Helminth parasites of Galictis cuja (Carnivora, Mustelidae), from localities in the Atlantic forest of Brazil

Helmintos parasitos de Galictis cuja (Carnivora, Mustelidae), em localidades de Mata Atlântica no Brasil

Pilar Corrêa Cecília Bueno Fabiano Matos Vieira Luís Cláudio Muniz-Pereira About the authors

Abstract

The current study aimed to investigate the helminth parasites of a population of Galictis cuja (Carnivora, Mustelidae) that occur in Atlantic Forest in the Southeastern region of Brazil. We necropsied 18 specimens of G. cuja, collected between January 2009 and May 2014, ran over victims on BR-040 highway, between the municipalities of Duque de Caxias, state of Rio de Janeiro and Juiz de Fora, state of Minas Gerais, localities inserted in Atlantic rainforest Biome. A total of six species of helminths were identified: Dioctophyme renale, Molineus elegans, Physaloptera sp., Strongyloides sp., Platynosomum illiciens, and Pachysentis gethi. Molineus elegans, Physaloptera sp. and P. illiciens were recorded for the first time in this host. Data provided in the current study when compared to the previous reports of parasitism by helminths in G. cuja in Brazil demonstrate that this study is the most representative with this host species.

Keywords:
Galictis cuja; helminth; BR-040 highway; road kill; wild mammal; Brazil

Resumo

O presente estudo teve como objetivo investigar a fauna de helmintos de uma população de Galictis cuja (Carnivora, Mustelidae) que ocorre em uma região de Mata Atlântica na região Sudeste do Brasil. Foram necropsiados 18 espécimes de G. cuja, coletados entre Janeiro de 2009 e Maio de 2014, que foram mortos acidentalmente por atropelamentos na rodovia BR-040, entre os municípios de Duque de Caxias, no Estado do Rio de Janeiro e Juiz de Fora, no Estado de Minas Gerais, localidades inseridas no Bioma Mata Atlântica. No total seis espécies de helmintos foram identificadas: Dioctophyme renale, Molineus elegans, Physaloptera sp, Strongyloides sp, Platynosomum illiciens e Pachysentis gethi. Molineus elegans, Physaloptera sp. e P. illiciens foram registradas pela primeira vez nesta espécie de hospedeiro. O estudo amplia a diversidade de helmintos conhecidos para o hospedeiro em questão. Os dados fornecidos no presente estudo quando comparados com os registros prévios de helmintos em G. cuja no Brasil demonstram que este estudo é o mais representativo com esta espécie de hospedeiro.

Palavras-chave:
Galictis cuja; helmintos; rodovia BR-040; atropelamento; mamífero silvestre; Brasil

Introduction

The lesser grison, Galictis cuja (Molina, 1872) (Carnivora, Mustelidae), is the smallest representative of the family Mustelidae. It is restricted to South America, with distribution from northeastern Brazil to southern Peru, western Bolivia, central and southern Chile, Paraguay, Uruguay, Argentina, and southeastern Brazil, at elevations from sea level to 4200 m, and habitats from Atlantic Forest, and cold steppe in Patagonia to exotic forest plantations in Chile (YENSEN & TARIFA, 2003Yensen E, Tarifa T. Galictis cuja. Mamm Species 2003; 728: 1-8. http://dx.doi.org/10.1644/728.
http://dx.doi.org/10.1644/728...
; PREVOSTI & TRAVAINI, 2005Prevosti FJ, Travaini A. New records of (Molina, 1782) (Carnivora, Mustelidae) in southern Patagonia. Galictis cujaMamm Biol 2005; 70(5): 317-320. http://dx.doi.org/10.1016/j.mambio.2005.03.004.
http://dx.doi.org/10.1016/j.mambio.2005....
; NABTE et al., 2009Nabte MJ, Saba SL, Monjeau A. Mamíferos terrestres de la Península de Valdés: lista sistemática comentada. Mastozool Neotrop 2009; 16(1): 109-120.; ZÚÑIGA et al., 2009Zúñiga A, Muñoz-Pedreros A, Fierro A. Uso de hábitat de cuatro carnívoros terrestres en el sur de Chile. Gayana 2009; 73(2): 200-210.; ROCHA-MENDES et al., 2010Rocha-Mendes F, Mikich SB, Quadros J, Pedro WA. Feeding ecology of carnivores (Mammalia, Carnivora) in Atlantic Forest remnants, southern Brazil. Biota Neotrop 2010; 10(4): 21-30. http://dx.doi.org/10.1590/S1676-06032010000400001.
http://dx.doi.org/10.1590/S1676-06032010...
; BORNHOLDT et al., 2013Bornholdt R, Helgen K, Koepfli K-P, Oliveira L, Lucherini M, Eizirik E. Taxonomic revision of the genus Galictis (Carnivora: Mustelidae): species delimitation, morphological diagnosis, and refined mapping of geographical distribution. Zool J Linn Soc 2013; 167(3): 449-472. http://dx.doi.org/10.1111/j.1096-3642.2012.00859.x.
http://dx.doi.org/10.1111/j.1096-3642.20...
; POO-MUÑOZ et al., 2014Poo-Muñoz DA, Escobar LE, Townsend P, Astorga F, Organ JF, Medina-Vogel G. Galictis cuja (Mammalia): an update of current knowledge and geographic distribution. Iheringia: Sér Zool 2014; 104(3): 341-346. http://dx.doi.org/10.1590/1678-476620141043341346.
http://dx.doi.org/10.1590/1678-476620141...
). According to the IUCN (2016)International Union for Conservation of Nature and Natural Resources – IUCN. The World Conservation Union: the IUCN Red List of Threatened Species 2016 [online]. Gland: IUCN; 2016 [cited 2016 February 2]. Available from: http://www.iucnredlist.org/
http://www.iucnredlist.org/...
, this species is not included in the main endangered categories, and its conservation status is of “least concern”.

