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Arquivo Brasileiro de Medicina Veterinária e Zootecnia

versão On-line ISSN 1678-4162

Arq. Bras. Med. Vet. Zootec. vol.68 no.3 Belo Horizonte mai./jun. 2016

http://dx.doi.org/10.1590/1678-4162-8157 

Veterinary Medicine

Endoparasites of wild animals from three biomes in the State of Mato Grosso, Brazil

Endoparasitas de animais silvestres de três biomas do Mato Grosso, Brasil

D.G.S. Ramos1 

A.R.G.L.O. Santos2 

L.C. Freitas2 

S.H.R. Correa2 

G.V. Kempe2 

T.O. Morgado2 

D.M. Aguiar2 

R.W. Wolf2 

R.V. Rossi2 

A.L. Sinkoc2 

R.C. Pacheco2 

1Universidade Federal de Goiás - Jataí, GO

2Universidade Federal de Mato Grosso ˗ Cuiabá, MT

ABSTRACT

The population of wild animals is regulated by many biotic and abiotic factors, and parasites are a biotic factor that affects the dynamic and density of host populations. From 2002 to 2014, 62 wild animals from the biomes Pantanal, Amazon, and "Cerrado" (or Savanna), which died in attendance in the veterinary hospital or have been road-killed, underwent necropsy for parasitological examination. Overall, 36 species of parasites were identified from 24 host species. Among the parasites, the most prevalent order was Oxyurida (29.1%), followed by Strongylida (20.9%), Spirurida (19.4%), Ascaridida (16.2%), Pentastomida (3.2%), Echinostomida (3.2%), Gygantorhynchia (3.2%), Rhabditida (1.6%), Plagiorchiida (1.6%), and Monilimorfida (1.6%), especially nematodes, which have more biotic potential and is more easily adapted to the environment than other classes. The occurrence of endoparasites was observed more frequently in endothermic than ectothermic animals, and herein is reported eleven new host occurrences for endoparasites in wild animals. The study has contributed to the knowledge on the biodiversity of parasites in wild animals from three biomes in central-western Brazil.

Keywords: helminths; parasitism; Amazon; Cerrado; Pantanal

RESUMO

Populações de animais selvagens são reguladas por diversos fatores bióticos e abióticos, e parasitas são um fator biótico que afetam a dinâmica e a densidade de populações. De 2002 até 2014, 62 animais silvestres provenientes dos biomas Pantanal, Amazônia e Cerrado, que vieram a óbito no atendimento do hospital veterinário ou foram encontrados atropelados em rodovias, foram submetidos à necropsia parasitológica. Ao todo 36 espécies de parasitas foram identificadas em 24 espécies de hospedeiros. Entre os parasitas, a ordem mais prevalente foi Oxyurida (29,1%), seguida por Strongylida (20,9%), Spirurida (19,4%), Ascaridida (16,2%), Pentastomida (3,2%), Echinostomida (3,2%), Gygantorhynchia (3,2%), Rhabditida (1,6%), Plagiorchiida (1,6%) e Monilimorfida (1,6%), destacando-se os nematódeos, por seu maior potencial biótico e facilidade de adaptação ao meio do que as demais classes. A maior ocorrência de endoparasitas foi observada em animais endotérmicos que ectotérmicos, e este estudo registra onze novas ocorrências de hospedeiros para endoparasitas de animais selvagens. O estudo contribui para o conhecimento da biodiversidade de parasitas em animais silvestres dos três biomas do Centro-Oeste do Brasil.

