Parasitol Latinoam 61: 152 - 159, 2006 FLAP

ARTÍCULO ORIGINAL

Helminths of the Spotted Nothura, Nothura maculosa (Temminck, 1815) (Aves, Tinamidae) in South America

ROBERTO MAGALHÃES PINTO^*,***, MARCELO KNOFF^*, CLÁUDIA TORRES GOMES^* and DELY NORONHA^*,**

* Laboratório de Helmintos Parasitos de Vertebrados, Departamento de Helmintologia, Instituto Oswaldo Cruz. Av. Brasil, 4365, 21040-900 Rio de Janeiro, Rio de Janeiro, Brasil.
** Curadora da Coleção Helmintológica do Instituto Oswaldo Cruz.
*** Corresponding author: E-mail: rmpinto@ioc.fiocruz.br - CNPq research fellow.

ABSTRACT

This study refers to the helminth fauna of the Spotted Nothura, Nothura maculosa (Temminck, 1815), on the basis of samples deposited in the Helminthological Collection of the Oswaldo Cruz Institute, and also on bibliographical data. The helminth survey of N. maculosa is represented by the digenetic trematode Brachylaemus (Centrodes) centrodes (Braun, 1901) Travassos & Kohn, 1964, by two cestode species, one included in Hymenolepis Weiland, 1858 and the other identified as Fuhrmannetta elongata (Fuhrmann, 1908), by the nematodes Heterakis gallinarum (Schrank, 1788) Freeborn, 1923, Heterakis spiculatus (Cobbold, 1861) Travassos, 1918, Subulura olympioi Barreto, 1918, Eucoleus penidoi Freitas & Lins, 1935, Hadjelia curvata Vaz & Pereira, 1935, Hempelia hempeli Vaz, 1936, Tetracheilonema quadrilabiatum (Molin, 1858), one species included in Capillaria Zeder, 1800, and another in Trichostrongylidae Leiper, 1912; the acanthocephalan is represented by Mediorhynchus pintoi Travassos, 1923. Fuhrmannetta elongata is referred for the first time in this host since its proposal in 1908. There is a report of the finding of the habronematid nematode Procyrnea cameroni Gupta & Kazim, 1978 from N. maculosa in Brazil; the species is not illustrated taking into account the status of the original reference. The probable occurrence of the digeneans Prosthogonimus ovatus (Rudolphi, 1803), Athesmia heterolecithodes (Braun, 1899) Looss, 1899, and the nematode Heterakis brasiliana Linstow, 1899, is indicated.

Key words: Nothura maculosa, helminths, South America.

RESUMO

Este estudo diz respeito à fauna helmintológica da codorna-comum Nothura maculosa (Temminck, 1815) e é baseado em amostras depositadas na Coleção Helmintológica do Instituto Oswaldo Cruz (CHIOC) e, também, em dados bibliográficos. A helmintofauna de N. maculosa é representada pelo trematódeo digenético Brachylaemus (Centrodes) centrodes (Braun, 1901) Travassos & Kohn, 1964, por duas espécies de cestóides, uma incluída em Hymenolepis Weinland, 1858, e a outra identificada a Fuhrmannetta elongata (Fuhr-mann, 1908), por nematóides identificados a Heterakis gallinarum (Schrank, 1788) Freeborn, 1923, Heterakis spiculatus (Cobbold, 1861) Travassos, 1918, Subulura olympioi Barreto, 1918, Eucoleus penidoi Freitas & Lins, 1935, Hadjelia curvata Vaz & Pereira, 1935, Hempelia hempeli Vaz, 1936, Tetracheilonema quadri-labiatum (Molin, 1858), uma espécie incluída em Capillaria Zeder, 1800 e outra em Trichostrongylidae Leiper, 1912; o acantocéfalo é representado por Mediorhynchus pintoi Travassos, 1923. Fuhrmanneta elongata é referida pela primeira vez neste hospedeiro desde a sua proposição em 1908.

A possível ocorrência dos trematódeos digenéticos Prosthogonimus ovatus (Rudolphi, 1803), Athesmia heterolecithodes (Braun, 1899) Looss, 1899 e dos nematóides Heterakis brasiliana Linstow, 1899, Procyrnea cameroni Gupta & Kazim, 1978 é indicada. Há um registro do encontro de um nematóide habronematídeo Procyrnea cameroni Gupta & Kazim, 1978 de N. maculosa no Brasil, espécie que não é ilustrada, considerando-se a informalidade da citação.

INTRODUCTION

The Spotted Nothura, Nothura maculosa (Temminck, 1815) (Tinamiformes) is of veterinary and commercial importance, since eggs of this bird are widely accepted and considered of high nutritional value. Nothuras are found from northeast Argentina, east of Paraguay, Uruguay and east Brazil, from the States of Rio de Janeiro to Rio Grande do Sul, including the south of Mato Grosso (Campo Grande and Vacaria municipalities)¹; these birds inhabit savannahs, scrubs, caatingas as well as agricultural land. While eating seeds, they also feed on insects and ticks that are found near or on the cattle².