To date, there have been few studies on the helminth parasite fauna of G. cuja in South America. The most recent compilations about helminth parasites in wild mammals in some South American countries have reported few helminth species in this host species. Lunaschi & Drago (2007)Lunaschi LI, Drago FB. Checklist of digenean parasites of wild mammals from Argentina. Zootaxa 2007; 1580: 35-50. http://dx.doi.org/10.11646/zootaxa.3936.3.1.
http://dx.doi.org/10.11646/zootaxa.3936....
and Fugassa (2015)Fugassa MH. Checklist of helminths found in Patagonian wild mammals. Zootaxa 2015; 4012(2): 271-328. PMid:26623857. http://dx.doi.org/10.11646/zootaxa.4012.2.3.
http://dx.doi.org/10.11646/zootaxa.4012....
did not mention any occurrences of helminths in this mammal in Argentina. However, Moleón et al. (2015)Moleón MS, Kinsella JM, Moreno PG, Ferreyra HV, Pereira J, Pía M, et al. New hosts and localities for helminths of carnivores in Argentina. Zootaxa 2015; 4057(1): 106-114. PMid:26701468. http://dx.doi.org/10.11646/zootaxa.4057.1.6.
http://dx.doi.org/10.11646/zootaxa.4057....
provided the first report on occurrences of helminths in G. cuja in Argentina, consisting of the nematode Aonchotheca putorii (Rudolphi, 1819) (Trichocephalida, Capillariidae). In G. cuja from Paraguay, Seesee et al. (in YENSEN & TARIFA, 2003Yensen E, Tarifa T. Galictis cuja. Mamm Species 2003; 728: 1-8. http://dx.doi.org/10.1644/728.
http://dx.doi.org/10.1644/728...
) listed occurrences of unidentified nematode species of the genera Cruzia Travassos, 1917 (Spirurida, Kathlaniidae), Dirofilaria Railliet & Henry, 1910 (Spirurida, Onchocercidae), Gnathostoma Owen, 1836 (Spirurida, Gnathostomatidae), and Lagochilascaris Leiper, 1909 (Spirurida, Ascaridae), along with unidentified nematode species in the families Oxyuridae and Trichostrongylidae.

We consider that the studies about helminth parasites of G. cuja in Brazil have been more representative. The most recent studies on helminths in mammals in Brazil have so far recorded five species of helminths in this host, in several localities in this country (VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.; PINTO et al., 2011Pinto RM, Knoff M, Gomes DC, Noronha D. Nematodes from mammals in Brazil: an updating. Neotrop Helminthol 2011; 5(2): 139-183.). Therefore, the current study aimed to investigate the helminth parasites of a population of G. cuja living in a stretch of Atlantic Forest in the southeastern region of Brazil, and elaborate a checklist of helminth parasites of this host species in South America.

