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Revista Brasileira de Parasitologia Veterinária

Print version ISSN 0103-846XOn-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.27 no.4 Jaboticabal Oct./Dec. 2018  Epub Nov 08, 2018

http://dx.doi.org/10.1590/s1984-296120180078 

Original article

Nematode capilaridae in the tongue of Cerdocyon thous of free life in Brazil

Nematoide capilaridae na língua de Cerdocyon thous de vida livre no Brasil

Raul Henrique da Silva Pinheiro1 

Isabella Bittencourt Pires Chaves2 

Rogério Antonio Ribeiro Rodrigues1 

Érika Branco2 

Ana Rita de Lima2 

Elane Guerreiro Giese1  * 

1 Laboratório de Histologia e Embriologia Animal, Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia – UFRA, Belém, PA, Brasil

2 Laboratório de Pesquisa Morfológica Animal, Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia – UFRA, Belém, PA, Brasil

Abstract

Studies of helminths in road-killed wild animals are still uncommon but may provide promising results since they can identify the parasites in juvenile and adult hosts and meet the recommendations of current discussions on bioethics that prioritize alternative methods for the use of animals. This study evaluated three Cerdocyon thous individuals that were donated after dying from being run over. Two of them had small nematode adults in the epithelial and connective tissues of the tongue. The diagnosis was based on the presence of eggs, observed in histological sections, and morphological characteristics of the nematodes in the tongue. Morphologically, this nematode has a body with transverse grooves, simple mouth opening and no lips, esophagus and stichosome with stichocytes and bacillary bands along the body, which is characteristic morphology of the family Capilariidae and genus Capillaria . The presence of this nematode in the tongue of C. thous is an extremely important fact that contributes to what is known about the biodiversity of zoonotic parasites in wild canid populations. However, an explanation for these findings remains unclear because, until now, this has not been observed in the biological cycle of the species.

Keywords:  Nematoda; Capillaria; mammal; Amazon

Resumo

O estudo de helmintos de animais selvagens vitimados por atropelamento, ainda é uma prática pouco comum, porém pode ser promissor, uma vez que permite a identificação de helmintos a partir de hospedeiros juvenis e adultos, e atendem às atuais discussões em bioética, as quais priorizam métodos alternativos para o uso de animais. Foram avaliados 3 exemplares de Cerdocyon thous provenientes de doação pós-óbito por atropelamento. Dois deles apresentaram pequenos nematoides adultos inseridos nos tecidos epitelial e conjuntivo da língua. O diagnóstico foi baseado na análise de cortes histológicos que evidenciaram a presença de ovos no interior do nematoide e nas características morfológicas gerais do mesmo. Morfologicamente estes nematoides apresentavam corpo com estrias transversais, abertura bucal simples e lábios ausentes, esôfago trichuroiude com a presença de esticócitos e bandas bacilares ao longo do corpo, característica morfologicamente sugestiva da família Capillariidae e do gênero Capillaria . A presença de nematoides inseridos na língua de C. thous é um fato de extrema importância para o conhecimento da biodiversidade de parasitos zoonóticos circulantes presentes em populações selvagens de canídeos. Porém, permanece obscura a explicação para tais achados, uma vez que tal evento não foi observado no ciclo biológico das espécies até o momento.

Palavras-chave:  Nematoda; Capillaria; mamífero; Amazônia

Introduction

Studies involving the helminthofauna of wild animals are of great importance for the conservation of species and for public health, since some of these parasites can injure wild populations and have zoonotic potential ( LAFFERTY, 1997 ).

Some helminths that parasitize wild mammals belong to the family Capillaridae. The taxonomy of this family is still being revised and the group contains many species in the genus Capillaria ( GUARDONE et al., 2013; FUEHRER, 2014 ), of which Capillaria hepatica Bancroft, 1893 is the most commonly cited in the literature as a parasite of various domestic and wild animals ( FREITAS & LENT, 1936 ; ARAÚJO, 1967 ; SILVEIRA et al., 1975 ; GALVÃO, 1981 ; CHIEFFI et al., 1981 ; MANDORINO & REBOUÇAS, 1991 ; VICENTE et al., 1997 ; RUAS et al., 2003 ). Capillaria comprises a complex group of parasites, which has resulted in the proposal of the genera Calodium, Eucoleus, Paracapillaria, Pearsonema and Aonchotheca ( GUARDONE et al., 2013 ; FUEHRER, 2014 ). Within this complex, three species are of zoonotic importance: Paracapillaria philippinensis (Syn. Capillaria philippinensis), Eucoleus aerophila (Syn. Capillaria aerophila) and Calodium hepaticum (Syn. Capillaria hepatica, Trichocephalus hepaticus Bancroft, 1893 and Hepaticola hepatica Hall 1916.

