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Helminthfauna of road-killed cougars (Puma concolor) from the Northeastern Region of São Paulo State, Brazil

Helmintofauna de onças pardas atropeladas (Puma concolor) da região Nordeste do Estado de São Paulo, Brasil

Abstract

As the second-largest Neotropical carnivore, cougars (Puma concolor) are especially important for maintenance of the biodiversity and ecosystem health. Five wild adult cougars (Puma concolor), found roadkilled in highways in the Northeastern region of São Paulo, were evaluated in search for parasites. Ten species representing nine families were identified. The most prevalent helminths were Uncinaria bidens, Lagochilascaris major, Spirometra sp., and Oncicola canis, followed by Cylicospirura subaequalis, Toxascaris leonina, Taenia omissa, Echinococcus sp., Filaroides sp. and Oncicola oncicola. It is important to note that some helminths found in this study, such as L. major, Spirometra sp., O. oncicola, O. canis, Echinococcus sp., T. leonina, C. subaequalis, and Filaroides sp. are known to affect domestic carnivores, which may indicate interaction between wild and domestic hosts. This study represents a new host record for four of the species found in cougars, U. bidens, L. major, O. canis, and Filaroides sp., and new locality records for U. bidens, T. leonina, C. subaequalis, and Filaroides sp.

Keywords:
Felidae; Endoparasites; Nematoda; Cestoda; neotropical region; wildlife

Resumo

Como o segundo maior carnívoro neotropical, as onças-pardas são muito importantes para a manutenção da biodiversidade e a saúde do ecossistema. Cinco pumas adultos de vida livre (Puma concolor), mortos em rodovias na região Nordeste de São Paulo, foram avaliados quanto a presença de parasitas. Dez espécies, representando nove famílias foram identificadas. Os helmintos mais prevalentes foram Uncinaria bidens, Lagochilascaris major, Spirometra sp., e Oncicola canis, seguidos por Cylicospirura subaequalis, Toxascaris leonina, Taenia omissa, Echinococcus sp., Filaroides sp. e Oncicola oncicola. É importante salientar que alguns dos helmintos encontrados neste estudo, tais como Lagochilascaris major, Spirometra sp., O. oncicola, Oncicola canis, Echinococcus sp., Toxascaris leonina, Cylicospirura subaequalis, e Filaroides sp., afetam sabidamente carnívoros domésticos, o que pode indicar a interação entre hospedeiros selvagens e domésticos. Este estudo representa novos registros de hospedeiro para quatro espécies de helmintos, sendo elas U. bidens, L. major, O. canis, and Filaroides sp., além de novo registro de localidade para U. bidens, T. leonina, C. subaequalis, e Filaroides sp.

Palavras-Chave:
Felidae; Endoparasitas; Nematoda; Cestoda; região neotropical; vida Selvagem

As the second-largest Neotropical carnivore, cougars (Puma concolor) are especially important for biodiversity maintenance and ecosystem health (Melo et al., 2016Melo LF, Silva DS, Vieira FC, Mello WC. Histórico e perspectiva da conservação dos felinos silvestres ocorrentes no Brasil com estudos realizados entre os anos de 1945 a 2014. Rev Presença 2016; 2(4): 42-57.). These felids occupy extensive home ranges, with low tolerance to overlapping, they are often observed in low population density (Culver, 2010Culver M. Lessons and insights from evolution, taxonomy and conservation genetics. In: Hornocker MG, Sharon N, editors. Cougar: ecology and conservation. Chicago, USA: The University of Chicago Press; 2010; p. 27-40.). Even though, cougars are frequently observed in anthropized areas, as they are tolerant to human presence (Knopf et al., 2014Knopf AA, Knopf KH, Boyce MS, St. Clair CC. Flexible habitat selection by cougars in response to anthropogenic development. Biol Conserv 2014; 178: 136-145. http://dx.doi.org/10.1016/j.biocon.2014.07.017.
http://dx.doi.org/10.1016/j.biocon.2014....
). Human actions, especially agriculture and timber exploitation, wildfires and roadkills, are important factors linked to the reduction of the cougar population in several areas (Azevedo et al., 2013Azevedo FC, Lemos FG, Almeida LB, Campos CB, Beisiegel BM, Paula RC, et al. Avaliação do risco de extinção da Onça-parda Puma concolor (Linnaeus, 1771) no Brasil. Biodivers Bras 2013; 3(1): 107-121.). The Northeastern region of São Paulo State is covered by Cerrado savanna and Atlantic rainforest, both strongly affected by deforestation, resulting in a highly fragmented landscape, composed of some large stretches and several small patches of natural vegetation surrounded by plantations of sugarcane and eucalyptus, cattle farms, and roads and highways (Miotto et al., 2012Miotto RA, Cervini M, Begotti RA, Galetti Junior PM. Monitoring a puma (Puma concolor) population in a fragmented landscape in southeast Brazil. Biotropica 2012; 44(1): 98-104. http://dx.doi.org/10.1111/j.1744-7429.2011.00772.x.
http://dx.doi.org/10.1111/j.1744-7429.20...
).