Material and Methods

The specimens of Galictis cuja examined were collected between January 2009 and May 2014, roadkilled on BR-040 highway, between the municipalities of Duque de Caxias (22°35’33”S, 43°16’48”W), state of Rio de Janeiro and Juiz de Fora (21°49’02”S, 43°23’03”W), state of Minas Gerais, localities inserted in Atlantic rainforest Biome. A total of 18 hosts were necropsied, and the skeletons and taxidermized skin of hosts parasitized are deposited at Coleção de Mastozoologia do Museu Nacional do Rio de Janeiro (MNRJ), of the Universidade Federal do Rio de Janeiro (UFRJ), under the codes: MNRJ 79162, MNRJ 79190, MNRJ 79216, MNRJ 79247, MNRJ 79261, MNRJ 79294, MNRJ 79314, MNRJ 79326, MNRJ 79358, MNRJ 79379, MNRJ 79404, MNRJ 79407, MNRJ 79421, MNRJ 79443, MNRJ 79445, MNRJ 79471, and MNRJ 79501. The hosts were identified according to Yensen & Tarifa (2003)Yensen E, Tarifa T. Galictis cuja. Mamm Species 2003; 728: 1-8. http://dx.doi.org/10.1644/728.
http://dx.doi.org/10.1644/728...
and Bornholdt et al. (2013)Bornholdt R, Helgen K, Koepfli K-P, Oliveira L, Lucherini M, Eizirik E. Taxonomic revision of the genus Galictis (Carnivora: Mustelidae): species delimitation, morphological diagnosis, and refined mapping of geographical distribution. Zool J Linn Soc 2013; 167(3): 449-472. http://dx.doi.org/10.1111/j.1096-3642.2012.00859.x.
http://dx.doi.org/10.1111/j.1096-3642.20...
.

After being collected, the hosts were kept frozen in a freezer at -18 °C until necropsy. The organs were dissected in plastic trays, and washed in saline solution 0.9%. The helminth collected were fixed in AFA (70° GL ethanol, 93 parts; 37% formalin, 5 parts; glacial acetic acid, 2 parts) for 48 hrs, and then stored in 70° GL ethanol.

For microscopic identification the nematodes were clarified in Amann’s lactophenol (1: 1: 2: 1 – phenol: lactic acid: glycerin: distilled water) and mounted in temporary slides. Trematodes and acanthocephalans were stained with Mayer’s carmalum (HUMASON, 1979Humason GL. Animal tissue techniques. 4th ed. San Francisco: W. H. Freeman and Company; 1979.) and mounted in Canada balsam for examination as whole mounts. The helminth species were identified in Olympus BX 41 light microscope.

The nematodes were identified at generic level according to Anderson et al. (2009)Anderson RC, Chabaud AG, Willmott S, editors. Keys to the nematode parasites of vertebrates: archival volume. Wallingford: CABI International; 2009.. Sistematic classification of nematodes is according to Hodda (2011)Hodda M. Phylum Nematoda Cobb 1932. Zootaxa 2011; 3138: 63-95.. The specimens of the genus Molineus Cameron, 1923 (Strongylida, Molineoidea) were identified according to the bursal rays distribution (ANDERSON et al., 2009Anderson RC, Chabaud AG, Willmott S, editors. Keys to the nematode parasites of vertebrates: archival volume. Wallingford: CABI International; 2009.) and by the specific morphological descriptions made by Travassos (1921Travassos L. Contribuições para o conhecimento da fauna helmintolojica brasileira. XIII Ensaio Monográfico da família Trichostrongylidae Leiper, 1909. Mem Inst Oswaldo Cruz 1921; 13(1): 5-135. http://dx.doi.org/10.1590/S0074-02761921000100001.
http://dx.doi.org/10.1590/S0074-02761921...
, 1937Travassos L. Revisão da família Trichostrongylidae Leiper 1912. Monog Inst Oswaldo Cruz 1937; 1: 1-512.). Trematodes were identified at generic level according to Bray et al. (2008)Bray RA, Gibson DI, Jones A, editors. Keys to the Trematoda. Wallingford: CABI Publishing; 2008., and at specific level according to Rodrigues (1963)Rodrigues HO. Contribuição ao estudo do gênero Platynosomum, Looss, 1907 (Trematoda, Dicrocoeliidae). Mem Inst Oswaldo Cruz 1963; 61(3): 507-515. PMid:14141131. http://dx.doi.org/10.1590/S0074-02761963000300008.
http://dx.doi.org/10.1590/S0074-02761963...
. Acanthocephalans were identified according to Machado (1950)Machado DA. Revisão do gênero Prosthenorchis Travassos, 1915 (Acanthocephala). Mem Inst Oswaldo Cruz 1950; 48(1): 495-544. PMid:24539413. http://dx.doi.org/10.1590/S0074-02761950000100020.
http://dx.doi.org/10.1590/S0074-02761950...
and Schmidt (1972)Schmidt GD. Revision of the Class Archiacanthocephala Meyer, 1931 (Phylum Acanthocephala), with Emphasis on Oligacanthorhynchidae Southwell et Macfie, 1925. J Parasitol 1972; 58(2): 290-297. PMid:5022866. http://dx.doi.org/10.2307/3278091.
http://dx.doi.org/10.2307/3278091...
. The ecological terms and quantitative parameters of infrapopulations were according to Bush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak AW. 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...
.

