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Occurrence of potential wild hosts of Echinococcus vogeli in the forests of southwestern Brazilian Amazonia

Ocorrência de potenciais hospedeiros silvestres de Echinococcus vogeli nas florestas do sudoeste da Amazônia brasileira

Abstract

The helminth Echinococcus vogeliRausch & Bernstein, 1972RAUSCH, R.L.& BERNSTEIN, J.J. 1972. Echinococcus vogeli sp. n. (Cestoda: Taeniidae) from the bush dog, Speothos venaticus (Lund). Z. Tropenmed Parasit. 23:25–34. is a causative agent of Neotropical Echinococcosis, a chronic zoonotic disease which is endemic to the Neotropical region. This parasite is transmitted from bush dogs (Speothos venaticus) to their prey, which include lowland pacas (Cuniculus paca) and agoutis (Dasyprocta spp.). In Brazil, most human cases of Neotropical Echinococcosis have been recorded in the Amazonian states of Acre and Pará, although few data are available on the occurrence of the potential definitive or intermediate hosts of E. vogeli in the Amazon region. In the present study, we surveyed the forests surrounding 46 human communities located within and around of outside six sustainable-use protected areas in the southwestern Amazon basin of Brazil. The forests were surveyed using camera traps to determine the local presence of potential wild hosts of E. vogeli, and the exploitation of these hosts for game meat was evaluated through interviews with 136 subsistence hunters resident in the local communities. We recorded pacas, agoutis, and bush dogs, as well as domestic dogs (Canis familiaris), all potential reservoirs of Neotropical Echinococcosis, using the same habitats. We also confirmed the frequent consumption of paca and agouti meat by subsistence hunters and their families in the study communities. Our data contribute to the understanding of the occurrence of E. vogeli in Brazilian ecosystems.

Keywords
Neotropical echinococcosis; subsistence hunting; Brazilian Amazonia; camera trap

Resumo

O helminto Echinococcus vogeliRausch & Bernstein, 1972RAUSCH, R.L.& BERNSTEIN, J.J. 1972. Echinococcus vogeli sp. n. (Cestoda: Taeniidae) from the bush dog, Speothos venaticus (Lund). Z. Tropenmed Parasit. 23:25–34. é o agente causador da Equinococose Neotropical, uma doença zoonótica crônica e endêmica da região Neotropical. Este parasito é transmitido entre o cachorro-vinagre (Speothos venaticus) e suas presas, como pacas (Cuniculus paca) e cutias (Dasyprocta spp.). No Brasil, a maioria dos casos humanos de Equinococose Neotropical é registrada nos estados do Acre e Pará, embora existam poucos dados disponíveis sobre a ocorrência de potenciais hospedeiros definitivos e intermediários de E. vogeli na Amazônia. No presente estudo, foram investigadas áreas de floresta ao redor de 46 comunidades humanas localizadas no interior e entorno de seis unidades de conservação de uso sustentável no sudoeste da bacia amazônica brasileira e, por meio de armadilhas fotográficas, foram avaliadas as presenças de potenciais hospedeiros silvestres de E. vogeli. Adicionalmente, foram avaliados o padrão de consumo da carne dos hospedeiros silvestres por meio de entrevistas com 136 moradores dessas comunidades. Foram registradas pacas, cutias e cachorros-vinagre, bem como cães domésticos (Canis familiaris) utilizando os mesmos habitats, todos potenciais reservatórios da Equinococose Neotropical. Além disto, confirmamos a alto consumo de paca e cutia nas comunidades. Os dados do presente trabalho contribuem para pesquisas em andamento sobre a presença dos potenciais reservatórios de E. vogeli em ambientes brasileiros.

Palavras-chave
equinococose neotropical; caça de subsistência; Amazônia brasileira; armadilha fotográfica

Introduction

Infectious diseases with zoonotic potential are a research priority, given their potential impacts on public health, livestock, and wildlife conservation (Cleaveland et al. 2001CLEAVELAND, S., LAURENSON, M.K., TAYLOR, L.H. 2001. Diseases of humans and their domestic mammals: Pathogen characteristics, host range and the risk of emergence. Philos. Trans. R. Soc. Lond. B. Bio. Sci. 356:991–999.). Worldwide, zoonotic diseases are the leading cause (61%) of human infections (Cunningham 2005CUNNINGHAM, A.A. 2005. A walk on the wild side—emerging wildlife diseases. BMJ. 331(7527): 1214–1215.), and 70% of emerging infectious diseases originate from wildlife, in particular mammals (Cleaveland et al. 2001CLEAVELAND, S., LAURENSON, M.K., TAYLOR, L.H. 2001. Diseases of humans and their domestic mammals: Pathogen characteristics, host range and the risk of emergence. Philos. Trans. R. Soc. Lond. B. Bio. Sci. 356:991–999., Thompson et al. 2009THOMPSON, R.C.A., KUTZ, S.J., SMITH, A. 2009. Parasite zoonoses and wildlife: Emerging issues. Int. J. Environ. Res. Public Health 6:678–693., Johnson et al. 2015JOHNSON, P.T.J., DE ROODE, J.C., FENTON, A. 2015. Why infectious disease research needs community ecology? Science. 349:1259504–1259504.). Many of the helminths that infect humans are zoonotic pathogens with wild and domestic animal hosts (Carmena & Cardona 2014CARMENA, D. & CARDONA, G.A. 2014. Echinococcosis in wild carnivorous species: Epidemiology, genotypic diversity, and implications for veterinary public health. Vet. Parasitol. 202:69–94., Gordon et al. 2016GORDON, C.A., MCMANUS, D.P., JONES, M.K., GRAY, D.J., GOBERT, G.N. 2016. The Increase of Exotic Zoonotic Helminth Infections: The Impact of Urbanization, Climate Change and Globalization. Advan. Parasitol. 91:311–97., Otranto & Deplazes 2019OTRANTO, D. & DEPLAZES, P. 2019. Zoonotic nematodes of wild carnivores. Int. J. Parasitol. Parasites Wildl 9:370–383.). Wild mammals, such as carnivores and rodents, may often host a considerable diversity of zoonotic helminths (Cleaveland et al. 2001CLEAVELAND, S., LAURENSON, M.K., TAYLOR, L.H. 2001. Diseases of humans and their domestic mammals: Pathogen characteristics, host range and the risk of emergence. Philos. Trans. R. Soc. Lond. B. Bio. Sci. 356:991–999., Han et al. 2016HAN, B., KRAMER, A., DRAKE, J. 2016. Global patterns of zoological disease in mammals. Trends Parasitol. 32:565–577.).