The helminths parasites of cougars are known from studies developed in USA and a few South American countries (Waid & Pence, 1988Waid DD, Pence DB. Helminths of mountain lions (Felis concolor) from southwestern Texas, with a redescription of Cylicospirura subaequalis (Molin, 1860) Vevers, 1922. Can J Zool 1988; 66(10): 2110-2117. http://dx.doi.org/10.1139/z88-313.
http://dx.doi.org/10.1139/z88-313...
; Rickard & Foreyt, 1992Rickard LG, Foreyt WJ. Gastrointestinal parasites of cougars (Felis concolor) in Washington and the first report of Ollulanus tricuspis in a sylvatic felid from North America. J Wildl Dis 1992; 28(1): 130-133. http://dx.doi.org/10.7589/0090-3558-28.1.130. PMid:1548792.
http://dx.doi.org/10.7589/0090-3558-28.1...
; Noronha et al., 2002Noronha D, Vicente JJ, Pinto RM. A survey of new records for nematodes from mammals deposited in the Helminthological collection of the Oswaldo Cruz Institute (CHIOC). Rev Bras Zool 2002; 19(3): 945-949. http://dx.doi.org/10.1590/S0101-81752002000300032.
http://dx.doi.org/10.1590/S0101-81752002...
; Foster et al., 2006Foster GW, Cunningham MW, Kinsella JM, McLaughlin G, Forrester DJ. Gastrointestinal helminths of free-ranging florida panthers (Puma concolor coryi) and the efficacy of the current anthelmintic treatment protocol. J Wildl Dis 2006; 42(2): 402-406. http://dx.doi.org/10.7589/0090-3558-42.2.402. PMid:16870865.
http://dx.doi.org/10.7589/0090-3558-42.2...
; Vieira et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721(1): 1-23. http://dx.doi.org/10.11646/zootaxa.1721.1.1.
http://dx.doi.org/10.11646/zootaxa.1721....
; Pinto et al., 2011Pinto RM, Knoff M, Gomes DG, Noronha D. Nematodes from mammals in Brazil: an updating. Neotrop Helminthol 2011; 5(2): 139-183.; Aranda et al., 2013Aranda R, Serrano-Martínez E, Tantaleán M, Quispe M, Casas G. Identificación y frecuencia de parásitos gastrointestinales en félidos silvestres en cautiverio en el Perú. Rev Investig Vet Peru 2013; 24(3): 360-368. http://dx.doi.org/10.15381/rivep.v24i3.2585.
http://dx.doi.org/10.15381/rivep.v24i3.2...
; Moleón et al., 2015Moleón MS, Kinsella JM, Moreno PG, Ferreyra HDV, Pereira J, Pía M, et al. New hosts and localities for helminths of carnivores in Argentina. Zootaxa 2015; 4057(1): 106-114. http://dx.doi.org/10.11646/zootaxa.4057.1.6. PMid:26701468.
http://dx.doi.org/10.11646/zootaxa.4057....
; Gomez-Puerta et al., 2016Gomez-Puerta LA, Alarcon V, Pacheco J, Franco F, Lopez-Urbina MT, Gonzalez AE. Molecular and morphological evidence of Taenia omissa in pumas (Puma concolor) in the Peruvian Highlands. Rev Bras Parasitol Vet 2016; 25(3): 368-373. http://dx.doi.org/10.1590/S1984-29612016046. PMid:27580394.
http://dx.doi.org/10.1590/S1984-29612016...
). Two checklists group the data of these studies, listing ten species of nematodes, four cestodes, and three acanthocephalans (Vicente et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides Do Brasil. Parte V: nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl.1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; Vieira et al., 2008Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721(1): 1-23. http://dx.doi.org/10.11646/zootaxa.1721.1.1.
http://dx.doi.org/10.11646/zootaxa.1721....
). Even though, there is little information on parasites affecting cougars in São Paulo State, one of the Brazilian States most affected by human action, leading to the destruction and fragmentation of the original Atlantic rainforest cover. The close interface between wild and urban landscapes may increase parasite exchange between domestic and wild carnivores, as well as to humans. The aim of this study was to describe the parasites of roadkilled cougars collected in an anthropized area from São Paulo State, Brazil.

