ABSTRACT
Cerdocyon thous is considered the most common wild canid in Rio Grande do Sul, and can serve as a host for several parasites, playing an important role in maintaining the biological cycle. Despite being a widespread and abundant species, they have a relatively little-known fauna of endo and ectoparasites, mainly focusing on the different regions of their occurrence. With this work, the objective was to report the multiparasitism in a specimen of C. thous in the Brazilian Pampa. Using modified Centrifuge-Flotation and Spontaneous Sedimentation techniques, a high taxonomic diversity of parasites was observed, and the finding of eggs compatible with Lagochilascaris spp. in C. thous in Brazil, in addition to Uncinaria spp. eggs and Cystoisospora spp. oocysts in the same host in the south of the country. The presence of eggs of different helminths in the feces of C. thous is extremely important, mainly for public health, but also for the knowledge of the biodiversity of parasites present in wild populations of canids, until then little studied, thus allowing the implementation of control programs.
Keywords:
coproparasitological; endoparasites; wild fauna
RESUMO
Cerdocyon thous é considerado o canídeo silvestre mais comum no Rio Grande do Sul e pode servir como hospedeiro de diversos parasitos, desempenhando papel importante na manutenção do ciclo biológico. Mesmo sendo uma espécie difundida e abundante, têm uma fauna de endo e ectoparasitos relativamente pouco conhecida, principalmente enfocando as diferentes regiões de sua ocorrência. Com este trabalho, objetivou-se relatar o multiparasitismo em um espécime de C. thous no Pampa brasileiro. Por meio das técnicas de centrifugo-flutuação modificada e sedimentação espontânea, observou-se uma alta diversidade taxonômica de parasitos, sendo relatado, pela primeira vez, o achado de ovos compatíveis com Lagochilascaris spp. em C. thous no Brasil, além de ovos de Uncinaria spp. e oocistos de Cystoisospora spp. no mesmo hospedeiro, no sul do país. A presença de ovos de diferentes helmintos nas fezes de C. thous é de extrema importância, principalmente na saúde pública, mas também para o conhecimento da biodiversidade de parasitos presentes em populações silvestres de canídeos, até então pouco estudados, permitindo, assim, a implementação de programas de controle.
Palavras-chave:
coproparasitológico; endoparasitos; fauna silvestre
INTRODUCTION
Cerdocyon thous (Linnaeus, 1758), popularly known as "Cachorro-do-mato" or "Graxaim-do-mato", is a species of canid widely distributed in South America, occurring in almost all of Brazil, except in the amazon (Wilson and Reeder, 2005WILSON, D.E.; REEDER, D.M. Mammal species of the world: a taxonomic and geographic reference. 3.ed. Baltimore: Johns Hopkins University Press, 2005. 2000p.). It is found in forest and field areas, being considered the most common wild canid in Rio Grande do Sul (Dotto et al., 2001DOTTO, J.C.; FABIAN, M.E.; MENEGHETI, J.O. Atuação de Pseudalopex gymnocercus (Fischer, 1814) e de Cerdocyon thous (Linnaeus, 1776) (Mammalia Canidae) como fator de mortalidade de cordeiros no sul do Brasil. Bol. Soc. Biol. Concepcion, v.72, p.44-52, 2001.). It has a nocturnal and solitary habit, moves rarely, and lives in pairs, going along trails, forest edges and roads in search of food (Berta, 1982BERTA, A. Cerdocyon thous. Mamm. Species, v.186, p.1-4, 1982.).
This canid can serve as a host for several parasites and can play an important role in maintaining the biological cycle, mainly due to its generalist habits, tolerance to anthropogenic disturbances and interaction with other wild and domestic species (Curi, 2005).