Echinococcosis is a helminthic zoonotic infection caused by the larval stage of the tapeworms of the genus Echinococcus Rudolphi, 1801, which have a worldwide distribution. This zoonotic disease is clinically important and considered the most prevalent of the zoonotic helminthiases, which causes serious human morbidity and death, affecting not only humans, but also livestock and wildlife, with implications for the conservation of wild mammal populations (Jenkins et al. 2005JENKINS, D.J., ROMIG, T., THOMPSON, R.C.A. 2005. Emergence/re-emergence of Echinococcus spp. – A global update. Int. J. Parasitol. 35:1205–1219., Thompson et al. 2009THOMPSON, R.C.A., KUTZ, S.J., SMITH, A. 2009. Parasite zoonoses and wildlife: Emerging issues. Int. J. Environ. Res. Public Health 6:678–693., Gordon et al. 2016GORDON, C.A., MCMANUS, D.P., JONES, M.K., GRAY, D.J., GOBERT, G.N. 2016. The Increase of Exotic Zoonotic Helminth Infections: The Impact of Urbanization, Climate Change and Globalization. Advan. Parasitol. 91:311–97.). Echinococcosis can be transmitted through a variety of domestic, synanthropic, and sylvatic cycles, with wild animals being considered a major source of infection in humans (Carmena & Cardona 2014CARMENA, D. & CARDONA, G.A. 2014. Echinococcosis in wild carnivorous species: Epidemiology, genotypic diversity, and implications for veterinary public health. Vet. Parasitol. 202:69–94.). In a recent molecular study, Vuitton et al. (2020)VUITTON, D.A., MCMANUS, D.P., ROGAN, M.T., ROMIG, T., GOTTSTEIN, B., NAIDICH, A., et al. 2020. World Association of Echinococcosis. International consensus on terminology to be used in the field of echinococcoses. Parasite. 27:1–41. validated four Echinococcus species of public health interest: Echinococcus granulosus (Batsch, 1786) sensu lato (s.l.), which causes cystic echinococcosis; Echinococcus multilocularis Leuckart, 1863, causing alveolar echinococcosis; and Echinococcus vogeliRausch & Bernstein, 1972RAUSCH, R.L.& BERNSTEIN, J.J. 1972. Echinococcus vogeli sp. n. (Cestoda: Taeniidae) from the bush dog, Speothos venaticus (Lund). Z. Tropenmed Parasit. 23:25–34. and Echinococcus oligarthra Diesing, 1863, which cause neotropical echinococcosis. Only three of these species occur in Brazil (E. granulosus, E. vogeli and E. oligarthra), however, only two are prevalent: Echinococcus granulosus which is found in southern Brazil and causes cystic echinococcosis, and Echinococcus vogeli, which occurs in northern Brazil, and causes neotropical echinococcosis (Siqueira et al. 2013SIQUEIRA, N.G., DE SIQUEIRA, C.M.V.M., RODRIGUES-SILVA, R., SOARES, M. DO C.P., PÓVOA, M.M. 2013. Polycystic echinococcosis in the state of Acre, Brazil: Contribution to patient diagnosis, treatment and prognosis. Mem. Inst. Oswaldo Cruz 108:533–540.) (Figure 1).

Figure 1.
Map of Brazil showing endemic areas for Echinococcus vogeli and Echinococcus granulosus (s.l.).

