Parasitic nematodes of three species of wild carnivore mammals from Atlantic forest in the state of Minas Gerais, Brazil
Fabiano Matos Vieira (a), Luís Claudio Muniz-Pereira (a), Sueli de Souza-Lima (b), Bárbara Marun Rocha (b)⁎ ✉ , José Luis Luque (c)
Abstract
This study aimed to report the occurrence of species of nematodes in wild carnivore mammals from a locality of Atlantic forest in Brazil. Specimens of wild carnivore mammals of 3 species were necropsied: Chrysocyon brachyurus (Illiger, 1815), Cerdocyon thous (Linnaeus, 1766), and Puma (Herpailurus) yagouaroundi (É. Geoffroy, 1803). Seven species of nematodes were recorded: 5 in C. brachyurus [Uncinaria stenocephala (Railliet, 1884), Dioctophyma renale (Goeze, 1782), Strongyloides sp., Trichuris vulpis (Froelich, 1789), and Oslerus (Oslerus) sp.]; 2 in C. thous [Angiostrongylus raillieti (Travassos, 1927), and Strongyloides sp.], and only 1 species [ Cylicospirura subaequalis (Molin, 1860)] in P. (H.) yagouaroundi. Strongyloides sp., T. vulpis and Oslerus (Oslerus ) sp. were recorded for the first time in C. brachyurus from Brazil, and the first one of C. subaequalis in a host from Brazil in their type host since the original description date from 1860.
© 2017 Universidad Nacional Autónoma de México, Instituto de Biología. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Keywords:
Parasitic nematodes; Brazil; Wild mammals;
Nemátodos parásitos de tres especies de mamíferos carnívoros silvestres del bosque atlántico en el estado de Minas Gerais, Brasil
Resumen
El objetivo de este estudio fue registrar la presencia de especies de nemátodos en mamíferos carnívoros salvajes de una localidad del bosque atlántico en Brasil. Ejemplares de 3 especies de mamíferos carnívoros silvestres fueron necropsiados: Chrysocyon brachyurus (Illiger, 1815), Cerdocyon thous (Linnaeus, 1766) y Puma (Herpailurus) yagouaroundi (É. Geoffroy, 1803). Se registraron 7 especies de nemátodos: 5 en C. brachyurus uncinaria stenocephala (Railliet, 1884), Dioctophyma renale (Goeze, 1782), Strongyloides sp., Trichuris vulpis (Froelich, 1789) y Oslerus (Oslerus) sp.; 2 en C. thous (Angiostrongylus raillieti [Travassos, 1927] y Strongyloides sp.) y solo una especie (Cylicospirura subaequalis [Molin, 1860]) en P. (H.) yagouaroundi. Strongyloides sp., T. vulpis y Oslerus (Oslerus) sp. fueron colectados por primera vez en C. brachyurus de Brasil, mientras que C. subaequalis se registra en su hospedador tipo en Brasil desde la descripción original hecha en 1860.
Palabras clave:
Introduction
The first reports of helminths in wild carnivore mammals from Brazil were made by Rudolphi (1819), who described the cestode Taenia crassipora Rudolphi, 1819 and the nematode Toxocara alienata (Rudolphi, 1819 ), both collected in the intestine of Nasua nasua (Linnaeus, 1766). Until the early 20th Century, one of the most significant contributions to the study of helminths of wild carnivores from Brazil was that of Diesing (1850, 1851) , in which a total of 18 species of nematodes, cestodes, acanthocephalans, and trematodes, were described and reported.