Due to anthropic impacts, wild animals frequently come out of natural habitats in search of food and suffer injuries. Roads, starting at the construction phase, impact native fauna in several ways, producing direct and indirect effects on populations, such as mortality from being run over, loss of habitat, dispersion of exotic species and intensification of the presence of humans ( ASCENSÃO & MIRA, 2006 ). The study of helminths in road-killed animals is still uncommon; however, studies that use this methodology are promising since they can identify these parasites in adults and young individuals and meet the recommendations of current discussions on bioethics that prioritize alternative methods for the use of animals ( RICHINI-PEREIRA et al., 2006 ). In Brazil, among the wild carnivores, Cerdocyon thous is one of the most commonly road-killed species ( MALHEIROS, 2004 ; PRADA, 2004 ; PINOWSKI, 2005 ).

Based on the few studies about the presence of capillariids in wild animals, this study describes the first record in Brazil of a Capillariidae nematode parasitizing the tongue of C. thous, in the municipality of Paragominas in Pará State, in addition to collecting and analyzing retrospective data on the fauna of helminths of C. thous in Brazil.

Materials and Methods

We evaluated the tongues of three animals (C. thous) that were donated, after being run over by the company HYDRO Paragominas - bauxite mine, to the Laboratório de Pesquisa Morfológica Animal (LaPMA) - Instituto da Saúde e Produção Animal at the Universidade Federal Rural da Amazônia (UFRA), campus Belém (under authorization of SEMA-PA Nº 455/2009 and 522/2009), animals used for morphological studies.

To extract the tongues, used in morphological studies by LaPMA, an incision in the skin and muscles of the mentonian region was made. The tongue was folded ventrally after cutting the lingual frenulum and then cut caudally at the root to harvest the material. The material was fixed in a 10% formaldehyde solution for the histological analysis and in an AFA solution (93 parts 70% ethyl alcohol, 5 parts formaldehyde, and 2 parts glacial acetic acid) for the morphological analysis. Samples of the nematodes were separated from the lingual tissue, dehydrated in an ethanol series, clarified with lactophenol, placed on a microscope slide under a coverslip as a temporary mount, observed using a light microscope, and photographed with a LEICA DM2500 microscope with an image capturing system. This work was conducted in the Laboratório de Histologia e Embriologia Animal - Instituto da Saúde e Produção Animal. For scanning electron microscopy, fragments of the tongue with nematodes were fixed in 10% formaldehyde, post-fixed in 1% osmium tetroxide, critical point dried with CO2, coated with gold-palladium and analyzed with a VEGA 3 LMU/TESCAN scanning electron microscope. This was done in the Laboratório de Microscopia Eletrônica de Varredura - Instituto da Saúde e Produção Animal at the Universidade Federal Rural da Amazônia (UFRA), campus Belém. To avoid confusion, only names of genera of helminths are abbreviated and not those of hosts.

Results

Of the three animals evaluated, two had six small adult nematodes in the epithelial and conjunctive tissues of the tongue ( Figure 1 A and 2 AC). The six nematodes formed galleries within the epithelium ( Figure 1 D- E and 2 B) and their dispersal had a multifocal character. The diagnosis was based on the presence of eggs ( FERRER & CASTELLÀ, 1996 ), observed in histological sections, and morphological characteristics of the nematodes in the tongues, which were analyzed using scanning electron microscopy (body surface) and light microscopy

Figure 1 (A) Mesoscopic view of Capillaria sp. (*) inserted among the lingual filiform papillae (fi) of Cerdocyon thous in Pará State. (B) Lateral view of the Capillaria sp. female showing numerous intrauterine eggs. (C) Detail of eggs morphology with barrel shaped and two polar opercula with plugs on the ends. (D-E) Tongue photomicrographs of C. thous parasitized by Capillaria sp., in Pará State, stained with hematoxilin and eosin. (D) Lingual papillae (pl), sustained to loose connective tissue (tcf) and covered by keratinized stratified flat epithelial tissue (tep), where the Capillaria sp. (arrowhead) are inserted in interstitial space (*). (E) Cut of Capillaria sp. in keratinized stratified flat epithelial tissue (tep), sustained to loose connective tissue (tcf). Detail of cut of the nematode evidencing the cuticle (ct), uterine wall (uw), intrauterine eggs (ie), oesophagus (oe) and eggs (e) in the intertitial space (*). Scale bars: A= 1.5 cm, B=50 µm, C=20 µm, D= 200 µm, E=100 µm.  