Between the years 2016 and 2018, five road-killed cougars were referred to the Service of Wild Animal Pathology (SEPAS, FCAV/UNESP Jaboticabal). The highways where the animals were found run-over comprise four cities: Taquaritinga (21°24'21”S; 48°30'18”W), Matão (21°36'10”S; 48°21'57”W), Taquaral (21°04'19”S; 48°24'36”W), and Borborema (21°37'12”S; 49°04'26”W). After necropsy, the organs of each animal were individualized, slit open in metallic trays and thoroughly washed in tap water. The resultant material was sieved in metallic sieves (Tyler 100μm). The retained material was fixed and stored in 70% ethanol, in properly identified vials (organ, species, host sex, estimated age, and date of collection). The helminths were recovered after careful inspection of the contents under stereoscopic microscope. The taxonomic identification was based on morphological analyses of the parasites, which were prepared in temporary mounts. Taxonomic identifications were based on 10 individuals of each sex (dioecious), 10 adult individuals (monoecious) or the maximum number available. Images were obtained in Olympus BX51 microscope with digital camera, and then they were processed in Image Pro Plus 4.1 software. Morphologic and morphometric data were compared to previous published data (Lühe, 1910Lühe M. Parasitische Plattwurmer. II. Cestodes. In: Brauer A, editor. Die Susswasser Fauna Deutschlands. Jena: Verlag von Gustav Fischer; 1910. p. 687-710.; Travassos, 1917Travassos L. Contribuições para o conhecimento da fauna helmintolojica brazileira. Mem Inst Oswaldo Cruz 1917; 9(1): 5-62. http://dx.doi.org/10.1590/S0074-02761917000100001.
http://dx.doi.org/10.1590/S0074-02761917...
; Machado Filho, 1964Machado Filho DA. Contribuição para o conhecimento do gênero “Oncicola” Travassos 1916 (Archiancantocephala, Pashysentidae). Rev Bras Biol 1964; 24(1): 23-30. PMid:14182085.; Mueller, 1974Mueller JF. The biology of Spirometra. J Parasitol 1974; 60(1): 3-14. http://dx.doi.org/10.2307/3278670. PMid:4592501.
http://dx.doi.org/10.2307/3278670...
; Waid & Pence, 1988Waid DD, Pence DB. Helminths of mountain lions (Felis concolor) from southwestern Texas, with a redescription of Cylicospirura subaequalis (Molin, 1860) Vevers, 1922. Can J Zool 1988; 66(10): 2110-2117. http://dx.doi.org/10.1139/z88-313.
http://dx.doi.org/10.1139/z88-313...
; Vicente et al., 1997Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides Do Brasil. Parte V: nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl.1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001.
http://dx.doi.org/10.1590/S0101-81751997...
; Anderson et al., 2009Anderson RC, Chabaud AG, Willmott S. Keys to the Nematode parasites of vertebrates. Wallingford, UK: CAB International; 2009. http://dx.doi.org/10.1079/9781845935726.0000.
http://dx.doi.org/10.1079/9781845935726....
; Gomez-Puerta et al., 2016Gomez-Puerta LA, Alarcon V, Pacheco J, Franco F, Lopez-Urbina MT, Gonzalez AE. Molecular and morphological evidence of Taenia omissa in pumas (Puma concolor) in the Peruvian Highlands. Rev Bras Parasitol Vet 2016; 25(3): 368-373. http://dx.doi.org/10.1590/S1984-29612016046. PMid:27580394.
http://dx.doi.org/10.1590/S1984-29612016...
). Subsequently, the descriptors of infection (prevalence, mean abundance, mean intensity and range of intensity) were calculated based on Bush et al. (1997)Bush AO, Lafferty KD, Lotz JM, Shostak AL. Revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
http://dx.doi.org/10.2307/3284227...
. Vouchers were deposited in the Collection Oswaldo Cruz Institute (CHIOC/Fiocruz) and additional types were kept in the collection of the LabEPar, FCAV/Unesp.

A total of 344 adult helminths were found in the five necropsied animals, three adult males and two females, one adult and one young, all in good body condition. Ten different species were found: five nematodes, three cestodes and two acanthocephalans (Figure 1). All the cougars were infected by at least one species of helminth. Two to five species were observed simultaneously infecting the same host, with an average of two species per host. The descriptors of infection are presented in Table 1.