The first helminth species described in wild carnivore mammals by Brazilian researchers was the nematode Uncinaria carinii Travassos, 1915, collected in the intestine of Cerdocyon thous (Linnaeus, 1766) in the municipality of São Paulo, State of São Paulo ( Travassos, 1915 ). Since then, according to the checklist of helminth parasites in wild carnivore mammals from Brazil ( Vieira, Luque, & Muniz-Pereira, 2008 ), 21 species of hosts are reported for a total of 95 helminth species. After the study of Vieira et al. (2008) some new records of helminths in this group of hosts were reported (see Filoni et al., 2009; Gallas & Silveira, 2011; Gallas, Silveira, & Périco, 2014; Gomes, Olifiers, Santos, Simões, & Maldonado, 2015; Gomes, Olifiers, Souza, et al., 2015; Lux-Hoppe, Araújo-de Lima, Tebaldi, & Nascimento, 2010; Pinto, Knoff, Gonçalves, Sanches, & Noronha, 2009; Ribeiro, Verocai, & Tavares, 2009; Suárez, Pesenti, Macedo, Mascarenhas, & Müller, 2015; Vieira, Luque, Souza-Lima, Moraes-Neto, & Muniz-Pereira, 2012; Vieira, Muniz-Pereira, et al., 2012; Vieira et al., 2013 ). This demonstrates the potential for discovery of new data on the helminth parasites in wild carnivore mammals in Brazil.
The current study aimed to report the species of nematodes found in wild carnivore mammals from the municipality of Juiz de Fora, Minas Gerais state, Brazil.
Materials and methods
Twelve specimens of 3 species of wild carnivore mammals ( Table 1 ) were necropsied, between June 2002 and January 2010: Chrysocyon brachyurus (Illiger, 1815) (Carnivora, Canidae) (Maned Wolf) (5 specimens), Cerdocyon thous (Linnaeus, 1766) (Carnivora, Canidae) (Crab-eating Fox) (6 specimens), and Puma (Herpailurus) yagouaroundi (É. Geoffroy, 1803) (Carnivora, Felidae) (Jaguarundi) (1 specimen). The hosts examined were accidentally ‘road killed’ and were donated by the Regional Office of the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA), in the municipality of Juiz de Fora, in the state of Minas Gerais (21°41′20″ S, 43°20′40″ W). The hosts were identified according to Berta (1982), Dietz (1985), and Oliveira (1998).
Table 1
Quantitative data of nematode species reported in 3 species of wild carnivore mammals in the state of Minas Gerais, Brazil (% = prevalence, M = mean intensity, SD = standard deviation).
| Chrysocyon brachyurus
(n = 5) |
Cerdocyon thous
(n = 6) |
Puma (H.) yagouaroundi
(n = 1) |
||||
| % | M ± SD | % | M ± SD | % | M ± SD | |
| Ancylostomatoidea | ||||||
| Uncinaria stenocephala
(CHIOC 35935) |
60 | 33 ± 16 | – | – | – | – |
| Dioctophymatoidea | ||||||
| Dioctophyma renale
(CHIOC 35932) |
60 | 1.66 ± 1.15 | – | – | – | – |
| Metastrongyloidea | ||||||
| Angiostrongylus raillieti a
(CHIOC 35930) |
– | – | 20 | 19 | – | – |
| Oslerus (Oslerus) sp.
(CHIOC 35929c) |
40 | 205.5 ± 82.7 | – | – | – | – |
| Rhabditoidea | ||||||
| Strongyloides sp.
(CHIOC 35933) |
100 | 232.8 ± 120.2 | 100 | 227 ± 131.2 | – | – |
| Spiruroidea | ||||||
| Cylicospirura subaequalis a
(CHIOC 35931) |
– | – | – | – | 100 | 27 |
| Trichinelloidea | ||||||
| Trichuris vulpis a
(CHIOC 35934) |
20 | 27 | – | – | – | – |
a
The nematodes were collected in only 1 host.
The nematodes collected were fixed in AFA for 48 h, and preserved in 70% ethanol with 5% glycerin. For light microscopy studies, the nematodes were cleared in Amann’s lactophenol, and mounted on temporary slides.