Figure 2 Scanning electron microscopy of Capillaria sp. parasitizing the tongue of C. thous in Pará State. (A) Overview of the parasite inserted between the lingual papillae. (B) Detail of Capillaria sp. inserted in the interstitial space formed by keratinized, stratified, flat epithelial tissue. (C) Detail of the posterior region of the nematode strongly inserted in the keratinized, stratified, flat epithelial tissue of the tongue. (D) Detail of the bacillary bands present along the body of the nematode. Scale bars: A= 100 µm, B= 10 µm, C= 50 µm, D= 5 µm.  

During the histological analysis of the C. thous tongues, adult female nematodes were observed in transverse sections. These were inserted in the basal layers of stratified epithelial tissue, with eggs both inside the parasite as well as egg isolates and clusters within galleries developed by the nematodes ( Figure 1 DE). The eggs were barrel shaped with two polar opercula with plugs on the ends, which are diagnostic characteristics of the genus Capillaria ( Figure 1 BC). The size and the number of nematodes inserted in the tegument of the coating of the tongue did not cause inflammatory reactions and did not affect the morphology of the lingual papillae ( Figure 1 D).

A light microscopy analysis of a fragment of a nematode, clarified with Amman’s lactophenol, was conducted on the anterior region of the helminth because the rest of the body was strongly inserted in the tissue and it was not possible to completely remove the parasite ( Figure 3 AB). Morphologically, the nematodes have a body with transverse grooves, a simple mouth opening and no lips, stichosome esophagus formed by stichocytes and bacillary bands ( Figure 2 D) on the surface of the cuticle along the body, which are also morphological characteristics of Capillaria ( Figure 3 AB).

Figure 3 Photomicrographs of Capillaria sp. parasitizing the tongue of C. thous in Pará State. (A) Overview off anterior region in lateral position, simple oral opening with no lips and initial portion of stichosome esophagus (esf); (B) Lateral view of the middle region of Capillaria sp. showing the presence of stichocytes (st). Scale bars: A= 50 µm, B= 50 µm.  

Discussion

In studies of the nematofauna of C. thous, published between 1915 and 2017, adult and juvenile nematodes in 13 superfamilies (Ancylostomatoidea, Ascaridoidea, Dioctophymatoidea, Filarioidea, Metastrongyloidea, Oxyuroidea, Physalopteroidea, Rictularoidea, Rhabditoidea, Strongyloidea, Spiruroidea, Thichinelloidea, Trichostrongloidea) were recorded in 13 localities in Brazil ( Table 1 ). Of these, 15 families, 18 genera and 24 species of nematodes were identified. Some taxa were not identified to the specific level because the authors only conducted coprological exams. In the cases described as morphotypes, the authors provided morphological characteristics of the eggs (when possible) and/or measurements of the parasite; due to the lack of data, these were classified only as phylum Nematoda ( Table 2 ).

Table 1 Nematodes parasites of Cerdocyon thous distribuition in Brazilian territory according to register made for diferentes researchers between 1915 and 2017.  