Studies of endo and ectoparasites in wild animals are important in investigating the biodiversity of species and in determining the risk that parasites may pose to public health (Martins et al., 2004MARTINS, J.R.; MEDRI, I.M.; OLIVEIRA, C.M.; GUGLIELMONE, A. Ocorrência de carrapatos em Tamanduá-Bandeira (Myrmecophaga tridactyla) e Tamanduá Mirim (Tamandua tetradactyla) na Região do Pantanal Sul Mato-grossense, Brasil. Cienc. Rural, v.34, p.293-295, 2004.). However, for most wild species, there is still a lack of information. Even widespread and abundant species, such as C. thous, have a relatively little-known parasite fauna, mainly focusing on the different regions of their occurrence, and their role as a dispersing agent.
This work aimed to report the multiparasitism in a specimen of Graxaim-do-mato (Cerdocyon thous) in the Brazilian Pampa, including new records.
CASUISTRY
A fecal sample of an adult female Graxaim-do-mato (Cerdocyon thous) was received for parasitological diagnosis in the laboratory of the Study Group on Parasitic Diseases of the Federal University of Pelotas. The modified Zinc Sulfate Flotation Centrifuge techniques were used, as described by Monteiro (2017MONTEIRO, S.G. Parasitologia na medicina veterinária. 2.ed. Rio de Janeiro: Roca, 2017. 370p.) and Spontaneous sedimentation (Hoffmann et al., 1934HOFFMAN, W.A.; PONS, J.A.; JANER, J.L. Sedimentation concentration method in Schistosomiasis mansoni. Puerto Rico J. Public Health Trop. Med., v.9, p.283-298, 1934.).
For identification, all structures that could identify or differentiate an egg, in its smallest possible taxon, such as characteristics and shell ornaments, embryonic and larval formation, existence of operculum and aculea, were used. The identification was done by comparing the morphometry found with that of species previously described in the literature for the host species, using an Olympus optical microscope (CX22 series) (Monteiro, 2017MONTEIRO, S.G. Parasitologia na medicina veterinária. 2.ed. Rio de Janeiro: Roca, 2017. 370p.; Scioscia et al., 2018SCIOSCIA, N.P.; OLMOS, L.; GOROSÁBEL, A.; BERNAD, L. et al. Natural infection in Pampas fox (Lycalopex gymnocercus) by Lagochilascaris major Leiper, 1910 (Nematoda: Ascarididae) in Buenos Aires, Argentina. Parasitol. Res., v.117, p.3023-3027, 2018.; Araujo, 2020ARAUJO, R.B. Diversidade de parasitas gastrointestinais em cachorro-do-mato (Cerdocyon thous, LINNAEUS 1766) na região metropolitana de Fortaleza. 2020. 66f. Dissertação (Mestrado) - Programa de Pós-Graduação em Ciências Veterinárias, Universidade Estadual do Ceará, CE.; ; Izdebska and Rolbiecki, 2020IZDEBSKA, J.N.; ROLBIECKI, L. The Biodiversity of Demodecid Mites (Acariformes: Prostigmata), Specific Parasites of Mammals with a Global Checklist and a New Finding for Demodex sciurinus. Diversity, v. 12, p.1-29, 2020.; Ferraz et al., 2021FERRAZ, A.; BARWALDT, E.T.; CASTRO, T.A.; LIMA, C.M. et al. Coproparasitological diagnosis of Lagochilascaris sp. in domestic cat (Felis catus). Rev. Acad. Ciênc. Anim., v.19, p.1-5, 2021.). The mean and standard deviation were calculated using measurements of five eggs, oocysts, and mites, using the EpiTools epidemiological calculator (Sergeant, 2018SERGEANT, E.S.G. Epitools epidemiological calculators. Ausvet. 2018. Available in: http://epitools.ausvet.com.au. Accessed in: 27 Sep. 2022.
http://epitools.ausvet.com.au...
).