Palavras-chave: helmintos; parasitismo; Amazônia; Cerrado; Pantanal

INTRODUCTION

The population of wild animals is regulated by many biotic or abiotic factors, and parasites are a biotic factor that affects the dynamic and density of host populations (Anderson and May, 1979). The main relationships between parasites and hosts are that parasites may: kill their hosts; interfere in feeding and reproduction; contribute to the host dispersion; or not show any effect (Borgsteede, 1996). In this sense, serious problems may arise if a parasite is introduced into a new environment where suitable hosts are available, which are fully susceptible to these parasites (Borgsteede, 1996). Furthermore, most wild parasite biology is fully or partially unexplained, and may often occur in domestic animals and humans, such as have reported for Spirometra mansonoides and Sphaerirostris erraticus in cats by Ramos et al. (2013), and for sparganosis (Spirometra spp.) in humans by Mentz et al. (2011). These reports show how helminths that have wild animals as hosts in their life cycle may occur in domestic animals and humans in anthropic areas.

The Amazon biome is comprised of the Amazon forest, which is the biggest tropical forest in the world, with great richness of flora and fauna (Ab'Saber, 1977). The Pantanal biome is the largest tropical wetland area in the world. Located in central South America, including Brazil, Bolivia and Paraguay, the Pantanal ecosystem is characterized by flooding and drying cycles, which causes a constant movement of animals, variations in flora, and landscape changes (Junk and Cunha, 2005). It has been considered a World Natural Heritage and World Biosphere Reserve by UNESCO. Its fauna and flora are similar to the Brazilian "Cerrado" (Brazilian Savanna) biome (adjacent biome), which is a tropical savanna with unique and distinct characteristics from other savannas, with dimensions that extend across the Brazilian central plateau (Oliveira and Marquis, 2002). Although these biomes contain large preserved areas, animals routinely pass by roads or access the anthropic regions that are close to them.

Considering few records about parasite helminths in vertebrate species from these biomes, this study aimed to identify endoparasites in wild animals from the Pantanal, Amazon, and Cerrado biomes in the State of Mato Grosso, central-western Brazil.

MATERIALS AND METHODS

From 2002 to 2014, 62 wild animals from the Amazon (Alta Floresta, and Jauru municipalities), Cerrado (Chapada dos Guimarães and Cuiabá municipalities), and Pantanal (Poconé municipality) biomes (Fig. 1), that died in attendance in the veterinary hospital of the Federal University of Mato Grosso or were road-killed, were submitted to necropsy for parasitological examination. The esophagus, stomach, small intestine and large intestine were individually washed and filtered in 0.15 mm sieve, and examined in stereomicroscope under 10x magnification. The same procedure was performed with lungs, trachea, liver, heart, pancreas, kidneys, bladder, and the musculature (Ramos et al., 2013). All helminth parasites found were collected and processed according to Hoffman (1987). The identification was carried out following specific keys according to each taxonomic group: Anderson et al. (2009) and Gibbons (2010) for nematodes; and Bray et al. (2008) for trematodes. The specimens of Pentastomida have been clarified in Hoyer's medium and subsequently identified according to Riley et al. (1990). Revision works of Machado Filho (1950) were used to identify Acanthocephalans. The Ethic Committee on Animal Research of the Universidade Federal de Mato Grosso (UFMT) approved this study under protocol n° 23108.043095/13-6, and the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA) authorized the procedures for primates under the protocol n° 6364-1. Road-killed animals were cordially donated by IBAMA to the Veterinary Hospital of the Federal University of Mato Grosso.

Figure 1 Map of the biomes of Mato Grosso State, Brazil, and location of Alta Floresta, Jauru, Cuiabá, Chapada dos Guimarães and Poconé municipalities in their respective biomes. 

RESULTS

Overall, 36 species of parasites were identified from 24 host species and are listed in Table 1, according to hosts, animal's common name, number of parasitized animals, location of endoparasites, taxonomic identification, and location. Among parasites, the most prevalent order was Oxyurida (29.1%), followed by Strongylida (20.9%), Spirurida (19.4%), Ascaridida (16.2%), Pentastomida (3.2%), Echinostomida (3.2%), Gygantorhynchia (3.2%), Rhabditida (1.6%), Plagiorchiida (1.6%), and Monilimorfida (1.6%). Considering the animal regulation of body temperature, 49 endothermic animals were parasitized (79%) against 13 ectothermic animals (21%).