Family Parasite species Site in host Location References
Superfamily Ancylostomatoidea Chabaud, 1965
Family Ancylostomatidae (Looss, 1905)
Uncinaria carinii Travassos, 1915 Instestine SP a Travassos (1915) , Vicente et al. (1997) e , Vieira et al. (2008)e,
Pinto et al. (2011)e , Moraes (2016) c
Ancylostoma buckleyi Le Roux & Biocca, 1957 d Small intestine, intestine, lung, heart and stomach PE, SP,
MG, MS, PB
Santos et al. (2003) ,
Santos et al. (2004) , Griese (2007)c, Duarte (2007)c,
Vieira et al. (2008)e, Lima (2009)c, Pinto et al. (2011)e,
Lima et al. (2013) , Gomes et al. (2015) , Moraes (2016)c
Ancylostoma caninum (Ercolani, 1859) d Small intestine and stomach SP, RJ, MS, PA, ES, RS Noronha et al. (2004) , Ruas (2005)c,
Ruas et al. (2008) , Vieira et al. (2008)e, Moraes (2016)c
Ancylostoma braziliense Faria, 1910 d Small intestine SP Griese (2007)c, Moraes (2016)c
Ancylostoma sp.d - PB Curi et al. (2010) b , Santos et al. (2015)b
Morphotype 1 - PR, MG, PI Brandão (2007)b,c, Brandão et al. (2009)b
Morphotype 2
Indeterminate Heart, lung, pulmonary artery MS, RJ, PE, PB,
RN, CE, PI, MG
Travassos & Freitas (1943) , Santos (2008b)b,c,
Santos et al. (2012)b, Santos (2013)b,c
Superfamily Ascaridoidea Railliet & Henry, 1915
Family Ascarididae Baird, 1853
Ascaridia galli (Schrank, 1788) Small intestine PR, MS, PB Gomes et al. (2015) , Santos et al. (2015)
Toxocara canis (Werner, 1782) d Intestine, small intestine RJ, PE, PB,
RN, CE, PI
Noronha et al. (2002) , Vieira et al. (2008)e, Lima (2009)c,
Pinto et al. (2011)e, Lima et al. (2013) ,
Santos (2013)b,c, Santos et al. (2015)b
Toxocara sp. d - PR, MG Curi (2005)a,b, Curi et al. (2010)b,
Santos et al. (2012)b, Santos (2013)b,c
Morphotype 1 - PE, PB,
RN, CE, PI
Brandão (2007)b, Santos (2008a),
Brandão et al. (2009)b, Santos (2013)a,b
Morphotype 2
Morphotype 3
Morphotype 4
Indeterminate
Superfamily Dioctophymatoidea Railliet, 1916
Family Dioctophymatidae (Railliet, 1915)
Dioctophma renale (Goeze, 1782) Kidney RJ Ribeiro et al. (2009) , Pinto et al. (2011)e
Superfamily Filarioidea (Weinland, 1858)
Indeterminate Heart, lung, pulmonary artery MS, RJ Travassos & Freitas (1943)
Family Onchocercidae (Leiper, 1911)
Dirofilaria sp. d Kidney MS Noronha et al. (2002) , Vieira et al. (2008)e, Pinto et al. (2011)e
Dirofilaria repens Railliet & Henry, 1911 d Under the skin MS Vieira et al. (2008)e, Pinto et al. (2011)e
Superfamily Metastrongyloidea Lane, 1917
Family Angiostrongylidae (Boerhm & Gebauer, 1934)
Indeterminate Small intestine PR Moraes (2016) c
Angiostrongylus railliet (Travassos, 1927) Grisi, 1971 Lung, right ventricle, pulmonary arteries, heart RJ, GO Travassos et al. (1927) , Grisi (1971)
Vicente et al. (1997)e, Vieira et al. (2008)e, Vieira (2011)c
Angiostrongylus vasorum (Railliet, 1866) Lung, heart, small intestine, and stomach MG, SP, DF Duarte (2007)c, Duarte et al. (2007) ,
Griese (2007)c, Pinto et al. (2011)e, Moraes (2016)c, Ferreira et al. (2017)
Angiostrongylus sp. Heart, lung, pulmonary artery MS, RJ Travassos & Freitas (1943) , Vicente et al. (1997)e,
Vieira et al. (2008)e, Vieira (2011)c
Family Protostrongylidae Leiper, 1926
Aelurostrongylus sp. Heart MS Vieira et al. (2008)e, Pinto et al. (2011)e
Superfamily Oxyuroidea Cobbold, 1864
Family Oxyuridae Cobbold, 1864
Enterobius vermicularis Linnaeus, 1758 d - PE, PB,
RN, CE, PI
Santos (2013) b,c
Morphotype 1
Morphotype 2
Morphotype 3
Morphotype 4
Morphotype 5
Superfamily Physalopteroidea Sobolev, 1949
Family Physalopteridae (Railliet, 1893)