In the present report, we observed a high taxonomic diversity of parasites diagnosed through the examination of C. thous faeces, including new records, which are illustrated in figure 1. The average measurements are shown in table 1. In total, eggs of six helminths, oocysts of one protozoan and one mite were observed; compatible with: Spirometra spp. (Figure 1 - A), Alaria sp. (Figure 1 - B), Lagochilascaris spp. (Figure 1 - C), Demodex canis (Figure 1 - D), Capillaria spp. (Figure 1 - E), Uncinaria spp. (Figure 1 - F), Ancylostoma spp. (Figure 1 - G) and Cistoisospora spp. oocysts (Figure 1 - H).
DISCUSSION
Except for D. canis and Cystoisospora spp., all the others have zoonotic potential and, therefore, can parasitize humans. According to Murphy et al. (2012MURPHY, T.M.; O’CONNELL, J.; BERZANO, M.; DOLD, C. et al. The prevalence and distribution of a potential zoonotic parasite, in foxes in Ireland. Parasitol. Res., v.111, p.283-290, 2012.), more than 45% of zoonotic pathogens have a carnivorous host in their life cycle. Thus, wild canids play an important role in the maintenance and transmission of pathogens.
Infection by the nematode Capillaria spp., tapeworm Spirometra spp. and the trematode Alaria spp. was previously reported in the region by Lucas (2000LUCAS, A. S. Estudo qualitativo da fauna parasitária de canídeos silvestres na Região Sul do Rio Grande do Sul. 2000. 41f. Monografia (Conclusão de Curso) - Graduação em Ciências Biológicas, Universidade Federal de Pelotas, Pelotas, Rio Grande do Sul, RS.) and Ruas (2007RUAS, J.L. Caracterização da fauna parasitária do Pseudalopex gymnocercus (graxaim-do-campo) e do Cerdocyon thous (graxaim-do-mato) na região sul do Rio Grande do Sul. Acta Sci. Vet., v.35, p.257-258, 2007.). And according to Ruas (2007), they had a prevalence of 5.56%, 61.11% and 50%, respectively, in the same host species. Both have a heteroxenic life cycle, requiring at least one intermediate host (Monteiro, 2017MONTEIRO, S.G. Parasitologia na medicina veterinária. 2.ed. Rio de Janeiro: Roca, 2017. 370p.). The origin of the infection is possibly due to the canids' diet, which is considered omnivorous and quite diversified, consisting of the consumption of freshwater fish and crustaceans, mollusks, and different vertebrates (birds, reptiles, amphibians, small mammals) that would act as intermediate or paratenic hosts of helminths and, therefore, need an environment with the presence of areas with good irrigation, which favor the development of some of them (Dotto et al., 2001DOTTO, J.C.; FABIAN, M.E.; MENEGHETI, J.O. Atuação de Pseudalopex gymnocercus (Fischer, 1814) e de Cerdocyon thous (Linnaeus, 1776) (Mammalia Canidae) como fator de mortalidade de cordeiros no sul do Brasil. Bol. Soc. Biol. Concepcion, v.72, p.44-52, 2001.). Furthermore, considering that wild animals can become infected and harbor metacerparous, they act as living beings of Alaria (Jaksic et al., 2002JAKSIC, S.; UHITIL, S.; MARIJA, V. Mesocercariae of fluke Alaria alata determined in wild boar meat. Z. Jagdwissenschaft, v.48, p.203-207, 2002.), also serving as a source of fermentation for wild canids and humans. Due to the presence of wild boar (Sus scrofa) and wild hog (Sus scrofa scrofa) in the study region, similar situations may occur, where the species can serve as a source of occurrence.
