catalogo das aves do Brasil 1. Empresa Grafica da Revista dos Tribunais, Sao Paulo, 446 pp.

Rego AA, Vicente JJ 1988. Eastrongylides ignotas Jagerskiold, 1909 (Nematoda: Dioctophymatoidea), parasito de peixes, anfibios, repteis e aves. Distribuicao e taxonomia. Ciencia e Cultura 40. 478-483.

Sick H 1984. Ornitologia brasileira, uma introducao. 1. Universidade de Brasilia, 474 pp.

Vicente JJ, Pinto RM, Noronha D 1993. Remarks on six species of heterakid nematodes parasites of Brazilian tinamid birds with a description of a new species. Mem Inst Oswaldo Cruz 88: 271-278.

Wong PL, Anderson RC 1986. Revision of the genus Desportesius Chabaud and Campana, 1949 (Nematoda: Acuarioidea) mainly from the gizzard of ciconifonn birds. Can J Zool 64: 2520-2530.

Wong PL, Lankester MW 1984. Revision of the genus Viktorocara Guschanskaya, 1950 (Nematoda: Acuarioidea). Can J Zool 62:2541-2549.

Copyright 1995 Fundacao Oswaldo Cruz


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