Table 1 Endoparasites found in wild vertebrates examined in the present study. Parasite specimens are deposited in the Laboratory of Parasitic Diseases, Veterinary Hospital, Federal University of Mato Grosso, Cuiabá, Mato Grosso State, Brazil. 

Hosts Common Name N Organs Endoparasites Identification Parasite Order Location Parasite Description Reference
Anphibians
Rhinella schneideri Cururu Toad 1 Lungs Rhabdias sp. Rhabditida Poconé Stiles and Hassall, 1906
Reptiles
Boa constrictor Boa 1 Celomatic Cavity Hastospiculum onchocercum Spirurida Chapada dos Guimarães Chitwood, 1932
3 Small Intestine Kalicephalus subulatus Strongylida Chapada dos Guimarães; Cuiabá; Poconé Molin, 1861
1 Celomatic Cavity Ophidascaris spp. Ascaridida Poconé Baylis, 1920
1 Lung Sebekia oxicephala*** Pentastomida Poconé Diesing, 1835
Eunectes murinus Anaconda 1 Stomach Physaloptera liophis*** Spirurida Poconé Vicente and Santos, 1974
1 Lung Sebekia oxicephala*** Pentastomida Poconé Diesing, 1835
Gerochelone carbonaria* - 1 Small Intestine Labiduris gulosa Ascaridida Cuiabá Rudolphi, 1819
Iguana iguana Green Iguana 2 Large Intestine Ozolaimus cirratus Oxyurida Chapada dos Guimarães; Cuiabá Linstow, 1906
Tupinambis sp. Crocodile Tegu 1 Stomach Physaloptera retusa Spirurida Chapada dos Guimarães Rudolphi, 1819
Birds
Crotophaga ani Smooth-billed Ani 1 Small Intestine Cyrnea semilunaris*** Spirurida Poconé Molin, 1860
Pavo cristatus Peafowl 1 Large Intestine Heterakis nattereri Strongylida Chapada dos Guimarães Travassos, 1923
Rhea americana Greater Rhea 1 Large Intestine Deletrocephalus spp. Strongylida Cuiabá Diesing, 1851
1 Celomatic Cavity Dicheilonema rheae Spirurida Chapada dos Guimarães Owen, 1843
1 Proventriculus Odontospirura zschokkei Spirurida Poconé Railliet and Henry, 1911
Mammals
Ateles chamek¹ Black Spider Monkey 1 Large Intestine Trypanoxyuris spp. Oxyurida Alta Floresta Vevers, 1923
Callicebus moloch Titi Monkey 1 Small Intestine Prosthenorchis sigmoides*** Gigantorhynchia Alta Floresta Machado Filho, 1950
Chrysocyon brachyurus*,² Maned Wolf 1 Small Intestine Ancylostoma caninum Strongylida Cuiabá Ercolani, 1859
Dasyprocta azarae Azara's Agouti 1 Large intestine Eucyathostomum copulatum Strongylida Chapada dos Guimarães Molin, 1861
Didelphis albiventris White-eared Opossum 2 Small Intestine Cruzia tentaculata Oxyurida Cuiabá Rudolphi, 1819
1 Liver Zonorchis spp. Plagiorchiida Cuiabá Travassos, 1944
Didelphis marsupialis Black-eared Opossum 2 Small Intestine Aspidodera spp. Ascaridida Cuiabá; Poconé Railliet and Henry, 1912
1 Small Intestine Cruzia tentaculata Oxyurida Poconé Rudolphi, 1819
Herpailurus yagouaroundi² Jaguarundi 1 Lung Metathelazia spp.*** Spirurida Poconé Skinker, 1931
Hydrochoerus hydrochaeris Capybara 1 Large Intestine Taxorchis schistocotyle Echinostomida Poconé Fischoeder, 1901
3 Large Intestine Protozoophaga obesa Oxyurida Chapada dos Guimarães Diesing, 1851
Mico emiliae Snethlage's Marmoset 2 Small Intestine Primasubulura spp. Ascaridida Alta Floresta Inglis, 1958
4 Large Intestine Trypanoxyuris callithricis*** Oxyurida Alta Floresta Solomon, 1933
Mico melanurus** Black-tailed Marmoset 4 Large Intestine Trypanoxyuris callithricis Oxyurida Chapada dos Guimarães; Cuiabá; Poconé Solomon, 1933
3 Small Intestine Primasubulura spp. Ascaridida Cuiabá Inglis, 1958
Myrmecophaga tridactyla¹ Giant Anteater 1 Small Intestine Moniliformis moniliformis*** Monilimorfida Chapada dos Guimarães Bremser, 1811
Panthera onca*,² Jaguar 1 Small Intestine Toxascaris leonina Ascaridida Cuiabá Linstow, 1902
Sapajus apella Tufted Capuchin 2 Lungs Filariopsis barretoi Strongylida Alta Floresta Travassos, 1921
1 Small Intestine Molineus torulosus Strongylida Alta Floresta Molin, 1861
3 Stomach Physaloptera spp. Spirurida Alta Floresta Rudolphi, 1819
1 Small Intestine Prosthenorchis sigmoides*** Gigantorhynchia Alta Floresta Machado Filho, 1950
1 Small Intestine Spirura spp. Spirurida Alta Floresta Blanchard, 1849
1 Small Intestine Trichostrongylus cesticillus Strongylida Alta Floresta Molin, 1861
1 Large Intestine Trypanoxyuris callithricis*** Oxyurida Alta Floresta Solomon, 1933
Tamandua tetradactyla* Southern Tamandua 1 Stomach Physaloptera praeputialis*** Spirurida Cuiabá Linstow, 1889
Tapirus terrestris¹ Lowland Tapir 2 Large Intestine Neomurshidia spp. Strongylida Jauru; Poconé Chabaud, 1957
1 Large Intestine Cladorchis pyriformis Echinostomida Jauru Diesing, 1838