Echinococcus vogeli is endemic to the Neotropical region, where its definitive host is the bush dog (Speothos venaticus Lund, 1842), and the principal intermediate host is the lowland paca (Cuniculus paca Linnaeus, 1766), which is the preferred prey of bush dog (D’Alessandro et al. 1981D’ALESSANDRO, A., RAUSCH, R.L., MORALES, G.A., COLLET, S., ANGEL, D. 1981. Echinococcus infections in Colombian animals. Am. J. Trop. Med. Hyg. 30:1263–1276. , D’Alessandro 1997D’ALESSANDRO, A. 1997. Polycystic echinococcosis in tropical America: Echinococcus vogeli and E. oligarthrus. Acta Trop. 67:43–65., D’Alessandro & Rausch 2008D’ALESSANDRO, A. & RAUSCH, R.L. 2008. New aspects of Neotropical polycystic (Echinococcus vogeli) and unicystic (Echinococcus oligarthrus) echinococcosis. Clin. Microbiol. Rev. 21:380–401.). Other wild animals are known to act as hosts of E. vogeli in Brazil, including the agouti (Dasyprocta leporina Linnaeus, 1758), and the nine-banded armadillo (Dasypus novemcinctus Linnaeus, 1758 (Santos et al. 2012SANTOS, G.B., SOARES, M.C.P., ELISABETE, E.M., RODRIGUES, A.L., SIQUEIRA, N.G., GOMES-GOUVEA, M.S., ALVES, M.M., CARNEIRO, L.A., MALHEIROS, A.P., PÓVOA, M.M., ZAHA, A., HAAG, K.L. 2012. Mitochondrial and nuclear sequence polymorphisms reveal geographic structuring in Amazonian populations of Echinococcus vogeli (Cestoda: Taeniidae). Inter. J. Parasitol. 2:1115–1118., Almeida et al. 2013ALMEIDA, F., CALDAS, R., CORRÊA, C., RODRIGUES-SILVA, R., SIQUEIRA, N., MACHADO-SILVA, J.R. 2013. Co-infections of the cestode Echinococcus vogeli and the nematode Calodium hepaticum in the hystricomorphic rodent Agouti paca from a forest reserve in Acre, Brazil. J. Helminthol. 87:489–493., Soares et al. 2014SOARES, M.C.P., SOUZA DE SOUZA, A.J., PINHEIRO MALHEIROS, A., MARCELIANO NUNES, H., ALMEIDA CARNEIRO, L., MOREIRA ALVES, M., DA CONCEIÇÃO, B.F., GOMES-GOUVEA, M.S., POVOA, M.M. 2014. Neotropical echinococcosis: Second report of Echinococcus vogeli natural infection in its main definitive host, the bush dog (Speothos venaticus). Parasitol. Int. 63:485–487.). In addition to the natural cycle of the parasite in these animals, E. vogeli may circulate in a partially synanthropic cycle, in particular, through the hunting and consumption of the meat of wild paca (an intermediate host of E. vogeli), and the introduction of domestic hunting dogs (Canis familiaris), which may feed on infected paca tissue (Eckert & Deplazes 2004ECKERT, J. & DEPLAZES, P. 2004. Biological, Epidemiological, and Clinical Aspects of Echinococcosis, a Zoonosis of Increasing Concern. Clin. Microbiol. Rev. 17:107–135., D’Alessandro & Rausch 2008D’ALESSANDRO, A. & RAUSCH, R.L. 2008. New aspects of Neotropical polycystic (Echinococcus vogeli) and unicystic (Echinococcus oligarthrus) echinococcosis. Clin. Microbiol. Rev. 21:380–401.).

The subsistence hunting of wild mammals is common and widespread in the rural and indigenous communities of the Amazon region (Peres & Palacios 2007PERES, C.A. & PALACIOS, E. 2007. Basin-wide effects of game harvest on vertebrate population densities in Amazonian forests: implications for animal-mediated seed dispersal. Biotropica 39: 304–315.), which paca and agouti are important game species to rural communities in central-western portion of Brazilian Amazon (Sampaio et al. 2022SAMPAIO, R., MORATO, R.G., ABRAHAMS, M.I., PERES, C.A., CHIARELLO, A. G. 2022. Physical geography trumps legal protection in driving the perceived sustainability of game hunting in Amazonian local communities. J. Nat. Conserv. 67: 126175.) and dogs are widely used for hunting (Bittencourt-Oliveira et al. 2018BITTENCOURT-OLIVEIRA, F., TEIXEIRA, P., ALENCAR, A., MENEZES, R., CORRÊA, C., NEVES, L., ALMEIDA, F., DAIPERT-GARCIA, D., MACHADO-SILVA, J.R., RODRIGUES-SILVA, R. 2018. First parasitological, histopathological and molecular characterization of Echinococcus vogeli Rausch and Bernstein, 1972 from Cuniculus paca Linnaeus, 1766 in the Cerrado biome (Mato Grosso do Sul, Brazil). Vet. Parasitol. 250:35–39., Guimarães et al. 2019). Humans are considered to be an accidental intermediate host of E. vogeli (Rausch & Bernstein 1972RAUSCH, R.L.& BERNSTEIN, J.J. 1972. Echinococcus vogeli sp. n. (Cestoda: Taeniidae) from the bush dog, Speothos venaticus (Lund). Z. Tropenmed Parasit. 23:25–34.) – they are infected through the accidental ingestion of eggs present in the feces of domestic dogs (Eckert & Thompson 2017ECKERT, J. & THOMPSON, R.C.A. 2017. Historical Aspects of Echinococcosis. Adv. Parasitol. 95:1–64.).