Figure 1
Helminths found in cougars road-killed in the Northeast Region of the State of São Paulo, Brazil. A) Uncinaria bidens, oral capsule provided with plates. Scale: 300µm B) Cylicospirura subaequalis, anterior region, presence of bifid teeth. Scale: 300µm C) Lagochilascaris major, presence of three lips, interlabial groove and absence of cervical wings. Scale: 300µm. D) Toxascaris leonina, anterior region with elongated cervical wings, three small lips. Scale: 500µm. E) Echinococcus sp. pyriform scolex with four suction cups, Scale: 500µm. F) Filaroides sp. Female, caudal extremity, lateral view. Scale: 300µm. G) Taenia omissa, rostelo armed with two rows of hooks. Scale: 300µm. H) Oncicola oncicola and Oncicola canis, parasites attached to the intestinal mucosa. I) Spirometra sp., mature proglotides with spiral-shaped uterus and genital pore. Scale: 500µm. Light microscopy.
Table 1
Descriptors of helminth infection observed on road-killed wild cougars (Puma concolor) collected in Northeastern region São Paulo State, between the years 2016 and 2018.

Human-induced environmental modification drives the emergence of diseases in humans and in domestic and wild animals (Nava et al., 2017Nava A, Shimabukuro JS, Chmura AA, Luz SLB. The impact of global environmental changes on infectious disease emergence with a focus on risks for Brazil. ILAR J 2017; 58(3): 393-400. http://dx.doi.org/10.1093/ilar/ilx034. PMid:29253158.
http://dx.doi.org/10.1093/ilar/ilx034...
). Animals carcasses found roadkilled can provide study materials for parasitological investigations and are regarded as advantageously available samples in eco-epidemiological studies (Richini-Pereira et al., 2010Richini-Pereira V, Bosco S, Theodoro R, Barrozo L, Bagagli E. Road-killed wild animals: a preservation problem useful for eco-epidemiological studies of pathogens. J Venom Anim Toxins Incl Trop Dis 2010; 16(4): 607-613. http://dx.doi.org/10.1590/S1678-91992010000400011.
http://dx.doi.org/10.1590/S1678-91992010...
). Carnivores are known to harbor several pathogens, such as zoonotic helminths (Brown, 2004Brown C. Emerging zoonoses and pathogens of public health significance--An overview. Rev Sci Tech 2004; 23(2): 435-342. http://dx.doi.org/10.20506/rst.23.2.1495. PMid:15702711.
http://dx.doi.org/10.20506/rst.23.2.1495...
), in addition to which data found this study can be attributed to other animal species in the region through the circulation of pathogens between predator prey and the environment. The increase in wildlife-domestic carnivores-humans contact is of great concern due to the potential that this interaction represents for the emergence of diseases and the dissemination of parasites, especially in highly fragmented and anthropized areas such as the region studied (Daszak et al., 2001Daszak P, Cunningham AA, Hyatt AD. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 2001; 78(2): 103-116. http://dx.doi.org/10.1016/S0001-706X(00)00179-0. PMid:11230820.
http://dx.doi.org/10.1016/S0001-706X(00)...
). It is important to note that some helminths found in this study, such as L. major, Spirometra sp., O. oncicola, O. canis, Echinococcus sp., T. leonina, C. subaequalis, and Filaroides sp., are known to affect domestic carnivores (Dantas-Torres & Otranto, 2014Dantas-Torres F, Otranto D. Dogs, cats, parasites, and humans in Brazil: opening the black box. Parasit Vectors 2014; 7(1): 22. http://dx.doi.org/10.1186/1756-3305-7-22. PMid:24423244.
http://dx.doi.org/10.1186/1756-3305-7-22...
), which may indicate that at some point, an interchange between these hosts may have occurred.

Considering the four valid species of the genus Echinococcus (Cestoda), two species, E. vogeli and E. oligarthrus, occur widely in the Neotropical region, using several carnivores as their definitive hosts (D'Alessandro & Rausch, 2008D’Alessandro A, Rausch RL. New Aspects of Neotropical Polycystic (Echinococcus vogeli) and Unicystic (Echinococcus oligarthrus) Echinococcosis. Clin Microbiol Rev 2008; 21(2): 380-401. http://dx.doi.org/10.1128/CMR.00050-07. PMid:18400802.
http://dx.doi.org/10.1128/CMR.00050-07...
). The cougars are the type-host for E. oligarthrus (Lühe, 1910Lühe M. Parasitische Plattwurmer. II. Cestodes. In: Brauer A, editor. Die Susswasser Fauna Deutschlands. Jena: Verlag von Gustav Fischer; 1910. p. 687-710.). In the State of São Paulo, there are two human cases of infection by metacestodes of this parasite reported at the Ribeirão Preto Medical School Hospital (UHFMRP) (Meneghelli et al., 1992Meneghelli UG, Martinelli ALC, Llorach Velludo MAS, Bellucci AD, Magro JE, Barbõ MLP. Polycystic hydatid disease (Echinococcus vogeli): Clinical, laboratory and morphological findings in nine Brazilian patients. J Hepatol 1992; 14(2-3): 203-210. http://dx.doi.org/10.1016/0168-8278(92)90159-M. PMid:1500684.
http://dx.doi.org/10.1016/0168-8278(92)9...
), the same region of the present study. As cougars are frequently registered close to rural settlements and urban areas in the studied region, the risk of human infection must be considered, especially regarding people with close contact to forest remnants and riparian forests, where these animals live.