N= numbers of specimens analyzed. *Animals raised in captivity in the zoo at the Federal University of Mato Grosso. **Only one specimen raised in the zoo at the Federal University of Mato Grosso. ***New host occurrence.

¹Risk of extinction according to both, IUCN (2014) and ICMBio (2014).

²Risk of extinction according to ICMBio (2014).

Among animals sampled, five were from captivity, and of these, three (Chrysocyon brachyurus, Panthera onca, and Tamandua tetradactyla) showed occurrence of parasites (Ancylostoma caninum, Toxascaris leonina, and Physaloptera praeputialis), commonly found in domestic animals. Furthermore, this study provided eleven new occurrences of endoparasites in wild animals as showed in Table 1.

DISCUSSION

Considering identification of three of the four major groups of helminths (nematodes, trematodes and acanthocephalans), as well as arthropods species (pentastomida - Sebekia oxycephala), this study showed diversity of endoparasites of wild animals commonly found in the Amazon, Pantanal, and Cerrado biomes. Between 1828 and 1829, Diesing and Rudolphi have described parasites of several species of hosts from the Pantanal region and Cuiabá municipality, State of Mato Grosso, which were deposited in Berlin and Vienna museums (Rego and Vicente, 1988). These and the samples collected by Travassos from 1922 to 1948, resulted practically in all parasitic fauna currently known that occurs in wild animals from Pantanal (Rego and Vicente, 1988). After these reports, there are few records of wild animals' helminths from Pantanal, and from other biomes of the State (Costa and Catto, 1994; Zattermann et al., 2005; Lopes Torres et al., 2009; Simões et al., 2010; Campião et al., 2014). The spectrum of parasitic disease in wild animals has great importance in human and veterinary medicine, and the knowledge about their parasites is essential since biotic and abiotic components may interfere in the dynamics and structure of parasite communities, as well as in the parasite communities of humans and domestic animals (Esch et al., 1990). The occurrence of Trypanoxyuris callithricis in primates of genera Sapajus and Mico, may be associated to the fact that T. callithricis has been adapted to parasitize infra communities of primates in Amazonia and Cerrado biomes, since it is commonly observed infecting Callithrix jacchus, and other species of the same gender (Vicente et al., 1997). This possible adaptation described above has also been observed in Prosthenorchis sigmoides, which was described parasitizing the small intestine of C. jacchus (Machado Filho, 1950), and herein it was detected in Callicebus moloch and Sapajus apella.