In Brazil, most human cases of neotropical echinococcosis have been reported from the Amazonian states of Acre and Pará (Siqueira et al. 2013SIQUEIRA, N.G., DE SIQUEIRA, C.M.V.M., RODRIGUES-SILVA, R., SOARES, M. DO C.P., PÓVOA, M.M. 2013. Polycystic echinococcosis in the state of Acre, Brazil: Contribution to patient diagnosis, treatment and prognosis. Mem. Inst. Oswaldo Cruz 108:533–540.). In Acre, infection by E. vogeli has also been reported in both the paca (Meneghelli et al. 1992MENEGHELLI, U.G., MARTINELLI, A.L., LLORACH-VELLUDO, M.A., BELLUCCI, A.D., MAGRO, J.E., BARBO, M.L. 1992. Polycystic hydatid disease (Echinococcus vogeli): clinical, laboratory and morphological findings in nine Brazilian patients. J. Hepatol. 14:203–210., Almeida et al. 2013ALMEIDA, F., CALDAS, R., CORRÊA, C., RODRIGUES-SILVA, R., SIQUEIRA, N., MACHADO-SILVA, J.R. 2013. Co-infections of the cestode Echinococcus vogeli and the nematode Calodium hepaticum in the hystricomorphic rodent Agouti paca from a forest reserve in Acre, Brazil. J. Helminthol. 87:489–493., Oliveira 2016OLIVEIRA, FB 2016. Alterações histopatológicas e identificação de helmintos por meio de análises parasitológicas e/ou moleculares em fígados de pacas (Cuniculus paca) oriundas do Acre e Mato Grosso do Sul, Brasil. Dissertação de Mestrado, Instituto Oswaldo Cruz, Rio de Janeiro.) and domestic dogs (Neves et al. 2017NEVES, L.B., TEIXEIRA, P.E.F., SILVA, S., DE OLIVEIRA, F.B., GARCIA, D.D., DE ALMEIDA, F.B., RODRIGUES-SILVA, R., MACHADOSILVA, J.R. 2017. First molecular identification of Echinococcus vogeli and Echinococcus granulosus (sensu stricto) G1 revealed in feces of domestic dogs (Canis familiaris) from Acre, Brazil. Parasit. Vectors 10:1–6.), which indicates the occurrence of both sylvatic and domestic cycles in this region. Despite these findings, relatively few data are available on the occurrence of the potential hosts of E. vogeli, whether definitive or intermediate, in most areas of Brazilian Amazonia.

In the present study, we used camera traps to survey forests in the vicinity of 46 human villages located within and immediately outside of six sustainable-use protected areas in the southwestern Brazilian Amazon in order to investigate the local occurrence of potential wild hosts of E. vogeli, that may maintain the wild cycle of this parasite in the region. Through interviews with 136 local hunters, we also evaluated the frequency of the consumption of the meat of these mammals of the local communities.

Material and Methods

1. Study area

The study was carried out in and around six sustainable-use protected areas located in southwestern Brazilian Amazonia in 2018, 2019, and 2020 (Figure 2). Four of these protected areas, the Cazumbá-Iracema Extractive Reserve (CIR), the Riozinho da Liberdade Extractive Reserve (RLR), the Liberdade State Forest (LF), and the Mogno State Forest (MF), hereafter Liberdade Reserves (LR), all protect areas above are located in the Brazilian state of Acre, while the other two – the Arapixi Extractive Reserve (AR) and the Médio Purus Extractive Reserve (MPR) – are located in Amazonas state. The families residing in the local communities live on plots of 300–500 ha, with a mean of four members per household, which are distributed along rivers, streams, and roads. The financial income of these families is derived from cattle ranching and farming (manioc, corn, and rice), as well as rubber tapping and the harvesting of Brazil nut from the forest (Oliveira & Calouro 2020OLIVEIRA, M.A. & CALOURO, A.M. 2020. Medium-sized and large mammals of the Cazumbá-Iracema Extractivist Reserve, Acre, Brazil. Check List 16:127–136.). Subsistence is based on livestock, agricultural produce, forest resources, fishing, and hunting (Tourinho et al. 2013TOURINHO, M.M., ALEIDA, D., SAYAGO, V. 2013. Uso de recursos naturais por comunidades ribeirinhas amazônicas: bases para as políticas de concessões florestais. Novos Cadernos NAEA 16:79–100., Souza et al. 2021SOUZA, L.S., PROGÊNIO, M., DE SOUZA, L.S., SANTOS, F.G.A. 2021. Consumption of wild animals in extractive communities in the State of Acre, Brazilian Amazon. Biota Amazôn. 11:7–30.).

Figure 2.
Location of the three study areas (panels A–C) within lowland Amazonia (green portion of the upper left panel), South America. (A) Cazumbá-Iracema Extractive Reserve (CIR) and Arapixi Extractive Reserve (AR); (B) Riozinho da Liberdade Extractive Reserve (RLR), Liberdade State Forest (LF) and Mogno State Forest (MF); and (C) Médio Purus Extractive Reserve (MPR). The maps show the 46 study communities (white dots), 452 camera traps (blue dots), the nearest urban centers (red dots), and the shapes of the protected areas (orange polygons).