The observation of oocysts performed with Cystoisospora spp. and eggs hatched with Uncinaria spp. and Ancylostoma spp. may be related to the presence of the domestic dog, preferential for the parasites. It is common to use dogs in field management with sheep and cattle herds in this region, which allows these animals to move in the habitat of wild canids, that is, there is an overlap of niches between species of canids (wild and domestic) allowing the infection (Port, 2002PORT, D. Partilha de recursos entre duas duas espécies de canídeos (Cerdocyon thous e Pseudalopex gymnocercus) simpátricos no sul do Brasil. 2002. 42f. Dissertação (Mestrado) - Programa de Pós-Graduação em Biologia: Diversidade e Manejo de Vida Silvestre, Universidade do Vale do Rio dos Sinos, São Leopoldo, Rio Grande do Sul, RS.). Vizcaychipi et al. (2016VIZCAYCHIPI, K.A.; RINAS, M.; IRAZU, L.; MIYAGI, A. et al. Neotropical zoonotic parasites in bush dogs (Speothos venaticus) from upper Paraná Atlantic forests in Misiones, Argentina. Vector Borne Zoonotic. Dis., v.16, p.664-672, 2016.) observed Cystoisospora spp. oocysts in feces of bush dog (Speothos venaticus) in Misiones province, Argentina. In Brazil, infection by this coccidia in C. thous had only been reported in a young animal treated at the Veterinary Hospital of the Federal University of Sergipe (Silva et al., 2017SILVA, M.A.D.; SCHETTINO, S.C.; MAGALHÃES, L.A. et al. Cistoisosporose em cachorro do mato, Cerdocyon thous Linnaeus, 1966 (CARNIVORA, CANIDAE) - relato de caso. In: CONGRESSO BRASILEIRO DA ANCLIVEPA, 38., 2017, Recife. Anais... Recife: CBA, 2017, p.1730. (Resumo).). Uncinaria spp. was described parasitizing C. thous in the city of São Paulo (Travassos, 1915TRAVASSOS, L. Uncinaria carinii n. sp. (nota prévia). Braz. Méd., v.29, p.79-80, 1915.;) and in the coproparasitological diagnosis of an animal of the same species in Fortaleza, Ceará (Araújo, 2020). Now, both are reported for the first time in southern Brazil in this host. In contrast, Ancylostoma spp. was identified as the most frequent parasite in C. thous in the same region of the present study (Ruas, 2007RUAS, J.L. Caracterização da fauna parasitária do Pseudalopex gymnocercus (graxaim-do-campo) e do Cerdocyon thous (graxaim-do-mato) na região sul do Rio Grande do Sul. Acta Sci. Vet., v.35, p.257-258, 2007.).
The presence of Demodex canis in the feces can be explained considering that these parasites, at all stages, can be found in the lymph nodes, intestinal wall, spleen, liver, kidneys, bladder, lung, thyroid, blood, urine and feces, in addition to of the dermis (within the hair follicle and in the sebaceous glands). However, when observed in these extracutaneous organs, they may be usually dead and degenerated, representing a drainage to any of these areas, via the blood or lymphatic stream of the infested animal (Oliveira, 2005OLIVEIRA, M.C. Anticorpos anti-Demodex canis e Dermatophagoides pteronyssinus em soro de cães com demodicose. 2005. 65f. Dissertação (Mestrado) - Programa de Pós-Graduação em Imunologia e Parasitologia Aplicadas, Universidade Federal de Uberlândia, Uberlândia, MG.; Monteiro, 2017MONTEIRO, S.G. Parasitologia na medicina veterinária. 2.ed. Rio de Janeiro: Roca, 2017. 370p.). So far, only four species have been described parasitizing canids: Demodex canis, Demodex cornei, Demodex cyonis and Demodex injai (Izdebska and Rolbiecki, 2020IZDEBSKA, J.N.; ROLBIECKI, L. The Biodiversity of Demodecid Mites (Acariformes: Prostigmata), Specific Parasites of Mammals with a Global Checklist and a New Finding for Demodex sciurinus. Diversity, v. 12, p.1-29, 2020.). The differences between these species are limited to the size of the mite (Delayte, 2015DELAYTE, E.H. Demodicidose canina. In: LARSSON.C.E.; LUCAS, R. (Eds.). Tratado de medicina externa dermatologia veterinária. São Caetano do Sul: Interbook, 2015. p.369-389.). However, molecular