The anthropic action may increase the contact between domestic and wild animals, as well as between humans and wildlife. New epidemiological situations may be resultant of these interactions and monitoring of wildlife diseases may provide valuable information (Daszak et al., 2001Daszak P, Cunningham AA, Hyatt AD. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 2001; 78(2): 103-116. http://dx.doi.org/10.1016/S0001-706X(00)00179-0. PMid:11230820.
http://dx.doi.org/10.1016/S0001-706X(00)...
). The occurrence of helminths such as L. major, Spirometra sp., O. oncicola, O. canis, Echinococcus sp., T. leonina, C. subaequalis, and Filaroides sp. which are known to affect domestic carnivores, may indicate the permutation between wild and domestic hosts, in addition to the study representing new host records for four of the species found in cougars, U. bidens, L. major, O. canis, and Filaroides sp.; and also new locality records for U. bidens, T. leonina, C. subaequalis, and Filaroides sp.

Our results contribute to monitoring the health of this cougar population and combined with other ecological, behavioral and parasitic data, will help guide conservation actions to maintain a viable cougar population in that region as well as for public health.

Acknowledgments

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

  • How to cite: Benatti D, De Santi M, Werther K, Tebaldi JH, Hoppe EGL. Helminthfauna of road-killed cougars (Puma concolor) from the Northeastern Region of São Paulo State, Brazil. Braz J Vet Parasitol 2021; 30(1): e024120. https://doi.org/10.1590/S1984-29612021008

References

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    » http://dx.doi.org/10.15381/rivep.v24i3.2585
  • Azevedo FC, Lemos FG, Almeida LB, Campos CB, Beisiegel BM, Paula RC, et al. Avaliação do risco de extinção da Onça-parda Puma concolor (Linnaeus, 1771) no Brasil. Biodivers Bras 2013; 3(1): 107-121.
  • Brown C. Emerging zoonoses and pathogens of public health significance--An overview. Rev Sci Tech 2004; 23(2): 435-342. http://dx.doi.org/10.20506/rst.23.2.1495 PMid:15702711.
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    » http://dx.doi.org/10.1128/CMR.00050-07
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    » http://dx.doi.org/10.1186/1756-3305-7-22
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    » http://dx.doi.org/10.1016/S0001-706X(00)00179-0
  • Foster GW, Cunningham MW, Kinsella JM, McLaughlin G, Forrester DJ. Gastrointestinal helminths of free-ranging florida panthers (Puma concolor coryi) and the efficacy of the current anthelmintic treatment protocol. J Wildl Dis 2006; 42(2): 402-406. http://dx.doi.org/10.7589/0090-3558-42.2.402 PMid:16870865.
    » http://dx.doi.org/10.7589/0090-3558-42.2.402
  • Gomez-Puerta LA, Alarcon V, Pacheco J, Franco F, Lopez-Urbina MT, Gonzalez AE. Molecular and morphological evidence of Taenia omissa in pumas (Puma concolor) in the Peruvian Highlands. Rev Bras Parasitol Vet 2016; 25(3): 368-373. http://dx.doi.org/10.1590/S1984-29612016046 PMid:27580394.
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    » http://dx.doi.org/10.1016/j.biocon.2014.07.017
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  • Meneghelli UG, Martinelli ALC, Llorach Velludo MAS, Bellucci AD, Magro JE, Barbõ MLP. Polycystic hydatid disease (Echinococcus vogeli): Clinical, laboratory and morphological findings in nine Brazilian patients. J Hepatol 1992; 14(2-3): 203-210. http://dx.doi.org/10.1016/0168-8278(92)90159-M PMid:1500684.
    » http://dx.doi.org/10.1016/0168-8278(92)90159-M
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    » http://dx.doi.org/10.1111/j.1744-7429.2011.00772.x
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    » http://dx.doi.org/10.11646/zootaxa.4057.1.6
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Publication Dates

  • Publication in this collection
    29 Mar 2021
  • Date of issue
    2021

History

  • Received
    23 Oct 2020
  • Accepted
    20 Jan 2021
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
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