2. Data collection and analysis

The study areas were surveyed using unbaited Bushnell® digital camera traps, which are cameras triggered remotely by heat and motion. We used these devices to record the presence of potential wild mammalian reservoirs of polycystic echinococcosis during two distinct phases of sampling. A total of 452 camera traps were installed in the vicinity of 46 human communities in continuous primary terra firme forest. The total sampling effort was 21,909 trap-days, with each individual camera being operational for between half a day and 62 days (mean ± SD = 49.3±9 days).

The camera traps were deployed only in areas of primary forest found in the vicinity of each community, being distributed along a logarithmic gradient of distances of between 220 m and 7 km from the nearest community. The traps were affixed to tree trunks approximately 30–45 cm above the ground and programmed to operate continuously for 24 hours per day. Once triggered, each camera took photographs at 10-second intervals until no further movement was detected, with the following information being logged for each photograph: the date, time, season, and species (Srbek-Araujo & Chiarello 2013SRBEK-ARAUJO, A.C. & CHIARELLO, A.G. 2013. Influência do desenho amostral na taxa de captura e na estrutura da comunidade de mamíferos registrada a partir de armadilhas fotográficas no sudeste do Brasil. Biota Neotrop. 13:51–62.). The photographs were uploaded to the Camera Base (https://www.atrium-biodiversity.org/tools/camerabase/) and Wild.id (https://github.com/ConservationInternational/Wild.ID) databases for processing.

We calculated the frequency of sightings of each host species based on the number of photographs of a given species obtained by the same camera trap at an interval of at least one hour. These photographs were considered to be independent records of occurrence, following the recapture protocol of Srbek-Araujo & Chiarello (2013)SRBEK-ARAUJO, A.C. & CHIARELLO, A.G. 2013. Influência do desenho amostral na taxa de captura e na estrutura da comunidade de mamíferos registrada a partir de armadilhas fotográficas no sudeste do Brasil. Biota Neotrop. 13:51–62.. We calculated the Relative Abundance (RA) of each species, where RA = the number of records of the species/the number of trap-days × 100) following Springer et al. (2012)SPRINGER, M.T., CARVER, A.D., NIELSEN, C.K., CORREA, N.J., ASHMORE, J.R., ASHMORE, J.R., LEE, J.G. 2012. Relative abundance of mammalian species in a central Panamanian rainforest. Latin. Am. J. Conservation 3:19–26. and O’Brien (2010)O’BRIEN, T.G. 2010. Wildlife picture index: implementation manual version. Wildlife Conserv. Soc. Working Papers 39:1285–129..

After obtaining explicit consent from all the participating communities and informants, we interviewed experienced subsistence hunters, who were willing informants and had been indicated to us based on a community-level snowball approach. A semi-structured questionnaire was applied to determine how often each hunter consumed the meat of the paca and agouti (reservoirs of E. vogeli). The study was approved by the Ethics Committee of the University of São Paulo (process number 2296078) and by the Brazilian Federal System of Biodiversity Information and Authorisation (SISBIO), through license number 68985-1.

Results

Based on a total sampling effort of 21,909 trap-days, we obtained 4,334 independent records of potential E. vogeli reservoirs (Table 1). We recorded the agouti (Figure 3a) in 44 (96%) of the communities surveyed, with detection distances in relation to the nearest community ranging from 293.6 to 7,316.6 meters (mean±SD = 3,135.4±1,650.5 m). This species was recorded most frequently in the early morning (between 6:27 am and 9:00 am) and around sunset (5:00 pm). We recorded the paca (Figure 3b) in 45 (98%) communities, at distances of between 293.6 and 7316.6 meters (mean = 3172.9 ± 1732.1 m), with the highest frequency of records being recorded between 7:00 pm and 11:00 pm.

Table 1.
Number of camera trap records (N) and the Relative Abundance (RA) of the four potential wild and domestic hosts of Echinococcus vogeli recorded in the communities located in and around the sustainable-use protected areas in the southwestern Brazilian Amazon basin.
Figure 3.
Potential wild and domestic hosts of Echinococcus vogeli captured by the camera traps deployed in the study region in the southwestern Amazon basin of Brazil (see Figure 2): (A) Dasyprocta ssp., (B) Cuniculus paca, (C) Speothos venaticus, and (D) Canis familiaris.

We recorded the bush dog (Figure 3c) in only nine (20%) communities, where the photographs were obtained in the mid-morning, between 9:23 am and 12:32 pm, at distances of between 495.0 and 5,923.7 meters from the nearest community (mean = 3,538.6±1,683.4 m). Records of this species were more frequent in the communities in which pacas and agoutis were more abundant. Domestic dogs (Figure 3d) were recorded moving along the trails in the forests located in the vicinity of 30 (65%) communities, at distances of between 439.7 and 6,507.4 meters from the local community (mean = 2,509.4±1,604.8 m).

We interviewed 136 subsistence hunters resident in all the different communities of the study region. Most of the interviewees in all the communities indicated that they consume paca (71.3% − n = 96) and agouti (33.1% − n = 45) meat, with the paca being the species reported most often (Figure 4). All residents also reported that domestic dogs are fed with the raw viscera of these animals.

Figure 4.
Frequency of the reports of the consumption of paca and agouti meat by the 136 subsistence hunters interviewed in the rural communities surveyed in the southwestern Amazon basin of Brazil (see Figure 2).