Voucher specimens of helminths are deposited in the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC), Rio de Janeiro, Brazil (Table 1). The current study was performed under authorization from Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis – IBAMA/SISBIO (Request No 30727-4).

Table 1
Species of helminths collected in Galictis cuja of the current study, site of infection, and ecological data of each helminth.

Results

Among the specimens of Galictis cuja examined in the current study, the total prevalence of parasitism was 94.4% (17 infected hosts out of the sample of 18 hosts analyzed). The helminth richness was six species, of which four were nematodes: Dioctophyme renale (Goeze, 1782) (Dioctophymatida, Dioctophymatidae), Molineus elegans (TRAVASSOS, 1921Travassos L. Contribuições para o conhecimento da fauna helmintolojica brasileira. XIII Ensaio Monográfico da família Trichostrongylidae Leiper, 1909. Mem Inst Oswaldo Cruz 1921; 13(1): 5-135. http://dx.doi.org/10.1590/S0074-02761921000100001.
http://dx.doi.org/10.1590/S0074-02761921...
) (Rhabditida, Trichostrongylidae), Physaloptera sp. (Spirurida, Physalopteridae) and Strongyloides sp. (Panagrolaimida, Strongyloididae). There was one species of trematode, Platynosomum illiciens (Braun, 1901) (Trematoda, Dicrocoeliidae), and one of Acanthocephala, Pachysentis gethi (MACHADO, 1950Machado DA. Revisão do gênero Prosthenorchis Travassos, 1915 (Acanthocephala). Mem Inst Oswaldo Cruz 1950; 48(1): 495-544. PMid:24539413. http://dx.doi.org/10.1590/S0074-02761950000100020.
http://dx.doi.org/10.1590/S0074-02761950...
) (Oligacanthorhynchida, Oligacanthorhynchidae) (Tables 1 and 2).

Table 2
Checklist of helminth parasites of Galictis cuja from South America.

Until the current study, five species of helminth parasites of G. cuja in Brazil were known, and other six species of helminth in this host from Paraguay and Argentina was reported (Table 2).