Specimens of this bird have been used in surveys of ectoparasites^3,4, bacteria, protozoa⁵, in investigations related to anatomy, embryology^6,7, as live baits for the collection of mosquitoes in studies of host preference and stratification of insets⁸, and also in works focusing genetic approaches⁹ . Despite of the fact that the Spotted Nothura is one of the better known of the tinamous, data on the helminths recovered from this host are remarkably scattered; thus, the present study aims to gather information regarding the helminth fauna of N. maculosa in order to provide the prompt identification of the species and promote further eventual epidemiological approaches.

MATERIALS AND METHODS

Thirteen analyzed samples (11 of nematodes, 01 of cestodes, and 01 of acanthocephalans), deposited in the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC) were collected from Brazilian specimens of N. maculosa between 1916-1970, in the States of Bahia, São Paulo, and Minas Gerais. The material was preserved either as whole mounts or wet material. Specimens under the latter condition were processed for study as described elsewhere¹⁰. Additional samples of helminths (one trematode and two nematode species) previously referred in nothuras but recovered from other tinamid hosts and deposited in the CHIOC were also analyzed. Classification of the helminths is in accordance with taxonomic keys for the parasites^11-13 and data about their host is based on the literature ^1,14,15. Most of the figures were reproduced from original papers. Values are in millimeters (mm).

RESULTS AND REMARKS

PLATYHELMINTHES,
TREMATODA, DIGENEA
Brachylaemidae Joyeux & Folley, 1930
Brachylaemus (Centrodes) centrodes (Braun, 1901) Travassos & Kohn, 1966
(Figure 1)

Remarks: This species was originally described as Harmostomum centrodes parasitizing specimens of N. maculosa and other tinamids in Brazil¹⁶. Later, a new names were proposed the new combination Brachylaemus (Centrodes) centrodes^17,18 in Brazilian specimens of N. maculosa, Crypturellus variegatus (Gmelin, 1789) (Variegated Tinamou, "inambu-chororão"), C. obsoletus (Brown Tinamou, "inambuguaçu"), Tinamus solitarius (Solitary Tinamou, "macuco"). The illustrated specimen represents CHIOC no. 17502 (whole mount), recovered from an unidentified tinamid¹⁹. Concerning other digeneans, personal communication refers to Prosthogonimus ovatus and Athesmia heterolecithodes, parasitizing specimens of N. maculosa in Argentina²⁰. Nevertheless, taking into account that these occurrences have not been confirmed so far, these species were not included in the present survey.

EUCESTODA, ORDER CYCLOPHYLIDAE
Davaineidae Braun, 1900
Fuhrmannetta elongata (Fuhrmann, 1909) (= Davainea elongata, Raillietina elongata)
(Figures 2-4)

Remarks: this is the second report of a cestode species in N. maculosa, taking into account that investigators refer to the finding of specimens, (not properly figured) allocated in Hymenolepis parasitizing Spotted Nothuras captured in Argentina⁵. In the present investigation, although some rostelar hooks were lacking in the studied specimens of F. elongata, other morphological aspects permited the diagnosis of the species. Fuhrmannetta elongata was described as Davainea elongata from South American tinamids, namely Rhynchotus rufescens (Red-winged Tinamou, "perdiz"), Nothura minor [= Nothura media] (Lesser Nothura, "codorna mineira, codorniz") and Tynamus sp. (?) in Paraguay, Uruguay an Argentina²¹. The species was listed later as Raillietina elongata²². This is a new host record for F. elongata. Original figures of the species presented here, are based on the sample CHIOC no. 30261 (wet material).

NEMATODA
TRICHINELLOIDEA
Trichuridae Railliet, 1915
Eucoleus penidoi (Freitas & Almeida, 1935) Lopez-Neyra, 1947 (= Capillaria penidoi Freitas & Almeida, 1935, Ritaklossia penidoi Freitas, 1959)
(Figures 5-7)

Remarks: the species was proposed as Capillaria penidoi²³ on the basis of nematodes recovered from the crop of a specimen of N. maculosa captured in Avaré, State of São Paulo. Although since the early 40's²⁴ the combination of the species refers to Eucoleus , the species was referred in Capillaria²⁵ in a survey of nematodes recovered from Argentinean specimens of N. maculosa. Previously has been⁵ reported to the finding of specimens of Capillaria from N. maculosa in Argentina; the nematodes probably represent E. penidoi. The species was also included in Ritaklossia²⁶, that was also considered a synonym of Eucoleus²⁷. The type material (CHIOC no. 7502, wet material) was presently revised and included as whole mounts under the no. 36509 a-c, on which the figures presented here are based.