Discussion

The present study investigated the local occurrence of three wild mammals (the agouti, paca, and bush dog) and the domestic dog in the vicinity of 46 rural communities located both within and adjacent to six sustainable-use protected areas in southwestern Brazilian Amazonia. All these species are potentially important hosts of Neotropical echinococcosis, which is caused by E. vogeli, and are often found in areas close to human settlements, which are used as communal hunting grounds. Subsistence hunting is the only known route for the establishment of the domestic cycle of E. vogeli (Meneghelli et al. 1992MENEGHELLI, U.G., MARTINELLI, A.L., LLORACH-VELLUDO, M.A., BELLUCCI, A.D., MAGRO, J.E., BARBO, M.L. 1992. Polycystic hydatid disease (Echinococcus vogeli): clinical, laboratory and morphological findings in nine Brazilian patients. J. Hepatol. 14:203–210., D’Alessandro et al. 2008D’ALESSANDRO, A. & RAUSCH, R.L. 2008. New aspects of Neotropical polycystic (Echinococcus vogeli) and unicystic (Echinococcus oligarthrus) echinococcosis. Clin. Microbiol. Rev. 21:380–401., Almeida et al. 2013ALMEIDA, F., CALDAS, R., CORRÊA, C., RODRIGUES-SILVA, R., SIQUEIRA, N., MACHADO-SILVA, J.R. 2013. Co-infections of the cestode Echinococcus vogeli and the nematode Calodium hepaticum in the hystricomorphic rodent Agouti paca from a forest reserve in Acre, Brazil. J. Helminthol. 87:489–493.). This occurs through contact with the domestic dogs that accompany the hunts and are often fed raw game meat, which may sometimes be infected with E. vogeli (Siqueira et al. 2013SIQUEIRA, N.G., DE SIQUEIRA, C.M.V.M., RODRIGUES-SILVA, R., SOARES, M. DO C.P., PÓVOA, M.M. 2013. Polycystic echinococcosis in the state of Acre, Brazil: Contribution to patient diagnosis, treatment and prognosis. Mem. Inst. Oswaldo Cruz 108:533–540., Bittencourt-Oliveira et al. 2018BITTENCOURT-OLIVEIRA, F., TEIXEIRA, P., ALENCAR, A., MENEZES, R., CORRÊA, C., NEVES, L., ALMEIDA, F., DAIPERT-GARCIA, D., MACHADO-SILVA, J.R., RODRIGUES-SILVA, R. 2018. First parasitological, histopathological and molecular characterization of Echinococcus vogeli Rausch and Bernstein, 1972 from Cuniculus paca Linnaeus, 1766 in the Cerrado biome (Mato Grosso do Sul, Brazil). Vet. Parasitol. 250:35–39.).

The bush dog is a rare species in the wild, and our records are new for its range in the Amazon basin (Michalski 2010MICHALSKI, F. 2010. The bush dog Speothos venaticus and short-eared dog Atelocynus microtis in a fragmented landscape in southern Amazonia. Oryx 44:300–303., Rocha 2015ROCHA, D.G., RAMALHO, E.E., ALVARENGA, G.C., GRÄBIN, D.M., MAGNUSSON, W.E. 2015. Records of the bush dog (Speothos venaticus) in Central Amazonia, Brazil. J. Mammal. 96:1361–1364., Oliveira et al. 2018OLIVEIRA, T.G., MICHALSKI, F., BOTELHO, A.L.M., MICHALSKI, L.J., CALOURO, A.M., DESBIEZ, A.L.J. 2018. How rare is rare? Quantifying and assessing the rarity of the bush dog Speothos venaticus across the Amazon and other biomes. Oryx 52:98–107.), and possibly also the occurrence of E. vogeli in these areas. Oliveira & Calouro (2019)OLIVEIRA, M.Á.& CALOURO, A.M. 2019. Hunting agreements as a strategy for the conservation of species: The case of the cazumbÁ-iracema extractive reserve, state of acre, brazil. Oecologia Aust. 23:357–366. recently surveyed medium- and large-bodied mammals in the Cazumbá-Iracema Extractive Reserve through both direct observations (e.g. camera trapping, sightings, and the collection of vestiges and osteological material) and indirect records, such as interviews. While these authors reported the presence of the paca, agouti, and bush dog in this protected area, only the paca and agouti were recorded directly, with the bush dog only being reported by the local residents. The results of the present study confirm the findings of Oliveira & Calouro (2019)OLIVEIRA, M.Á.& CALOURO, A.M. 2019. Hunting agreements as a strategy for the conservation of species: The case of the cazumbÁ-iracema extractive reserve, state of acre, brazil. Oecologia Aust. 23:357–366., including the presence of the bush dog, which was recorded by the camera traps.