Discussion

The genus Molineus (Strongylida, Molineoidea) was proposed by Cameron (1923)Cameron TWM. Studies on two new genera and some little known species of the nematode family, Trichostrongylidae Leiper. J Helminthol 1923; 1(2): 71-96. http://dx.doi.org/10.1017/S0022149X00002765.
http://dx.doi.org/10.1017/S0022149X00002...
, and its type species is Molineus felineus Cameron, 1923, which is a parasite of the small intestine of Puma (Herpailurus) yagouaroundi (Carnivora, Felidae) in South America. Currently, this genus has 28 nominal species, of which seven have been reported in Neotropical primates and 21 in carnivorous mammals throughout the world, except in Australia (DURETTE-DESSET et al., 2000Durette-Desset MC, Boomker J, Malan FS. n. sp. (Nematoda, Trichostrongylina, Molinenoidea), a parasite of feral cats, . Molineus catiFelis catus Linnaeus, 1758 in South AfricaOnderstepoort J Vet Res 2000; 67(3): 173-177. PMid:11131118., 2001Durette-Desset MC, Fribourg Blanc LA, Vuong PN. (Nematoda, Trichostrongylina, Molineoidea) a parasite of Neotropical primates: new morphological and histological data. Molineus torulosusParasite 2001; 8(1): 53-60. PMid:11304951. http://dx.doi.org/10.1051/parasite/2001081053.
http://dx.doi.org/10.1051/parasite/20010...
). In carnivorous mammals in Brazil, seven species of this genus have been reported: Molineus barbaris Cameron, 1936, which was found to be a parasite in Eira barbara (Linnaeus, 1758) (Mustelidae) in the state of Mato Grosso do Sul (VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.); M. brachiurus Costa & Freitas, 1967, which occurs in Chrysocyon brachyurus (Illiger, 1815) (Canidae) in the state of Minas Gerais (VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.); M. felineus Cameron, 1923, reported in Puma (Herpailurus) yagouaroundi (Geoffroy, 1803) (Felidae) at an unspecified locality (TRAVASSOS, 1937Travassos L. Revisão da família Trichostrongylidae Leiper 1912. Monog Inst Oswaldo Cruz 1937; 1: 1-512.; VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.); M. major Cameron, 1936, parasitizing E. barbara in the states of Mato Grosso do Sul and Rio de Janeiro (TRAVASSOS, 1937Travassos L. Revisão da família Trichostrongylidae Leiper 1912. Monog Inst Oswaldo Cruz 1937; 1: 1-512.; TRAVASSOS & FREITAS, 1943Travassos L, Freitas JFT. Relatório da sétima excursão científica do Instituto Oswaldo Cruz, realizada a zona da Estrada de Ferro Noroeste do Brasil, em maio de 1942. Mem Inst Oswaldo Cruz 1943; 38(3): 385-412. http://dx.doi.org/10.1590/S0074-02761943000300007.
http://dx.doi.org/10.1590/S0074-02761943...
; VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.) and parasitizing Pteronura brasiliensis (Gmelin, 1788) (Mustelidae) in the state of Mato Grosso do Sul (VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.); M. nasuae Lent & Freitas, 1938, parasitizing Nasua nasua (Linnaeus, 1766) (Procyonidae) in the state of Pará (LENT & FREITAS, 1938Lent H, Freitas JFT. Pesquisas helminthologicas realisadas no estado do Pará. IV. Trichostrongylideos de mammiferos. Mem Inst Oswaldo Cruz 1938; 33(3): 363-380. http://dx.doi.org/10.1590/S0074-02761938000300004.
http://dx.doi.org/10.1590/S0074-02761938...
; VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.); M. paraensis Travassos, 1937, reported in Potos flavus (Schreber, 1774) (Procyonidae) in the state of Pará; and M. elegans (TRAVASSOS, 1921Travassos L. Contribuições para o conhecimento da fauna helmintolojica brasileira. XIII Ensaio Monográfico da família Trichostrongylidae Leiper, 1909. Mem Inst Oswaldo Cruz 1921; 13(1): 5-135. http://dx.doi.org/10.1590/S0074-02761921000100001.
http://dx.doi.org/10.1590/S0074-02761921...
) parasitic from C. thous of the state of Paraíba (TRAVASSOS, 1937Travassos L. Revisão da família Trichostrongylidae Leiper 1912. Monog Inst Oswaldo Cruz 1937; 1: 1-512.; LENT & FREITAS, 1938Lent H, Freitas JFT. Pesquisas helminthologicas realisadas no estado do Pará. IV. Trichostrongylideos de mammiferos. Mem Inst Oswaldo Cruz 1938; 33(3): 363-380. http://dx.doi.org/10.1590/S0074-02761938000300004.
http://dx.doi.org/10.1590/S0074-02761938...
; VICENTE et al. 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.; LIMA et al., 2013Lima RC, Lux Hoppe EGL, Tebaldi JH, Cruz BC, Gomes AAB, Nascimento AA. Gastrintestinal helminths of (Linnaeus, 1766 - Smith, 1839) from the caatinga area of the Paraíba State, Brazil. Cerdocyon thousSemina: Ciênc Agrár 2013; 34(6): 2879-2888.). In Brazil, Molineus elegans also is reported in this type host Saimiri sciureus (Linnaeus, 1758) (Primates, Cebidae) of the state of Pará (CORRÊA et al., 2016Corrêa P, Bueno C, Soares R, Vieira FM, Muniz-Pereira LC. Checklist of helminth parasites of wild primates from Brazil. Rev Mex Biod 2016; 87(3): 908-918. http://dx.doi.org/10.1016/j.rmb.2016.03.008.
http://dx.doi.org/10.1016/j.rmb.2016.03....
). Until the current study, no reports of nematodes of the genus Molineus parasitizing G. cuja existed. Therefore, the current report of M. elegans in G. cuja in Brazil is the first report of this genus of nematodes in this host.