Physaloptera praeputialis Linstow, 1889 Stomach PR, PB Vieira et al. (2008)e, Lima (2009)c,
Pinto et al. (2011)e, Lima et al. (2013) , Moraes (2016)c
Physaloptera terdentata Molin, 1860
Physaloptera digitata Scheneider, 1866
Physaloptera sp. Stomach MG, MS, PI Santos (2008b)b,c, Vieira et al. (2008)e, Brandão (2007)b,
Brandão et al. (2009)b, Pinto et al. (2011)e, Santos et al. (2012)b
Indeterminate Heart, lung, pulmonary artery, stomach, MS, RJ, RS, PE, PB, RN, CE, PI Travassos & Freitas (1943) , Ruas (2005)c,
Ruas et al. (2008) , Santos (2013)b,c
Superfamily Trichinelloidea Railliet, 1916
Family Trichuridae (Ransom, 1911)
Trichuris vulpis (Froelich, 1789) Cecum, large intestine MS, PB Vieira et al. (2008)e, Lima (2009)c,
Pinto et al. (2011)e, Curi et al. (2010) , Lima et al. (2013)
Trichuris sp. d Large intestine PI, RS, PR Chame (1988)b,c, Ruas (2005)c, Ruas et al. (2008) ,
Pinto et al. (2011)e, Santos et al. (2012)b,
Snak et al. (2017)b
Morphotype 1 - PE, PB,
RN, CE, PI
Santos (2013) b,c
Morphotype 2
Morphotype 3
Morphotype 4
Indeterminate Heart, lung, pulmonary artery MS, RJ, PI, MG Travassos & Freitas (1943) , Santos (2008a)
Family Capillariidae
Capillaria hepatica (Bancroft 1893) d Liver RS Ruas et al. (2003) , Ruas (2005)c,
Ruas et al. (2008) , Vieira et al. (2008)e, Pinto et al. (2011)e
Capillaria sp. d Urinary bladder RS, PR, MG Ruas (2005)c, Ruas et al. (2008) ,
Curi et al. (2010) , Snak et al. (2017)b
Pearsonema linsi (Freitas & Lent, 1935) Urinary bladder RJ Vieira et al. (2008)e,Pinto et al. (2011) e
Pearsonema feliscati (Diesing, 1851)
Superfamily Rhabditoidea Travasso, 1920
Family Strongyloididae Chitwood & McIntosh, 1934
Strongyloides stercoralis (Bavay, 1876) d Small intestine PB Lima (2009)c, Lima et al. (2013)
Strongyloides sp. Small intestine,
large intestine
MG, RS, RJ Ruas (2005)c, Ruas et al. (2008) ,
Vieira et al. (2008)e, Pinto et al. (2011)e,
Vieira (2011)c, Santos et al. (2012)b
Indeterminate PE, PB, RN,
CE, PI
Santos (2013) b,c
Superfamily Rictularoidea Railliet, 1916
Family Rictulariidae Railliet, 1916
Rictularia sp. Small Intestine MG, SP Griese (2007)c, Curi et al. (2010)
Pterygodermatites (Multipectines) affinis (Jagerskiöld, 1904) Quentin, 1969 Small Intestine PB Duarte (2007)c, Lima (2009)c, Lima et al. (2013)
Pterygodermatites (Multipectines) pluripectinata
Hoppe, Lima, Tebaldi & Nascimento, 2010
Small intestine PB, MS Lima (2009)c, Hoppe et al. (2010) , Pinto et al. (2011)e,
Lima et al. (2013) , Gomes et al. (2015)
Indeterminate - PE, PB,
RN, CE, PI
Santos (2013) b,c
Superfamily Strongyloidea Weinland, 1858
Family Strongylidae Baird, 1853
Indeterminate - PR Snak et al. (2017) b
Superfamily Spiruroidea Oerley, 1885
Family Spirocercidae Chitwood & Wehr, 1932
Spirocerca lupi (Rudolphi, 1809) - MG, PE, PB, RN, CE, PI Santos et al. (2012)b, Santos (2013)b,c
Spirocerca sp. MG Curi et al. (2010)
Superfamily Trichostrongyloidea Cram, 1927
Indeterminate - PI Santos (2008a)
Morphotype 1 PE, PB,
RN, CE, PI
Santos (2013) b,c
Morphotype 2
Family Molineidae Skrjabin & Schulz, 1937
Molineus felineus Cameron. 1923 - RS Ruas (2005)c, Ruas et al. (2008) , Pinto et al. (2011)f
Molineus elegans (Travassos, 1921) Small Intestine PB Lima (2009) c
Lima et al. (2013)
Molineus sp. Small Intestine
Indeterminate Small Intestine, Stomach
Phylum Nematoda (Rudolphi, 1808) - PE, PB,
RN, CE, PI
Brandão et al. (2009)b, Santos (2013)b,c
Morphotype 1
Morphotype 2
Morphotype 3
Morphotype 4
Morphotype 5
Morphotype 6
Morphotype 7
Morphotype 8
Ideterminado