SUBULUROIDEA
Subuluridae Yorke & Maplestone, 1926
Subulura olympioi Barreto, 1918
(Figure. 8 )

Remarks: S. olympioi seems to be the most prevalent nematode species in N. maculosa, in Brazil and in Argentina. In the present survey, 54.5% of the nematode samples were represented by S. olympioi. Nascimento et al.²⁸ referred to a prevalence of 66.5%, whereas in Argentina this value was of 45.0%²⁵.The species also occurs in other tinamid birds, namely Rhynchotus rufescens, Crypturellus parvirostris (Small-billed Tinamou, "nambu-chororó" "nambuzinho") and C. undulatus (Undulated Tinamou, "jaó")^{28, 29}. Deposited samples CHIOC no. 1118, 4611, 6217, 7794, 10485 (wet material), 30725 a-f (whole mounts). The specimen illustrated here, derives from the sample CHIOC no. 1118.

HETERAKOIDEA
Heterakidae Railliet & Henry, 1914
Heterakis spiculatus (Cobbold, 1861) Travassos, 1918 (=Heterakis valvata Schneider, 1866)
(Figures 9-10)

Remarks: although not recorded so far from Brazilian specimens of N. maculosa, the species is commonly found infecting other tinamids in Brazil [Crypturellus tataupa , (Tataupa Tinamou, "nambu-chintã"), C. noctivagus , (Yellow-legged tinamou, "jaó, zabelê" and C. variegatus]; H. spiculatus was referred ^{5, 25} as Heterakis valvata occurring in N. maculosa in Argentina. Samples of this nematode species deposited in the CHIOC were either recovered from C. variegatus or from unidentified specimens of the tinamou Crypturellus sp., captured in São Paulo in the early 1900's (CHIOC no. 9, 1415, wet material). Samples recovered from C. variegatus and C. noctivagus: CHIOC no. 32855 a-c (whole mounts) and 15879 (wet material), respectively. Specimens illustrated now represent the sample 32855 a.

Remarks: H. gallinarum is a common and outspread nematode species, found parasitizing a wide range of hosts represented by the Galliformes, Anseriformes and Timamiformes. Specimens illustrated here represent the sample CHIOC no. 32853 a-c (whole mounts), derived from the sample 20092 (wet material) recovered from the ceca of N. maculosa in 1943.

Nematodes included in Heterakis, found in tinamid birds share great similarities; concerning H. spiculatus and H. gallinarum that occur in N. maculosa, the prompt differentiation between these two species is mainly based on the size of the esophagus and spicules. In H. spiculatus the esophagus is 1.26-1.75 long and the spicules 2.36-2.56, 1.02-1.05, compared to 0.91-0.96 (esophagus) and 2.24-2.31, 0.67-0.70 (spicules) in H. gallinarum.

There is a reference of Heterakis brasiliana, occurring in an unidentified species of the genus Nothura. Taking into account that three species of this bird are referred in Brazil, namely N. maculosa, N. minor and N. boraquira [White-bellied Nothura, "codorna-do-nordeste, codorna, codorna-baiana, codorna-buraqueira, codorna-de-cabeça-preta, codornil", H. brasiliana is only cited^{13, 30}, considering the lack of reliable data on the specific host identification.

Figures 1-12. 1. Brachylaemus (Centrodes) centrodes. total. 2-4. Fuhrmannetta elongate. 2. rostelar hooks. 3. scolex. 4. mature proglottids. 5-7. Eucoleus penidoi. 5. anterior portion of male. 6. posterior extremity of male. 7. vulvar region. 8. Subulura olympioi, posterior portion of male. 9-10. Heterakis spiculatus. 9. anterior portion of female. 10. posterior portion of male. 11-12. Heterakis gallinarum. 11. anterior portion of female. 12. posterior extremity of male. Bar common to Figures 1-12 (= 1.5 in figure 1; 0.02 in figure. 2; 0.1 in figures 3, 7; 0.5 in figure. 4; 0.09 in figures 5, 6; 0.6 in figure. 8; 0.3 in figures 9, 10, 11; 0.06 in figure 12). Figure. 1. after Travassos & Kohn 17; figures 2-4: original; figures 5-7. after Freitas & Almeida23 figure 8. after Barreto29; figuress 9-12. after Vicente et al30.