Currently, the genus Physaloptera Rudolphi, 1819 (Spirurida, Physalopteroidea), has approximately 104 nominal species, which occur in amphibians, reptiles, birds and mammals throughout the world (PEREIRA et al., 2012Pereira FB, Alves PV, Rocha BM, Lima SS, Luque JL. A New Physaloptera (Nematoda: Physalopteridae) parasite of (Squamata: Teiidae) from Southeastern Brazil. Tupinambis merianaeJ Parasitol 2012; 98(6): 1227-1235. PMid:22712869. http://dx.doi.org/10.1645/GE-3159.1.
http://dx.doi.org/10.1645/GE-3159.1...
). According to Vieira et al. (2008)Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23. and Pinto et al. (2011)Pinto RM, Knoff M, Gomes DC, Noronha D. Nematodes from mammals in Brazil: an updating. Neotrop Helminthol 2011; 5(2): 139-183., six species of this genus have been reported in wild carnivorous mammals in Brazil. Physaloptera anomala Molin, 1860, was found in Panthera onca (Linnaeus, 1758) (Felidae) at an unspecified locality (VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.); P. digitata Schneider, 1866, was reported parasitizing Leopardus wiedii (Schinz, 1821) (Felidae) in the state of Pará (NORONHA et al., 2002Noronha D, Vicente JJ, Pinto RM. A survey of new host records for nematodes from mammals deposited in the Helminthological collection of the Institute Oswaldo Cruz (CHIOC). Rev Bras Zool 2002; 19(3): 945-949. http://dx.doi.org/10.1590/S0101-81752002000300032.
http://dx.doi.org/10.1590/S0101-81752002...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.) and Puma concolor (Linnaeus, 1771) (Felidae) in the states of Rio de Janeiro and São Paulo (VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.); P. maxillaris Molin, 1860, was reported as a parasite of Conepatus chinga (Molina, 1782) (Mephitidae) in the states of Pernambuco and Rio Grande do Sul (VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.); P. praeputialis Linstow, 1889. was reported in Cerdocyon thous (Linnaeus, 1766) (Canidae) in the state of Paraná (VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.) and in C. brachyurus in the state of Minas Gerais (VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.); P. semilanceolata Molin, 1860, was found parasitizing N. nasua in the states of Mato Grosso do Sul and Pará (VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.); and P. terdentata Molin, 1860, was found in P. concolor in the state of Rio de Janeiro (VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.). Unidentified species of Physaloptera was reported in C. thous in the state of Mato Grosso do Sul, in E. barbara in the state of Amazonas, in L. wiedii in the state of Pará (VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.), in Leopardus pardalis (Linnaeus, 1758) (Felidae) in the states of Mato Grosso do Sul and Pará (TRAVASSOS & FREITAS, 1943Travassos L, Freitas JFT. Relatório da sétima excursão científica do Instituto Oswaldo Cruz, realizada a zona da Estrada de Ferro Noroeste do Brasil, em maio de 1942. Mem Inst Oswaldo Cruz 1943; 38(3): 385-412. http://dx.doi.org/10.1590/S0074-02761943000300007.
http://dx.doi.org/10.1590/S0074-02761943...
; VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.) and in N. nasua in the states of Mato Grosso, Mato Grosso do Sul and Rio de Janeiro (TRAVASSOS & FREITAS, 1943Travassos L, Freitas JFT. Relatório da sétima excursão científica do Instituto Oswaldo Cruz, realizada a zona da Estrada de Ferro Noroeste do Brasil, em maio de 1942. Mem Inst Oswaldo Cruz 1943; 38(3): 385-412. http://dx.doi.org/10.1590/S0074-02761943000300007.
http://dx.doi.org/10.1590/S0074-02761943...
; VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.). In the current study, we found only female specimens of this nematode, therefore, it was not possible to identify the species. The occurrence of an unidentified species of Physaloptera parasitizing C. cuja in the current study is the first record of this nematode in this host species.

The monotypic genus Dioctophyme Collet-Megret, 1802 (Enoplida, Dioctophymatoidea) is composed by D. renale (Goeze, 1782), which is a parasite of the kidneys or peritoneum of mammals, especially of the families Mustelidae and Canidae (VICENTE et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: Nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; ANDERSON et al., 2009Anderson RC, Chabaud AG, Willmott S, editors. Keys to the nematode parasites of vertebrates: archival volume. Wallingford: CABI International; 2009.). In Brazil, this species has been reported in several wild carnivorous hosts, including specimens of G. cuja that originated from the state of Rio de Janeiro (VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.).

Species of Strongyloides Grassi, 1879 (Rhabditida, Rhabiditoidea) are parasites of several groups of domestic and wild vertebrates throughout the world (ANDERSON et al., 2009Anderson RC, Chabaud AG, Willmott S, editors. Keys to the nematode parasites of vertebrates: archival volume. Wallingford: CABI International; 2009.). Nevertheless, reports of this genus in wild carnivorous mammals in Brazil are rare and the occurrences have been limited to unidentified species of Strongyloides parasitizing C. thous and Galictis vittata (Schreber, 1776), both in the state of Rio de Janeiro (VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.), and G. cuja in the state of Rio Grande do Sul (MULLER et al., 2009Müller G, Pesenti TC, Mascarenhas CS. Parasitos de animais silvestres com potencial zoonótico no Rio Grande do Sul. Vet Foco 2009; 6(2): 185-190.; PINTO et al., 2011Pinto RM, Knoff M, Gomes DC, Noronha D. Nematodes from mammals in Brazil: an updating. Neotrop Helminthol 2011; 5(2): 139-183.). Species of Strongyloides have not been previously recorded in G. cuja in Atlantic forest localities in the states of Rio de Janeiro and Minas Gerais, and therefore this is the first report of this nematode in this host species in these states.