Identification and classification of nematodes to the generic level follow Anderson, Chabaud, and Willmott (2009) and Gibbons (2010) . The specific identification follows Grisi (1971), Junker et al. (2013), Travassos (1927), Vicente, Rodrigues, Gomes, and Pinto (1997) , and Waid and Pence (1988).
Voucher specimens are deposited in the Instituto Oswaldo Cruz Helminthological Collection (CHIOC), Rio de Janeiro, Brazil ( Table 1).
Results
In the 3 wild carnivore mammal species studied herein, 7 nematodes species were recorded ( Table 1). Oslerus (Oslerus ) sp. (Filaroididae) was collected under the mucosa of the inner surface of the trachea and bronchii of C. brachyurus. Uncinaria stenocephala (Railliet, 1884) (Ancylostomatidae) was found in the small intestine of C. brachyurus. Specimens of Dioctophyma renale (Goeze, 1782) (Dioctophymatidae) were collected in the right kidney of C. brachyurus. Angiostrongylus raillieti (Travassos, 1927 ) (Angiostrongylidae) (= Angiostrongylus vasorum [Raillet, 1866] sensu Costa, Costa, & Guimarães, 2003 ) were registered in the pulmonary artery of C. thous. Unidentified Strongyloides sp. (Strongyloididae) specimens were collected in the small intestine of C. brachyurus and in C. thous. Trichuris vulpis (Froelich, 1789) (Trichuridae) were found in the intestinal caecum of C. brachyurus. Specimens of Cylicospirura subaequalis (Molin, 1860 ) (Spirocercidae) were collected from the cysts in the inner wall of the stomach of P. (H.) yagouaroundi.
Discussion
The genus Oslerus was proposed to accommodate Filaria osler described by Cobbold (1879), in domestic dogs in Europe. Anderson (1978) divided the genus in 2 subgenera based on the presence [ Oslerus (Anafilaroides ) (Gerichter, 1949)] or absence [ Oslerus (Oslerus ) (Hall, 1921)] of vaginal sphincters. Our specimens lack vaginal sphincter, thus were included in the subgenus Oslerus (Oslerus). Olerus (Oslerus) osleri (Cobbold, 1879 ) is reported in wild and domestic canids in Europe, North America, Africa, Asia and Oceania ( Dunsmore & Spratt, 1979; Hare, 1930; Kotani et al., 1995; Ortlepp, 1945 ). However, reports of this nematode in South America are scarce, restricted to domestic dogs from Chile ( Alcaíno & Gorman, 1999; Muñoz, Fredes, Faúndes, Sanz, & Gonzáles, 2007 ), and C. brachyurus from Brazil (Dias et al., 2012 ). However, this last report is doubtful because it was only based on clinical and coprological diagnosis of larval parasites. Due to significant morphological and morphometric differences between the males of the current study in comparison with previous morphological descriptions of Oslerus (Oslerus) osleri, we prefer to not identify them as O. (Oslerus) osleri . A more detailed study of the morphological features integrated with genetic studies of the specimens collected is necessary to verify that these specimens are a new species of Oslerus . Therefore, the current study is the first confirmed report Oslerus (Oslerus) parasitizing C. brachyurus from Brazil.
Reports of D. renale in wild hosts from Brazil document this nematode parasitizing, C. brachyurus and Lontra longicaudis (Olfers, 1818) (Carnivora, Mustelidae) ( Diesing, 1851); D. renale has been widely reported in Brazil parasitizing domestic dogs and C. brachyurus ( Vicente et al., 1997; Vieira et al ., 2008 ); and less frequently in other carnivores as Galictis cuja (Molina, 1782), G. vittata (Schreber, 1776), N. nasua, Speothos venaticus (Lund, 1842), and Cerdocyon thous (Linnaeus, 1766) ( Pesenti et al., 2012; Ribeiro et al., 2009; Vieira et al., 2008 ).