It is possible that the dynamics of infection may have possibly been modified in animals raised in captivity. Reports of Toxascaris leonina and Ancylostoma caninum detected in Panthera onca and Chrysocyon brachyurus, respectively, are scarce (Vincent et al., 1997). However, T. leonina has been found in carnivores in captivity, which is possibly associated with its short life cycle, and may be easily concluded in captivity compared with other parasites such as Toxocara spp. (Bowman, 2009). In contrast, Physaloptera praeputialis, which is a stomach parasite of mammals of the Carnivora order, especially domestic animals such as cats and dogs (Vicente et al., 1997), was reported for the first time in Tamandua tetradactyla. Other species of Physaloptera, such as P. magnipapilla and P. papillotruncata, have already been described parasitizing Myrmecophaga tridactyla and T. tetradactyla, respectively (Vicente et al., 1997). The occurrence of these parasites commonly described in domestic animals may be associated to their presence close to the wild animal's captivities, as observed in animals raised in the zoo at the Federal University of Mato Grosso.

Moniliformis moniliformis detected in the giant anteater (M. tridactyla) has already been described in humans (Salehabadi et al., 2008), and domestic animals (Asato et al., 1986). The acanthocephalan species usually found in rodents uses an arthropod as the intermediate host (Gadale et al., 1989), so the giant anteaters may act as definitive hosts by consuming infected intermediate hosts (cockroach and ants) during feeding. Also concerning endothermic hosts, the occurrence of Cyrnea semilunaris in Crotophaga ani is described for the first time. Metathelazia sp. has already been described in Puma concolor (Vicente et al., 1997), but its occurrence in Herpailurus yagouarandi is herein described for the first time

The occurrence of endoparasites was mostly observed in endothermic animals (79%). Esch et al. (1990) highlighted that the parasite communities of endothermic animals are higher due to greater movement and digestive complexity in these species, and to greater exposure to parasites with direct cycle and active penetration in ectothermic hosts.

Regarding the ectothermic animals, the genus Physaloptera is commonly observed parasitizing the stomach of their definitive hosts, which includes the Liophis miliaris snake as described by Vicente et al. (1993). However, this is the first occurrence of Physaloptera liophis in Eunectes murinus. Pentastomid species of the family Sebekidae are known to parasite fishes, using turtles and caimans as definitive hosts (Riley, 1986). Brito et al. (2012) have described the parasitism of Sebekia oxycephala in lung, stomach and intestine of Cayman yacare, but there are no records of this Pentastomid species in Pantanal snakes, such as Boa constrictor and Eunectes murinus as observed.

Our study contributes to knowledge of parasites in wild animals from Amazon, Pantanal, and Cerrado due to the importance of these biomes, its biodiversity and the increasing anthropic action and possible changes in the dynamics of transmission of helminths in wildlife, especially considering the scarce information about these relationships evidenced by the new host occurrences of parasites herein described. Finally, the occurrence of helminths in animals at risk of extinction showed how the knowledge of wild parasitism, so important for the management and conservation of species, needs to be increased and developed.

ACKNOWLEDGMENTS

To the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the financial support; to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the scholarships of D. M. Aguiar, and R.C. Pacheco; Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT); Laboratório de Patologia Veterinária (LPV)-UFMT.

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Received: February 09, 2015; Accepted: January 04, 2016

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