The genus Pachysentis Meyer, 1931 (Oligacanthorhynchida, Oligacanthorhynchidae), was proposed to accommodate Pachysentis canicola Meyer, 1931, a parasite of domestic dogs in South America (PETROCHENKO, 1971Petrochenko VI. Acanthocephala of domestic and wild animals. Jerusalem: Israel Program for Scientific Translations; 1971.). Currently, this genus contains 10 nominal species that parasitize domestic and wild mammals throughout the world (PETROCHENKO, 1971Petrochenko VI. Acanthocephala of domestic and wild animals. Jerusalem: Israel Program for Scientific Translations; 1971.; AMIN, 2013Amin OM. Classification of the Acanthocephala. Folia Parasitol 2013; 60(4): 273-305. PMid:24261131. http://dx.doi.org/10.14411/fp.2013.031.
http://dx.doi.org/10.14411/fp.2013.031...
). Pachysentis gethi (MACHADO, 1950Machado DA. Revisão do gênero Prosthenorchis Travassos, 1915 (Acanthocephala). Mem Inst Oswaldo Cruz 1950; 48(1): 495-544. PMid:24539413. http://dx.doi.org/10.1590/S0074-02761950000100020.
http://dx.doi.org/10.1590/S0074-02761950...
) was originally described by Machado (1950)Machado DA. Revisão do gênero Prosthenorchis Travassos, 1915 (Acanthocephala). Mem Inst Oswaldo Cruz 1950; 48(1): 495-544. PMid:24539413. http://dx.doi.org/10.1590/S0074-02761950000100020.
http://dx.doi.org/10.1590/S0074-02761950...
and was placed in the genus Prosthenorchis Travassos, 1915 (Oligacanthorhynchida, Oligacanthorhynchidae), from descriptions of specimens collected from E. barbara in the states of Rio de Janeiro and Pará. Vieira et al. (2008)Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23. searched for information on helminth parasites in wild carnivorous mammals in Brazil that was stored in the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC) and reported the same data as in the original description made by Machado (1950)Machado DA. Revisão do gênero Prosthenorchis Travassos, 1915 (Acanthocephala). Mem Inst Oswaldo Cruz 1950; 48(1): 495-544. PMid:24539413. http://dx.doi.org/10.1590/S0074-02761950000100020.
http://dx.doi.org/10.1590/S0074-02761950...
, along with two new records of this species, parasitizing G. cuja and G. vittata, both in the state of Rio de Janeiro.

Platynosomum illiciens (Braun, 1901) (Trematoda, Dicrocoeliidae) was described as an intestinal parasite of Falco sp. (Aves, Falconiformes) (TRAVASSOS, 1944Travassos L. Revisão da família Dicrocoeliidae Odhner, 1910. Monog Inst Oswaldo Cruz 1944; 2: 1-557.). This species was reported by Travassos (1944)Travassos L. Revisão da família Dicrocoeliidae Odhner, 1910. Monog Inst Oswaldo Cruz 1944; 2: 1-557. and Yamaguti (1958)Yamaguti S. Systema Helminthum, Vol I. The digenetic Trematodes of vertebrates – Parts I and II. New York: Interscience Publishers; 1958. as an exclusive parasite of the liver of some bird species in Brazil. However, Rodrigues (1963)Rodrigues HO. Contribuição ao estudo do gênero Platynosomum, Looss, 1907 (Trematoda, Dicrocoeliidae). Mem Inst Oswaldo Cruz 1963; 61(3): 507-515. PMid:14141131. http://dx.doi.org/10.1590/S0074-02761963000300008.
http://dx.doi.org/10.1590/S0074-02761963...
observed large polymorphs in P. semifuscum Looss, 1907, which is a parasite of European birds; in P. proxilliciens (Canavan, 1937), which is a parasite of Asian birds; in P. fastosum Kossack, 1910, which is a parasite of several species of mammals in Asia and North and South America; and in P. brauni (Freitas & Lent, 1937), which is a parasite of Brazilian birds. This author therefore considered all these species to be junior synonyms of P. illiciens. Pinto et al. (2016)Pinto HA, Mati VLT, Melo AL. Can the same species of (Trematoda: Dicrocoeliidae) infect both mammalian and avian hosts? PlatynosomumJ Helminthol 2016; 90(3): 372-376. PMid:25781630. http://dx.doi.org/10.1017/S0022149X15000152.
http://dx.doi.org/10.1017/S0022149X15000...
also considered that the morphometric differences observed in these species of Platynosomum were insufficient for specific differentiation, and stated that P. illiciens is a species with wide geographic distribution and host range, parasitizing both birds and mammals. In carnivore mammals from Brazil, P. illiciens has been previously reported as a parasite of G. vittata in the state of Rio de Janeiro (TRAVASSOS, 1944Travassos L. Revisão da família Dicrocoeliidae Odhner, 1910. Monog Inst Oswaldo Cruz 1944; 2: 1-557.; TRAVASSOS et al., 1969Travassos L, Freitas JFT, Kohn A. Trematódeos do Brasil. Mem Inst Oswaldo Cruz 1969; 67(1): 1-886. PMid:5397756.; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.), of P. yagouaroundi in the state of Pernambuco (BARBOSA & PONTUAL, 1949Barbosa FAZ, Pontual C. A new host for Platynosomum fastosum Kossack, 1910 (Trematoda, Dicrocoeliidae). J Parasitol 1949; 35(5): 546-547. PMid:18138192. http://dx.doi.org/10.2307/3273665.
http://dx.doi.org/10.2307/3273665...
; RODRIGUES, 1963Rodrigues HO. Contribuição ao estudo do gênero Platynosomum, Looss, 1907 (Trematoda, Dicrocoeliidae). Mem Inst Oswaldo Cruz 1963; 61(3): 507-515. PMid:14141131. http://dx.doi.org/10.1590/S0074-02761963000300008.
http://dx.doi.org/10.1590/S0074-02761963...
; VIEIRA et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721: 1-23.). Therefore, the current study is the first report of P. illiciens parasitizing G. cuja.