In Brazil, 12 species of the genus Trichuris Roederer & Wagler, 1761 parasitizing several groups of mammals are reported ( Vicente et al., 1997 ). However, only 2 species occur in carnivores: T. serratus (Linstow, 1879) in domestic canids and felids ( Vicente et al., 1997), and T. vulpis in domestic dogs and cats, as well as in wild specimens of C. thous ( Mundim, Oliveira-Júnior, Rodrigues, & Cury, 2004; Vicente et al., 1997; Vieira et al., 2008 ). The current study reports for the first time the parasistim by T. vulpis in C. brachyurus in this country.
Four species of Uncinaria Froelich, 1789 parasitizing wild carnivores ( Vieira et al., 2008) have been recorded in Brazil: Uncinaria bidens Lent & Freitas, 1938 in N. nasua, and Procyon cancrivorus (Cuvier, 1798) ( Vicente et al., 1997; Vieira et al., 2008 ); Uncinaria maxillaris (Molin, 1861) in Procyon cancrivorus ( Vicente et al., 1997; Vieira et al., 2008 ); Uncinaria carinii Travassos, 1915 has been recorded only once in C. thous by Travassos (1915), and U. stenocephala , species was reported initially in Europe and USA as intestinal parasite of the canids of the genus Vulpes Frisch, 1775 ( Erickson, 1944; Saeed, Maddox-Hyttel, Monrad, & Kapel, 2006 ). In Brazil, this species was first recorded by Mundim et al. (1991) parasitizing C. brachyurus in the state of Minas Gerais, as in the present study.
Angiostrongylus raillieti was described by Travassos (1927) as Haemostrongylus railiieti, from C. thous in the municipality of São Paulo, in the state of São Paulo. According to Grisi (1971), A. raillieti should be considered a valid species and not a synonym of A. vasorum from Brazil. In the study by Costa et al. (2003) , using specimens collected in domestic dogs from Brazil, the authors considered A. raillieti a synonym of A. vasorum . However, the molecular study conducted by Jefferies, Shaw, Viney, and Morgan (2009) supports the idea that A. vasorum does not occur in Brazil, based on the comparison of molecular characters of specimens of A. vasorum from Europe and South America, which corroborates with that affirmed by Grisi (1971).
Strongyloides Grassi, 1879 has a wide geographical distribution, mainly as parasite of mammals, but some species infect birds, reptiles and amphibians ( Little, 1996a,b). Ten species of Strongyloides parasitizing several species of mammals in Brazil ( Vicente et al., 1997 ). The only species of this genus recorded in Brazilian domestic dogs is S. stercoralis (Bavay, 1876) (Vicente et al., 1997 ), but so far it has not been recorded in wild carnivores of this country. Vieira et al. (2008) reported an undetermined species of Strongyloides parasitizing C. thous and G. cuja from Brazil. Therefore, the current study is the first report of Strongyloides sp. in C. brachyurus in Brazil.
Cylicospirura subaequalis was described by Molin (1860) as Spiroptera subaequalis Molin, 1860 in Puma concolor (Linnaeus, 1771) and P. (H.) yaguaroundi from Brazil (Molin, 1860 ). This species is recorded in domestic and wild felids throughout the world ( Bowman, Hendrix, Lindsay, & Barr, 2002 ); however, after the description by Molin (1860) this species has never been registered again in Brazilian hosts until now, that we found this parasitizing P. (H.) yaguaroundi . These nematodes are inserted into cysts in the stomach wall of their hosts, which can cause severe pathologies ( Bowman et al., 2002).
The most recent inventory of helminth parasites in wild carnivores in Brazil is the study of Vieira et al. (2008) , which lists 95 helminth species in 21 species of this hosts group. After the publication of Vieira et al. (2008) and until the current study, no new information had been published about the helminth parasites of Brazilian wild carnivores ( Table 2).