HABRONEMATOIDEA
Habronematidae (Chitwood & Wehr, 1932) Ivashkin, 1961
Hadjelia curvata Vaz & Pereira, 1935
(Figures 13,14)

Remarks: the species was proposed³¹on the basis of nematodes recovered from proventriculus and gizzard of a specimen of N. maculosa captured in the State of Goiás, Brazil and the types were deposited in the Helminthological Collection of the Instituto Biológico de São Paulo under the number 1685. Vicente et al¹³, do not present illustrations of H. curvata despite of the inclusion of data after Vaz & Pereira³¹, referred erroneously as 1933 in Table XXVIII (page 179). Thus, the original figures of H. curvata are reproduced in a Brazilian periodical for the first time, since the species was proposed in an article issued in the Transactions of the American Microscopical Society, misunderstood with Transactions of the Microscopical Society of Washington (?)¹³.

There is a report of the finding of the habronematid nematode Procyrnea cameroni from N. maculosa in Brazil³⁹. This species was not figured in the present study, considering the status of the results (unpublished data, reported by the senior author in a PhD thesis.

THELAZOIDEA
Thelaziidae Skrjabin, 1915
Hempelia hempeli Vaz, 1936
(Figures 15,16)

Remarks: H. hempeli was described ³² from the eyes of Rynchotus rufescens and N. maculosa. To the date, the species was not found again in Brazil. The only specimen deposited in the CHIOC (no. 32682, wet material) is darkened, broken and derived from the type material described³², formerly deposited in the Helminthological Collection of the Instituto Biológico de São Paulo, no. 232; the material was recovered from the eyes of a specimen of N. maculosa, captured in Itararé, State of São Paulo. Taking into account the poor conditions of the sample, original figures of H. hempeli are reproduced here.

APROCTOIDEA
Aproctidae Skrjabin & Shikhobalova, 1945
Tetracheilonema quadrilabiatum (Molin, 1858) Diesing, 1861 [= Filaria hoffmanni (Mazza & Fiora, 1932)]
(Figures 17-19)

Remarks: this species was well redescribed ³³ on the basis of samples recovered from two Brazilian tinamid birds, N. maculosa and Rhynchotus rufescens. This material is deposited in the Helminthological Collection of the Instituto Biológico de São Paulo no. 1409. The present illustrations are based on this sample. Specimens of T. quadrilabiatum from N. maculosa are deposited in the CHIOC no. 36846 a-c (whole mounts), formerly 9592 (wet material) erroneously identified as Pelecitus sp and also, with the site of infection misunderstood (wing musculature); the corrections were included in the original file, since this nematode (T. quadrilabiatum), differently from specimens of Pelecitus that commonly parasitize muscles, tendons and nodules of the legs and feet or footpads of birds¹⁰, is found in the body cavity of the hosts. This is probably a case of contamination during the necropsy, when the site of the infection was not correctly determined. In Argentina, T. quadrilabiatum was referred^{5, 25,35} in N. maculosa (the species was reported³⁴ as Filaria hoffmanni). This species was the most prevalent (40%) in one investigation⁵.

Two other nematode species (neither specifically identified nor properly figured), allocated in Capillaria and in Trichostrongylidae, respectively, parasitizing Argentinean spotted nothuras were reported⁵.

PHYLUM ACANTHOCEPHALA,
ARCHIACANTHOCEPHALA,
GIGANTORHYNCHIDA
Gigantorhynchidae Hamann, 1892
Mediorhynchus pintoi Travassos, 1923
(Figures 20, 21)

Remarks: the original description of the species³⁶ was based on a broken female (CHIOC no. 4501, wet material) and males remain unknown so far. The type material was recovered from a specimen of N. maculosa captured in Minas Gerais. Mediorhynchus pintoi was referred in a survey of acanthocephalans³⁷ when data³⁸ were reproduced. Thus, other reports or new findings related to the species, since the original description, are unavailable. The sample CHIOC no. 4.501 with the type broken female was presently re-examined but no further data could be accomplished on the basis of this damaged material. Figures of M. pintoi are reproduced in accordance with Travassos³⁶.

Figures 13-21. 13-14. Hadjelia curvata. 13. anterior portion of female, 14. posterior portion of male. 15-16. Hempelia hempeli. 15. anterior portion of female. 16. posterior portion of male. 17-19. Tetracheilonema quadrilabiatum. 17. anterior portion of female. 18. anterior extremity of male. 19. posterior extremity of male. 20-21. Mediorhynchus pintoi. 20. anterior portion of female. 21. proboscis of female. Bar common to Figures 13-21 (= 0.6 in figures 13, 15; 0.3 in figures 14, 19, 21; 0.1 in figures 16, 18; 0.06 in figure 17; 1.5 in figure. 20). Figures 13, 14. after Vaz & Pereira31; figures 15, 16. after Vaz32 ; figures 17-19. after Vaz33 ; figures 20, 21. after Travassos 37.

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Acknowledgements: To Dr Alain de Chambrier, Muséum d'Histoire Naturelle, Geneva, Switzerland, for the supply of the reprint by O. Fuhrmann (1909); to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil, for the research grant to R.M. Pinto.