The quantitative data from this study could not be compared with other previous studies from helminth from G. cuja (Table 1), since these previous studies do not show a number of compatible hosts with the present study, or do not provide quantitative data from parasitism. Some data of mean intensity and mean abundance of certain helminth infrapopulations observed herein, showed a large standard deviation (Table 1), suggesting heterogeneity in size of these infrapopulations. When the 95% confidence intervals of the mean intensity and abundance of these data were analyzed found that the quantitative data of P. gethi (Confidence intervals of mean intensity 0.959, 4.241; and of mean abundance -0.344, 1.744), P. illiciens (Confidence interval of mean abundance -0.439, 3.439), D. renale (Confidence intervals of mean intensity -0.953, 2.047; and of mean abundance -0.098, 0.698), and Strongyloides sp. were not statistically significant (Confidence interval of mean abundance -3.143, 17.743) (Table 1), which indicate that the number of studied hosts could not estimate the totality of the helminth infrapopulations, and that a higher sampling hosts should be analyzed for a more consistent study of the population ecology of G. cuja helminth at the studied area.

The most recent report of parasites in this host was in the study by Vieira et al. (2012)Vieira FM, Muniz-Pereira LC, Lima SS, Moraes AHA No, Gonçalves PR, Luque JL. Crenosoma brasiliense sp. n. (Nematoda: Metastrongyloidea) parasitic in lesser grison, Galictis cuja (Molina, 1782) (Carnivora, Mustelidae) from Brazil, with a key to species of Molin, 1861. CrenosomaFolia Parasitol 2012; 59(3): 87-94. PMid:23136799. http://dx.doi.org/10.14411/fp.2012.026.
http://dx.doi.org/10.14411/fp.2012.026...
, who proposed a new species of nematode, Crenosoma brasiliense Vieira, Muniz-Pereira, Souza Lima, Moraes Neto, Gonçalves & Luque, 2012 (Strongylida, Metastrongyloidea), which was collected in the lungs of one specimen of G. cuja in the municipality of Juiz de Fora, state of Minas Gerais.

Comparison of the data provided in the current study with the previous reports of helminth in G. cuja in Brazil (Table 2) demonstrates that the current study is the most representative report relating to this host species. Here, we studied a considerably sized sample of hosts (18 specimens) and recorded three new occurrences of helminths in G. cuja in Brazil, which is equivalent to 60% of what was previously known about this fauna.

Acknowledgements

Pilar Corrêa was supported by a student fellowship from CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil). Fabiano Matos Vieira was supported by a Postdoctoral fellowship from Programa Nacional de Pós-doutorado (PNPD) CAPES/FIOCRUZ (Fundação Instituto Oswaldo Cruz) at the Programa de Pós-graduação em Biodiversidade e Saúde (PPGBS) of the Instituto Oswaldo Cruz (IOC), Rio de Janeiro, RJ.

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Publication Dates

  • Publication in this collection
    01 Dec 2016
  • Date of issue
    Oct-Dec 2016

History

  • Received
    09 June 2016
  • Accepted
    27 July 2016
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