Table 2
Updated list of helminth parasites of wild carnivore mammals from Brazil, after study of Vieira et al. (2008).
| Helminth species | Hosts | Localities (States) | References |
| Acanthocephala | |||
| Archiacanthocephala | |||
| Oligacanthorhynchidae | |||
| Prosthenorchis cerdocyonis Gomes, Olifiers, Souza, Barbosa, D’Andrea & Maldonado Jr, 2015 | Cerdocyon thous (Canidae) | Mato Grosso do Sul | Gomes, Olifiers, Souza, et al. (2015) |
| Nematoda | |||
| Acuaroidea | |||
| Chandleronema longigutturata (Chandler 1942) | Procyon cancrivorus (Procyonidae) | Rio Grande do Sul | Suárez et al. (2015) |
| Ascaridoidea | |||
| Ascaridia galli (Schrank, 1788) | Cerdocyon thous (Canidae) | Mato Grosso do Sul | Gomes, Olifiers, Santos, et al. (2015) |
| Dioctophymatoidea | |||
| Dioctophyma renale | Cerdocyon thous (Canidae) | Rio de Janeiro | Ribeiro et al. (2009) |
| Filaroidea | |||
| Dirofilaria immitis (Leidy, 1856) | Leopardus tigrinus (Felidae) | São Paulo | Filoni et al. (2009) |
| Metastrongyloidea | |||
| Crenosoma brasiliense Vieira, Muniz-Pereira, Souza Lima, Moraes Neto, Gonçalves & Luque, 2012 | Galictis cuja (Mustelidae) | Minas Gerais | Vieira, Luque, et al. (2012) |
| Angiostrongylus felineus Vieira, Muniz-Pereira, Souza Lima, Moraes Neto, Guimarães & Luque, 2013 | Puma (H.) yagouaroundi (Felidae) | Minas Gerais | Vieira et al. (2013) |
| Physalopteroidea | |||
| Physaloptera sp. | Galictis cuja (Mustelidae) | Rio de Janeiro | Corrêa, Bueno, Vieira, and Muniz-Pereira (2016) |
| Pterygodermatites (Multipectines) pluripectinata Lux Hoppe, Araújo de Lima, Tebaldi & Nascimento, 2010 (Spirurida, Rictulariidae) | Cerdocyon thous (Canidae) | Paraíba | Lux-Hoppe et al. (2010) |
| Spiruroidea | |||
| Cylicospirura felineus (Chandler, 1925) | Leopardus geoffroyi (Felidae) | Rio Grande do Sul | Gallas et al. (2014) |
| Trichostrongyloidea | |||
| Molineus elegans (Travassos, 1921) | Galictis cuja (Mustelidae) | Rio de Janeiro
Minas Gerais |
Corrêa et al. (2016) |
| Platyhelminthes | |||
| Eucestoda | |||
| Cyclophyllidea | |||
| Taenia mustelae Gmelin, 1790 | Bassaricyon gabbii (Procyonidae) | Amazonas | Pinto et al. (2009) |
| Mesocestoides sp. | Leopardus colocolo (Felidae)
L. (Oncifelis) geoffroyi L. tigrinus Puma (H.) yagouaroundi (Felidae) |
Rio Grande do Sul | Gallas and Silveira (2011) |
| Dipylidium caninum (Linnaeus, 1758) | Cerdocyon thous (Canidae) | Minas Gerais | Vieira, Muniz-Pereira, et al. (2012) |
| Trematoda | |||
| Digenea | |||
| Platynosomum illiciens (Braun, 1901) | Galictis cuja (Mustelidae) | Rio de Janeiro
Minas Gerais |
Corrêa et al. (2016) |
Data from the current study combined with data published after the study of Vieira et al. (2008) include 15 helminth species more not reported previously in these host species ( Table 2), including 2 new hosts (B. gabbii, and L. colocolo ) for helminth in the list of wild carnivore mammals from Brazil. Therefore, we can affirm that currently 109 helminth taxa in 23 species are reported for wild carnivores in Brazil.
Acknowledgments
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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