a Abbreviations of States: Ceará – CE; Distrito Federal – DF; Espírito Santo – ES; Goiás – GO; Mato Grosso do Sul – MS; Minas Gerais – MG; Pará – PA; Paraíba – PB; Paraná – PR; Pernambuco – PE; Piauí – PI; Rio de Janeiro – RJ; Rio Grande do Norte – RN; Rio Grande do Sul – RS; São Paulo – SP

bData obtained by coprological examination.

cData obtained by monographs, dissertations and theses.

dThey present zoonotic potential.

eReview article of mammalian parasites in Brazil.

Table 2 Morphological description of egg morphotypes found in Cerdocyon thous , in Brazil, according to different studies conducted between 1915 and 2017.  

Parasite species Morphological characteristics Measurement (µm) References
Superfamily Ancylostomatoidea Chabaud, 1965
Family Ancylostomatidae (Looss, 1905)
Ancylostoma buckleyi Not reported 108 × 83 Santos et al. (2003)
Morphotype 1 Oval shape, shell double, thin and smooth, poles big and round 56.5 × 38.5 Brandão (2007) ,
Brandão et al. (2009)
Morphotype 2 Elliptical shape, shell smooth, poles uneven 59 × 39
Morphotype 3 Elliptical or round shape, shell single, thin, smooth and transparent, embryo morulate or larvae well developed 58.5 × 40 Santos (2013)
Indeterminate Not reported 54 ×33 Santos (2008b)
Ascaridoidea Railliet & Henry, 1915
Ascarididae Baird, 1853
Toxocara sp. Not reported 71 × 42.5 Santos (2008b)
Round shape, shell thick and covered by a rugged and ornate outer shell, embryonic mass in development or larvae well developed 85 × 76 Santos (2013)
Morphotype 1 Not reported 31 × 20 Santos (2008a)
Morphotype 2 Not reported 46 × 28
Morphotype 3 Elliptical shape, shell rough 61 × 36 Brandão (2007) ,
Brandão et al. (2009)
Morphotype 4 Oval or round shape, shell double and irregularly thick 65 × 7
Morphotype 5 Elliptical shape, shell thick and smooth, embryonic mass in development 67 × 46 Santos (2013)
Superfamily Trichinelloidea Railliet, 1916
Family Trichuridae (Ransom, 1911)
Trichuris sp. Not reported 57 × 27 Chame (1988)
Not reported 57 × 25 Santos (2008a)
Indeterminate Not reported 59 × 31
Indeterminate Not reported 64 ×28.6 Santos (2008b)
Morphotype 1 Barrel shape, two polar opercula slightly flattened, shell thin, smooth and brown, embryonic mass in development 55 × 25 Santos (2013)
Morphotype 2 Barrel shape, two opercula unequal and little prominent, shell thin and clear, embryonic mass, large compared to the rest of this family 82.5 × 37.5
Morphotype 3 Barrel shape, two polar opercula symmetric, shell thick, dark brown, embryonic mass or larvae well developed 80 × 38
Morphotype 4 Barrel shape, two polar opercula symmetric and prominent, light brown, shell thick and smooth, embryonic mass in development 58 × 28
Family Capillariidae
Capillaria hepatica - 59 × 31 Ruas et al. (2003)
Superfamily Physalopteroidea Sobolev, 1949
Family Physalopteridae (Railliet, 1893)
Physaloptera tendernata Ellipsoidal shape, shell thin 27 × 16 Lima (2009)
Physaloptera praeputialis Ellipsoidal shape, shell thin - In utero 27 × 23
Physaloptera sp. Not reported 36 × 28 Santos (2008b)
Elliptical to round shape, shell thick and smooth, containing larvae 43 × 25 Brandão et al. (2009)
Indeterminate Not reported 51 × 30 Santos (2008a)
Indeterminate Elliptical shape, shell single, thick and smooth, larvae well formed 57 × 35 Santos (2013)
Superfamily Rhabditoidea Travassos, 1920
Family Strongyloididae Chitwood & McIntosh, 1934
Indeterminate Elliptical or rounded shape, shell single, smooth, thin and transparent, larvae formed 54 × 28 Santos (2013)
Superfamily Strongyloidea Weinland, 1858
Family Strongylidae Baird, 1853
Indeterminate Not reported Snak et al. (2017)
Superfamily Spiruroidea Oerley, 1885
Family Spirocercidae Chitwood & Wehr, 1932
Spirocerca lupi Not reported 25.5 × 8.5 Santos (2008b)
Elliptical shape and small size, shell thick and smooth, larvae well developed 36 × 14 Santos (2013)
Superfamily Trichostrongyloidea Cram, 1927
Indeterminate 40 × 18 Santos (2008a)
Morfotipo 1 Elliptical shape, long and thin, shell thin and smooth, one side slightly convex and the other concave, larvae well developed 54 × 19 Santos (2013)
Morfotipo 2 Elliptical shape and larger, shell thin, transparent and smooth, larvae well developed 65 × 29
Family Molineidae Skrjabin & Schulz, 1937
Molineus sp. Elliptical shape 42 × 16 Lima (2009)
Indeterminate Not reported 60 ×25
Superfamily Rictularoidea Railliet, 1916
Family Rictulariidae Railliet, 1916
Pterygodermatites pluripectinata Dairy eggs - In utero 39 × 28.5 Lima (2009)
Pterygodermatites affinis Dairy eggs - In utero 25 × 17
Indeterminate Round shape, shell smooth, simple and thick, larvae well formed 40 × 31 Santos (2013)
Superfamily Oxyuroidea Cobbold, 1864
Family Oxyuridae Cobbold, 1864
Enterobius vermicularis Asymmetric shape, shell smooth, simple and transparent, larvae developed, poles unequal, one sharper and one more rounded 60 × 32 Santos (2013)
Morphotype 1 Asymmetric shape, dark brown, simple and fluted membrane, embryonic mass, sometimes with developed larvae 87 × 48
Morphotype 2 Asymmetric shape, light brown or coppery, larvae robust and well formed, apparently with two thin membranes in the shell 132 × 63
Morphotype 3 Asymmetric shape, light brown or coppery, larvae robust, very similar to morphotype 2, but slightly larger in size 185 × 83
Morphotype 4 Asymmetric shape, light brown or yellowish, shell simple and thin, larvae well developed 212 × 93
Morphotype 5 Asymmetric shape, shell double and thin, colorless, larvae in formation 99 × 43
Phylum Nematoda (Rudolphi, 1808) Santos (2008a) ,
Brandão et al. (2009) , Santos (2013)
Morphotype 1 Not reported 44 × 22.5
Morphotype 2 Not reported 27 × 14
Morphotype 3 Shell double and thick, larvae usually present, with protrusion at one end similar to an operculum 34 × 19
Morphotype 4 Shell oval and thick, with rounded structure slightly protruding at one end, may also be an operculum 60 × 47
Morphotype 5 Elliptical shape, shell thick, simple and smooth, larvae well formed 45.5 × 26
Morphotype 6 Elliptical shape, shell transparent, thin and smooth, larvae well formed 58.5 × 28
Morphotype 7 Barrel shape, shell smooth and relatively thick, dark brown, different polar regions, only one operculum, embryonic mass or larvae well developed 35 × 20
Morphotype 8 Round shape, medium size, shell smooth, thin, transparent, embryonic mass present 72 × 51

