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Infectious Diseases in Free-Ranging Blonde Capuchins, Sapajus flavius, in Brazil

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Abstract

The main threats to primates worldwide are the degradation, fragmentation, and loss of their habitats; hunting (especially for bushmeat); and illegal trade. For many species, the most important threat is forest fragmentation, resulting in small populations that are restricted to isolated forest patches. In this situation, primates are particularly vulnerable to disease. The Endangered blonde capuchin (Sapajus flavius) is now restricted to a few forest patches in Northeast Brazil. We investigated the occurrence of parasites and bacterial diseases in one of three free-ranging groups of S. flavius in a small forest patch in Paraíba state, Northeast Brazil. We tested for antibodies against Leishmania spp., Trypanosoma cruzi, Toxoplasma gondii, Leptospira spp. (24 strains), and Brucella spp.. We used molecular analysis to detect Plasmodium spp., and evaluated blood smears for the presence of hemoparasites. All individuals tested negative for Leptospira spp. and B. abortus, but 8 of 48 (16%) presented antibodies for both Leishmania spp. and T. cruzi. We identified antibodies to T. gondii in 12% of the individuals tested. Plasmodium brasilianum infection was present in 4% of the individuals tested, and blood smears showed microfilariae parasites in 46% of the individuals tested. The occurrence of these infectious diseases in S. flavius may pose a significant threat in terms of reduced recruitment and poor survival rates, and an understanding of the influence of pathogens is crucial for the management of small populations of primates.

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References

  • Alvarenga, D. A. M., Pina-Costa, A., Sousa, T. N., Pissinatti, A., Zalis, M. G., et al (2015). Simian malaria in the Brazilian Atlantic Forest: First description of natural infection of capuchin monkeys (Cebinae subfamily) by Plasmodium simium. Malaria Journal, 14(81), 1–9.

    Google Scholar 

  • Alves, C. J. (1995). Influência de fatores ambientais sobre a Proporção de Caprinos Soro-reatores para a leptospirose em cinco centros de criação do Estado da Paraíba, Brasil. Doctoral dissertation, Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo.

  • Ashford, R. W. (1996). Leishmaniasis reservoir and their significance in control. Clinics in Dermatology, 14, 523–532.

    Article  CAS  PubMed  Google Scholar 

  • Baitchman, E. J., Calle, P. P., James, S. B., Linn, M. J., & Raphael, B. L. (2006). Leptospirosis in Wied’s marmosets (Callithrix kuhlii). Journal of Zoo and Wildlife Medicine, 37, 182–185.

    Article  PubMed  Google Scholar 

  • Barbosa, M. R. V. (1996). Estudo florístico e fitossociológico da mata do Buraquinho, remanescente de Mata Atlântica em João Pessoa, PB. Doctoral dissertation, Universidade Estadual de Campinas, São Paulo. Available from Universidade Estadual de Campinas; Biblioteca Digital da Unicamp; vtls000107407.

  • Benchimol, B. P. R. (2006). The oral transmission of Chagas’ disease: An acute form of infection responsible for regional outbreaks. International Journal of Cardiology, 112(1), 132–133.

    Article  Google Scholar 

  • Bern, C., Kjos, S., Yabsley, M. J., & Montgomery, S. P. (2011). Trypanosoma cruzi and Chagas’ disease in the United States. Clinical Microbiology Reviews, 24(4), 655–681.

    Article  PubMed  PubMed Central  Google Scholar 

  • Brandão-Filho, P., Campbell-Lendrum, D., Brito, M. E., Shaw, J. J., & Davies, C. R. (1999). Epidemiological surveys confirm an increasing burden of cutaneous leishmaniasis in northeast Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene, 93(5), 488–494.

    Article  PubMed  Google Scholar 

  • Brazil, MAPA/SDA/DSA. (2006). Programa Nacional de Controle e Erradicação da Brucelose e da Tuberculose – PNCEBT 2006. Brasília: Ministério da Agricultura, Pecuária e Abastecimento (MAPA), Secretaria de Defesa Agropecuária (SDA), Departamento de Saúde Animal (DSA). www.adaptar.pr.gov.br/rquivos/File/GSA/PECEBT/MANUAL_PNCET.pdf. Accessed 16 June 2016.

  • Brazil, Ministério da Saúde. (2005). Manual de diagnóstico laboratorial da malária. Brasília: Secretaria de Vigilância em Saúde http://bvsms.saude.gov.br/bvs/publicacoes/malaria_diag_manual_final.pdf (Accessed Apr 11, 2016.

    Google Scholar 

  • Brazil, Ministério da Saúde. (2015). Sistema de Informação de Agravos de Notificação. Brasília. http://dtr2004.saude.gov.br/sinanweb/tabnet/dh?sinannet/malaria/bases/malabrnet.def (Accessed Dec 15, 2015).

  • Brazil, Ministério da Saúde. (2016). Sistema de Informação de Agravos de Notificação. Brasília: Ministério da Saúde. http://www.datasus.gov.br/DATASUS/index.php?area=0203&id=29878153 (Accessed Mar 16, 2016).

  • Brazil, Ministério do Meio Ambiente. (2014). Portaria n° 444, de 17 de Dezembro de 2014. Atualização da lista nacional oficial de espécies da fauna ameaçadas de extinção. Diário Oficial da União, Poder Executivo 18 dezembro 2014. Seção 1, pp. 121–130.