studies concluded that D. canis (224.3 ± 18.3 μm in length) and D. cornei (156.9 ± 11.12 μm in length) are the same mite with variations in size, and that D. injai is a species phylogenetically distinct from D. canis, with greater length (males with 361 ± 44μm and females with 334 ± 29μm in length) (Rojas et al., 2012ROJAS, M.; RIAZZO, C.; CALLEJÓN, R.; GUEVARA, D. et al. Molecular study on three morphotypes of Demodex mites (acarina: Demodicidae) from dogs. Parasitol. Res., v.111, p.2165-2172, 2012.; Sastre et al., 2012SASTRE, N.; RAVERA, I.; VILLANUEVA, S.; ALTET, L. et al. Phylogenetic relationships in three species of canine Demodex mite based on partial sequences of mitochondrial 16S rDNA. Vet. Dermatol., v.23, p.509, 2012.; Morita et al., 2018MORITA, T.; OHMI, A.; KIWAKI, A.; IKE, K. et al. A New stubby species of demodectic mite (Acari: Demodicidae) from the domestic dog (Canidae). J. Med. Entomol. v.55, p.323-328, 2018.). Also, according to Izdebska and Rolbiecki (2020), D. cyonis is described as a “short” species of Demodecidae, where males are 169.38 ± 13.89 μm in length and females are 168.8 ± 12.02 μm in length (Morita et al., 2018).
The finding of eggs compatible with those of Lagochilascaris spp. is recorded for the first time in C. thous feces in Brazil. The eggs of the parasites of this genus have a thick shell and have between 15 and 45 pits around the circumference (L. major: 33 to 45; L. minor: 15 to 26), similar to a “bottle cap” (Moura et al., 2012MOURA, M.Q.; JESKE, S.; GALLINA, T.; BORSUK, S. et al. First report of Lagochilascaris (Nematoda: Ascarididae) eggs in a public park in Southern Brazil. Vet. Parasitol., v.184, p.359-61, 2012.; Ferraz et al., 2021FERRAZ, A.; BARWALDT, E.T.; CASTRO, T.A.; LIMA, C.M. et al. Coproparasitological diagnosis of Lagochilascaris sp. in domestic cat (Felis catus). Rev. Acad. Ciênc. Anim., v.19, p.1-5, 2021.). Recently, Scioscia et al. (2018SCIOSCIA, N.P.; OLMOS, L.; GOROSÁBEL, A.; BERNAD, L. et al. Natural infection in Pampas fox (Lycalopex gymnocercus) by Lagochilascaris major Leiper, 1910 (Nematoda: Ascarididae) in Buenos Aires, Argentina. Parasitol. Res., v.117, p.3023-3027, 2018.) recorded Lagochilascaris minor in Lycalopex gymnocercus in Buenos Aires, Argentina, and Vizcaychipi et al. (2016VIZCAYCHIPI, K.A.; RINAS, M.; IRAZU, L.; MIYAGI, A. et al. Neotropical zoonotic parasites in bush dogs (Speothos venaticus) from upper Paraná Atlantic forests in Misiones, Argentina. Vector Borne Zoonotic. Dis., v.16, p.664-672, 2016.) found eggs of Lagochilascaris spp. in vinegar dog (Speothos venaticus) feces in the province of Misiones, in the same country. In the region of the present study, the parasite has already been reported in Leopardus geoffroyi (Trindade et al., 2019TRINDADE, M.A.C.; MACEDO, M.R.P.; DREHMER, C.J.; MULLER, G. First record of Lagochilascaris minor (Nematoda: Ascarididae) in Leopardus geoffroyi (Carnivora: Felidae) in Brazil. Rev. Bras. Parasitol. Vet., v.28, p.812-815, 2019.) and in domestic cats (Ferraz et al., 2021) in addition to egg findings in public squares (Moura et al., 2012). As infection by this parasite occurs through ingestion of the meat of the intermediate host, mainly rodents, containing encysted larvae (Monteiro, 2017MONTEIRO, S.G. Parasitologia na medicina veterinária. 2.ed. Rio de Janeiro: Roca, 2017. 370p.), the infection is linked to the host's eating habits. In addition, the increasing use of areas that serve as habitat for several wild species, for agricultural production purposes, has increased the possibility of contact between wild and domestic animals, favoring the transposition of parasites from one host to another (Ruas, 2007RUAS, J.L. Caracterização da fauna parasitária do Pseudalopex gymnocercus (graxaim-do-campo) e do Cerdocyon thous (graxaim-do-mato) na região sul do Rio Grande do Sul. Acta Sci. Vet., v.35, p.257-258, 2007.).