The first record of E. vogeli in a wild canid was from a bush dog captured in late 1969 in the province of Esmeraldas, Ecuador (Rausch and Bernstein 1972RAUSCH, R.L.& BERNSTEIN, J.J. 1972. Echinococcus vogeli sp. n. (Cestoda: Taeniidae) from the bush dog, Speothos venaticus (Lund). Z. Tropenmed Parasit. 23:25–34.), while the second was from the municipality of Anajás, in the Brazilian state of Pará (Soares et al. 2014SOARES, M.C.P., SOUZA DE SOUZA, A.J., PINHEIRO MALHEIROS, A., MARCELIANO NUNES, H., ALMEIDA CARNEIRO, L., MOREIRA ALVES, M., DA CONCEIÇÃO, B.F., GOMES-GOUVEA, M.S., POVOA, M.M. 2014. Neotropical echinococcosis: Second report of Echinococcus vogeli natural infection in its main definitive host, the bush dog (Speothos venaticus). Parasitol. Int. 63:485–487.). Both these reports highlight the importance of the bush dog as a definitive host, which may maintain the natural cycle of the parasite in different regions of northern South America, in particular in the Brazilian Amazon biome.

Domestic dogs may play a crucial role in the transmission of E. vogeli eggs to humans, and the present study recorded these animals in all the habitats in which the wild mammals were recorded. Using molecular markers, Neves et al. (2017)NEVES, L.B., TEIXEIRA, P.E.F., SILVA, S., DE OLIVEIRA, F.B., GARCIA, D.D., DE ALMEIDA, F.B., RODRIGUES-SILVA, R., MACHADOSILVA, J.R. 2017. First molecular identification of Echinococcus vogeli and Echinococcus granulosus (sensu stricto) G1 revealed in feces of domestic dogs (Canis familiaris) from Acre, Brazil. Parasit. Vectors 10:1–6. identified E. vogeli eggs in fecal samples collected from domestic dogs in Sena Madureira (Acre state), which further highlights the potential role of dogs as a source of infection for humans, thereby establishing and maintaining the domestic cycle.

The first report of the presence of E. vogeli in pacas in the state of Acre dates to 1989 (Meneghelli et al. 1992MENEGHELLI, U.G., MARTINELLI, A.L., LLORACH-VELLUDO, M.A., BELLUCCI, A.D., MAGRO, J.E., BARBO, M.L. 1992. Polycystic hydatid disease (Echinococcus vogeli): clinical, laboratory and morphological findings in nine Brazilian patients. J. Hepatol. 14:203–210.), although no records are available for the state of Amazonas. Our findings show that the known hosts of E. vogeli are common in the study region, providing the conditions necessary to maintain its parasitic cycle in this region. Reports of infection by E. vogeli in agoutis (Dasyprocta spp.) are rare overall, with only one record from Brazil, in the state of Pará, in the eastern extreme of the Amazon region (Soares et al. 1999SOARES, M.C.P., CRUZ, E.R.M., CARTÁGENES, P.R.B., ALVES, M. M., BENSABATH, G. 1999. Hidatidose policística e cisticercose em fígado e baço de cutias (Dasyprocta aguti) da Ilha de Marajó, Pará, Brasil. Rev. Soc. Bras. Med. Trop. 32:317.). There are no other published records of the infection of agouti by E. vogeli in the Amazon region.

Most human cases of neotropical echinococcosis recorded in Brazil come from the Amazon region, where the disease is commonly known as “Paca Disease” (D’Alessandro & Rausch 2008D’ALESSANDRO, A. & RAUSCH, R.L. 2008. New aspects of Neotropical polycystic (Echinococcus vogeli) and unicystic (Echinococcus oligarthrus) echinococcosis. Clin. Microbiol. Rev. 21:380–401., Daipert-Garcia et al. 2019DAIPERT-GARCIA, D., PAVAN, M.G., DAS NEVES, L.B.; DE ALMEIDA, F.B., SIQUEIRA, N.G., DOS SANTOS, G.B., DIAS-CORREIA, T.P., FERREIRA, H.B., RODRIGUES-SILVA, R. 2019. Genetic diversity of Echinococcus vogeli in the western Brazilian Amazon. Mem. Inst. Oswaldo Cruz 114:11–14.). In the state of Amazonas, six cases of the disease were reported (Guimarães et al. 2005GUIMARÃES, L.S.C., CHALUB, S.R.S., DUARTE, E.L., MAIA, M.V., JAIME, M.V. 2005. Cisto hidático – Relato de dois casos no Amazonas. Ver. Col. Bras. Cir. 32:S384.; Siqueira et al. 2013SIQUEIRA, N.G., DE SIQUEIRA, C.M.V.M., RODRIGUES-SILVA, R., SOARES, M. DO C.P., PÓVOA, M.M. 2013. Polycystic echinococcosis in the state of Acre, Brazil: Contribution to patient diagnosis, treatment and prognosis. Mem. Inst. Oswaldo Cruz 108:533–540.). In the state of Acre, many human cases have been recorded since 1992 (Meneghelli et al. 1992MENEGHELLI, U.G., MARTINELLI, A.L., LLORACH-VELLUDO, M.A., BELLUCCI, A.D., MAGRO, J.E., BARBO, M.L. 1992. Polycystic hydatid disease (Echinococcus vogeli): clinical, laboratory and morphological findings in nine Brazilian patients. J. Hepatol. 14:203–210., Daipert-Garcia et al. 2019DAIPERT-GARCIA, D., PAVAN, M.G., DAS NEVES, L.B.; DE ALMEIDA, F.B., SIQUEIRA, N.G., DOS SANTOS, G.B., DIAS-CORREIA, T.P., FERREIRA, H.B., RODRIGUES-SILVA, R. 2019. Genetic diversity of Echinococcus vogeli in the western Brazilian Amazon. Mem. Inst. Oswaldo Cruz 114:11–14.), which reflects the continuity of the parasitic cycle of the disease in the Amazon region. Three studies estimated the prevalence of infection in Acre based on serum antibody levels. In the first study, Pastore et al. (2003)PASTORE, R., VITALI, L.H., OLIVEIRA, M.V., PRATA, A. 2003. A serological survey of the infection by Echinococcus sp. in the municipality of Sena Madureira, AC. Rev Soc Bras Med Trop. 36:473–7. recorded a frequency of 4% in a group of 1064 individuals from the municipality of Sena Madureira, while Pereira (2016) found a frequency of 25% when analyzing 332 samples collected in the municipalities of Sena Madureira, and Bujarí. Souza (2021)SOUZA, L.S., 2021. Estudo sobre o ciclo de transmissão de Echinococcus vogeli em reservatórios silvestres e moradores de comunidades rurais da Amazônia brasileira. Dissertação de Mestrado, Instituto Oswaldo Cruz, Rio de Janeiro. investigated 327 residents of the Cazumbá-Iracema Extractive Reserve, in Sena Madureira, and recorded positive serology in 8.6% of the individuals and hydatid cysts in 10.3%. These studies demonstrated that Neotropical echicoccosis is prevalent within the study area in Acre, where conditions may be favorable for the maintenance of the parasitic cycle.