The nematodes found in the tongue of Cerdocyon thous, collected in the municipality of Paragominas, Pará State, in eastern Amazon, have similar characteristics to those of other species of the family Capillaridae Railliet, 1915, and genus Capillaria Zeder, 1800. The diagnosis of infection by Capillaria in this study is based on the presence of eggs with bipolar plugs, as well as the morphological characteristics of the nematodes found in the tongue. Capillariidae, one of the five families belonging to the superfamily Trichinellidea, comprise more than 300 known species of nematodes that parasitize all classes of vertebrates around the world ( ANDERSON, 2000 ; GIBSON, 2012 ; STAPF et al., 2013 ).

In the last 100 years, three taxonomic inventories of parasites in mammals were conducted, resulting in 13 superfamilies reported for the nematofauna of C. thous in Brazil ( VICENTE et al., 1997 ; VIEIRA et al., 2008 ; PINTO et al., 2011 ). Among the nematodes that comprise the nematofauna of C. thous, the members of the superfamily Ancylostomatoidea were the most representative in terms of number of species, such as Uncinaria carinii Travassos, 1915, Ancylostoma buckleyi Le Roux & Biocca, 1957, Ancylostoma caninum Ercolani, 1859, Ancylostoma braziliense Faria, 1910, and Ancylostoma sp. In addition to nematode adults, two egg morphotypes were found, as well as individuals that were not identified to the specific taxonomic level; although, they had features of this superfamily.

In Brazil, superfamily Trichinelloidea is represented by two families, (Trichuridae and Capillariidae), three genera (Trichuris, Capillaria, Pearsonema) and the following four species: Trichuris vulpis Froelich, 1789, a parasite of the cecum of the large intestine in host from Mato Grosso do Sul and Paraíba sates ( VIEIRA et al., 2008 ; LIMA 2009 ; PINTO et al., 2011 ; CURI et al., 2010 ; LIMA et al., 2013 ); Pearsonema linsi Freitas & Lent, 1935 and Pearsonema feliscati Diesing, 1851, parasites of the urinary bladder in host from Rio de Janeiro state ( VIEIRA et al., 2008 ); and C. hepatica, a parasite of the liver in host from Rio Grande do Sul state ( RUAS et al., 2003 ). In addition, Capillaria sp. occurs in different states of Brazil: Rio Grande do Sul ( RUAS, 2005; RUAS et al., 2008 ), Paraná ( SNAK et al., 2017 ) and Minas Gerais ( CURI et al., 2010 ).

This is the first report of a Capillaria infection in the tongue of C. thous in Brazil, but the occurrence of capillariids in the tongue of mammals has already been reported for other countries. Copland (1975) reports that C. papuensis parasitizes the tongue of Sus scrofa papuensis in Papua New Guinea. Scapino & Murphy (1978) describe the infection of the mucous membranes of the oral cavity of Procyon lotor , and suggests that the parasite is possibly Capillaria procyonis. Snyder (1988 , 1989 ) reports the occurrence of eggs of C. procyonis in the tongue of Procyon lotor; both accounts were for Illinois, in the United States. Capillaria garfiai is reported to parasitize the tongue of wild Sus scrofa in Spain ( FERRER & CASTELLÀ, 1996 ).

Löwenstein & Kutzer (1989) reported C. garfiai in wild boar in Austria, found a prevalence of 69% based on histopathological studies, and demonstrated that parasitism by C. garfiai in the tongue of this animal produces small pathological changes in the lingual tissue, which is different from what is reported in this article, since the nematodes did not cause injury.