Knowledge of the parasites that occur in a given region is of fundamental importance for the establishment of sanitary control programs. However, it requires a more detailed investigation into the circumstances of this finding, to obtain adults for morphological and molecular analyzes that can elucidate the epidemiological implication of this parasitism.
Eggs, oocysts, and mite diagnosed in feces of Graxaim-do-mato (Cerdocyon thous) in southern Rio Grande do Sul, BR. 400X magnification. (A) Spirometra spp.; (B) Alaria sp.; (C) Lagochilascaris spp.; (D) Demodex canis; (E) Capillaria spp.; (F) Uncinaria spp.; (G) Ancylostoma spp.; (H) Cistoisospora spp.
Mean values of measurements, in μm, of eggs, oocysts and mites diagnosed in feces examination of Graxaim-do-mato (Cerdocyon thous) in the south of Rio Grande do Sul, BR.
CONCLUSION
Eggs compatible with Lagochilascaris spp. in C. thous in Brazil, in addition to Uncinaria spp. and oocysts of Cystoisospora spp. in the same host in the south of the country were found. The presence of eggs of different helminths in the feces of C. thous is extremely important, mainly for public health, but also for the knowledge of the biodiversity of parasites present in wild populations of canids, until then little studied, thus allowing the implementation of control programs.
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- MARTINS, J.R.; MEDRI, I.M.; OLIVEIRA, C.M.; GUGLIELMONE, A. Ocorrência de carrapatos em Tamanduá-Bandeira (Myrmecophaga tridactyla) e Tamanduá Mirim (Tamandua tetradactyla) na Região do Pantanal Sul Mato-grossense, Brasil. Cienc. Rural, v.34, p.293-295, 2004.
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- MORITA, T.; OHMI, A.; KIWAKI, A.; IKE, K. et al. A New stubby species of demodectic mite (Acari: Demodicidae) from the domestic dog (Canidae). J. Med. Entomol. v.55, p.323-328, 2018.
- MOURA, M.Q.; JESKE, S.; GALLINA, T.; BORSUK, S. et al. First report of Lagochilascaris (Nematoda: Ascarididae) eggs in a public park in Southern Brazil. Vet. Parasitol., v.184, p.359-61, 2012.
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- ROJAS, M.; RIAZZO, C.; CALLEJÓN, R.; GUEVARA, D. et al. Molecular study on three morphotypes of Demodex mites (acarina: Demodicidae) from dogs. Parasitol. Res., v.111, p.2165-2172, 2012.
- RUAS, J.L. Caracterização da fauna parasitária do Pseudalopex gymnocercus (graxaim-do-campo) e do Cerdocyon thous (graxaim-do-mato) na região sul do Rio Grande do Sul. Acta Sci. Vet., v.35, p.257-258, 2007.
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Publication Dates
-
Publication in this collection
17 Apr 2023 -
Date of issue
Mar-Apr 2023
History
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Received
05 Oct 2022 -
Accepted
09 Nov 2022