The present study confirmed the presence of potential hosts of E. vogeli, both definitive and intermediate, within the same habitat in the southwestern Brazilian Amazon basin. This probably guarantees the full life cycle of this parasite through the contamination of the environment by bush dog feces infected with E. vogeli, which may be transferred to pacas and agoutis when they ingest eggs from contaminated soil (D’Alessandro & Rausch 2008D’ALESSANDRO, A. & RAUSCH, R.L. 2008. New aspects of Neotropical polycystic (Echinococcus vogeli) and unicystic (Echinococcus oligarthrus) echinococcosis. Clin. Microbiol. Rev. 21:380–401.). Both these rodents, in turn, are prey for the bush dog, which thus ensures the completion of the parasite’s wild cycle (Lima et al. 2009LIMA, E.S., PINTO JORGE, R.S., DALPONTE, J.C. 2009. Habitat use and diet of bush dogs, Speothos venaticus, in the Northern Pantanal, Mato Grosso, Brazil. Mammalia 73: 13–19., 2012LIMA, E.S., DEMATTEO, K.E., JORGE, R.S.P., JORGE, M.L.S.P., DALPONTE, J.C., LIMA, H.S., KLORFINE, S.A. 2012. First telemetry study of bush dogs: Home range, activity and habitat selection. Wildlife Res. 39: 512–519., Jorge et al. 2013JORGE, R.P.S., BEISIEGEL, B.M., LIMA, E.S., JORGE, M.L.S., LEITEPITMAN, M.R.P., PAULA, R.C. 2013. Avaliação do risco de extinção do cachorro-vinagre Speothos venaticus (Lund, 1842) no Brasil. Bio. Brasil. 3:179–190.), with the parasite being introduced into the domestic environment through intense subsistence hunting, as observed throughout the area of the present study.

Conclusions

The confirmation of the presence of potential wild reservoirs of Neotropical echinococcosis (caused by Echinococcus vogeli) in the study region, together with the frequent consumption of paca and agouti meat by local hunters and their families, indicate the existence of an environment favorable to the maintenance of both the wild and the domestic cycles of this parasite. These findings extend our understanding of the occurrence of the hosts of E. vogeli, which will be fundamental to the development of more systematic research and effective programs for the monitoring and control of this parasitic infection in the Amazon region.

Acknowledgments

We are immensely grateful to the local communities of the Caeté, Macauã, Liberdade, and Purus regions for their support, kind hospitality, and assistance during the fieldwork. We are also grateful to the Amazonas State Center for Conservation Units (CEUC/SDS/AM), the Acre State Division for Natural Protected Areas and Biodiversity (DapBio/SEMA/AC), and the Chico Mendes Institute for the Conservation of Biodiversity (ICMBio/MMA) for authorizations and logistic support during fieldwork. This study was supported by the Brazilian Coordination for Higher Education Personnel Training (CAPES) and the Rio de Janeiro State Research Foundation (FAPERJ) which provided scholarships, as well as the São Paulo State Research Foundation (FAPESP; grant number 2017/08461-8 to RGM), the National Geographic Society (grant number WW-122EC-17 to RS), the American Society of Mammalogists (Latin American Student Field Research Award 2017 to RS), Idea Wild (SAMPBRAZ0216 to RS), and the Amazonian Protected Areas Program of the Brazilian Environment Ministry (ARPA/MMA).

  • Ethics
    The study was approved by the Ethics Committee of the University of São Paulo (process number 2296078) and by the Brazilian Federal System of Biodiversity Information and Authorization (SISBIO), through license number 68985-1.
  • Data Availability
    Supporting data are available at <https://doi.org/10.5281/zenodo.6646839>

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Edited by

Associate Editor
Diego Astúa

Publication Dates

  • Publication in this collection
    30 Sept 2022
  • Date of issue
    2022

History

  • Received
    21 June 2022
  • Accepted
    24 Aug 2022
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