In Brazil, parasitism by capillariids includes different species of parasites and hosts, and C. hepatica is the most commonly cited in the literature as a parasite of wild animals, such as those found in Sciurus aestuans ( FREITAS & LENT, 1936 ), Rattus norvegicus ( ARAUJO, 1967 ; GALVÃO, 1981 ). Rattus rattus ( CHIEFFI et al., 1981 ), dogs and cats ( SILVEIRA et al., 1975 ), Tayassu tajacu ( MANDORINO & REBOUÇAS, 1991 ), Chrysocyon brachyurus ( VICENTE et al., 1997 ) and Lycalopex gymnocercus ( RUAS et al., 2003 ). Eggs of C. hepatica were found in insects ( SOLOMON & HANDLEY, 1971 ; FARHANG-AZAD, 1977 ). Lima et al. (2008) reported the occurrence of eggs of Capillaria spp. in the filet of Pseudupeneus maculatus Bloch, 1793, a fish sold in the metropolitan region of Recife, Pernambuco state, and noted the zoonotic potential of the genus and the need for more hygienic and sanitary control of the quality of the product offered to the consumer.

For C. thous, Ruas et al. (2003) reported the first case of parasitism of C. hepatica in the state of Rio Grande do Sul. In the state of Pará, Moreira et al. (2013) describes parasitism by C. hepaticum in synanthropic rodents R. norvegicus and R. rattus. Although Moravec (1982) included C. hepatica in the genus Calodium ( Calodium hepaticum), this name is rarely used, and many authors place it in Capillaria.

The site of infection of the capillariids reported in this study is possibly an erratic occurrence in the cycle of this parasite, and the hosts acquired the infection due to certain habits, such as licking the genitals and anus of other animals in the same pack. The life cycle of capillariids is monoxenic and the infection occurs by ingestion of infective eggs after death (e.g., due to cannibalism or predation) and decomposition of the host ( FARHANG-AZAD & SCHLITTER, 1978 ; KATARANOVSKI et al., 2010 ).

The presence of capillariids in C. thous and other wild canids is possibly related to their diet, which includes wild and urban rodents, and is often influenced by habitat loss and the ease of obtaining food close to urban centers. Ruas et al. (2003) describes capillariids as parasites of the hepatic parenchyma and urinary bladder of multiple hosts, which are most commonly found in rodents, especially rats. Pedó et al. (2006) describe C. thous as a versatile predator and that small rodent species are the most important food item in its diet, with a 52.8% relative frequency, including at least seven species from distinct habits, such as open areas (Cavia aperea Erxleben, 1777), semi-aquatic (Holochilus brasiliensis Desmarest, 1819), cursorial in forest and open areas (Akodon sp.), semi-arboreal (Oligoryzomys sp.), arboreal (Phyllomys dasythrix Hensel, 1872), semi-fossorial in forest and open areas (Oxymycterus sp.) and peridomiciliary ( Mus musculus Linnaeus, 1758). Birds, insects and fruits, as well as consuming the most abundant food resources in each season, have also been reported ( BISBAL & OJASTI, 1980 ; BERTA 1987 ; MOTTA-JUNIOR et al., 1994 ).

Conclusions

The presence of eggs and nematodes of Capillaria sp. in the tongue of C. thous is extremely important, not only as a public health issue, but to the knowledge of the biodiversity of zoonotic parasites present in wild populations of canids. However, an explanation of why the eggs and nematodes were in the epithelial and connective tissues of the tongue remains unclear since, until now, this has not been observed in the biological cycle of the species. Parasitism of C. thous by capillariids in Pará state requires a more detailed investigation into the circumstances of this finding, in order to obtain adults for morphological and molecular analyses that can elucidate the epidemiological implication of this parasitism and the potential zoonotic factor of this species, as well as to determine the wild rodents that can serve as reservoirs for the parasite.

Acknowledgements

The authors are grateful to the following the Laboratório de Histologia e Embriologia Animal and Laboratório de Microscopia Eletrônica de Varredura – Instituto da Saúde e Produção Animal – Universidade Federal Rural da Amazônia – UFRA, campus Belém, state of Pará, Brazil for the use of the scanning electron microscope. This study is part of the Ph.D. thesis of Raul Henrique da Silva Pinheiro, developed for the Programa de Pós-Graduação em Biologia de Agentes Infecciosos e Parasitários, Instituto de Ciências Biológicas, Universidade Federal do Pará-UFPA. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001", Ministério da Educação do Brasil.

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Received: July 18, 2018; Accepted: September 05, 2018

* Corresponding author: Elane Guerreiro Giese. Laboratório de Histologia e Embriologia Animal, Instituto da Saúde e Produção Animal, Universidade Federal Rural da Amazônia – UFRA, Av. Presidente Tancredo Neves, 2501, Terra Firme, CEP 66077-830, Belém, PA, Brasil. e-mail: elane.giese@ufra.edu.br

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