  • Bueno, M. G. (2012). Pesquisa de Leishmania spp. e Plasmodium spp. em primatas neotropicais provenientes de regiões de Mata Atlântica e Amazônia impactadas por ações antrópicas: Investigação in situ e ex situ. Doctoral dissertation, Departamento de Patologia Faculdade de Medicina Veterinária e Zootécnica – Universidade de São Paulo.

  • Bueno, G. B., Rohe, F., Kirchgatter, K., Di Santi, S. M., Guimarães, L. O., et al (2013). Survey of Plasmodium spp. in free-ranging Neotropical primates from the Brazilian Amazon region impacted by anthropogenic actions. EcoHealth, 10, 48–53.

    Article  PubMed  Google Scholar 

  • Catão-Dias, J. L., Epiphanio, S., & Kierulff, M. C. M. (2013). Neotropical primates and their susceptibility to Toxoplasma gondii: New insights for an old problem. In J. F. Brinkworth & E. Pechenkina (Eds.), Primates, pathogens, and evolution (pp. 253–289). Developments in Primatology: Progress and Prospects. New York: Springer Science + Business Media.

  • Cook, R. A., & Karesh, W. B. (2008). Emerging diseases at the interface of people, domestic animals and wildlife. In M. E. Fowler & R. E. Miller (Eds.), Zoo and wild animal medicine: Current therapy (pp. 55–65). St. Louis: Saunders-Elsevier.

    Chapter  Google Scholar 

  • Cross, P. C., Drewe, J., Patrek, V., Pearce, G., Samuel, M. D., & Delahay, R. J. (2009). Wildlife population structure and parasite transmission: Implications for disease management. In R. J. Delahay, G. C. Smith, & M. R. Hutchings (Eds.), Management of disease in wild mammals (pp. 1–15). Tokyo: Springer.

    Google Scholar 

  • Daszak, P., Cunningham, A. A., & Hyatt, A. D. (2000). Emerging infectious diseases of wildlife: Threats to biodiversity and human health. Science, 287, 443–449.

    Article  CAS  PubMed  Google Scholar 

  • de Lima, V. M., Fattori, K. R., Michelin, A. F., Silveira, D., Neto, L., & Vasconcelos, R. O. (2010). Comparison between elisa using total antigen and immunochromatography with antigen rK39 in the diagnosis of canine visceral leishmaniasis. Veterinary Parasitology, 173(3–4), 330–333.

    Article  PubMed  Google Scholar 

  • de Oliveira, M. M., Boubli, J. P., & Kierulff, M. C. M. (2015). Cebus flavius. The IUCN Red List of Threatened Species. Version 2014.3. www.iucnredlist.org (Accessed Mar 20, 2016).

  • Dean, A. G., Sullivan, K. M., & Soe, M. M. (2013). OpenEpi: Open source epidemiologic statistics for public health, version. http://www.openepi.com/Menu/OE_Menu.htm (Updated April 5, 2013; accessed Feb 16, 2017).

  • Deane, L. M. (1992). Simian malaria in Brazil. Memórias do Instituto Oswaldo Cruz, 87(3), 1–20.

    Article  PubMed  Google Scholar 

  • Deem, S. L., Karesh, W. B., & Weisman, W. (2001). Putting theory into practice: Wildlife health in conservation. Conservation Biology, 15, 1224–1233.

    Article  Google Scholar 

  • Dobson, A. J., & Barnett, A. G. (2002). An introduction to generalized linear models. Boca Raton: Chapman & Hall/CRC.

    Google Scholar 

  • Dória, J. D., Silva, A. G., & Costa, A. R. (1974). Leptospirose: Presença de aglutininas anti-leptospira no soro de saguis (Callithrix penicillata) no Estado da Bahia. Boletim do Instituto de Biologia da Bahia, 13, 148–149.

    Google Scholar 

  • dos Santos, L. C., Curotto, S. M. R., & Moraes, W. (2009). Detection of Plasmodium sp. in capybara. Veterinary Parasitology, 163, 148–151.

    Article  PubMed  Google Scholar 

  • Duarte, A. M. R. C., Malafronte, R. S., Cerutti Jr., C., Curado, I., Paiva, B. R., et al (2008). Natural Plasmodium infections in Brazilian wild monkeys: Are reservoirs for human infections? Acta Tropica, 107(2), 179–185.

    Article  PubMed  Google Scholar 

  • Dubey, J. P., & Desmonts, G. (1987). Serological responses of equids fed Toxoplasma gondii oocysts. Equine Veterinary Journal, 19, 337–339.

    Article  CAS  PubMed  Google Scholar 

  • Epiphanio, S., Sa, L. R. M., Teixeira, R. H. F., & Catão-Dias, J. L. (2000). Toxoplasmosis in a wild caught black lion tamarin (Leontopithecus chrysopygus). Veterinary Records, 149, 627–628.

    Article  Google Scholar 

  • Epiphanio, S., Sinhorini, I. L., & Catão-Dias, J. L. (2003). Pathology of toxoplasmosis in captive New World primates. Journal of Comparative Pathology, 129, 196–204.

    Article  CAS  PubMed  Google Scholar 

  • Escalante, A. A., Barrio, E., & Ayala, F. J. (1995). Evolutionary origin of human and primate malarias: Evidence from the circumsporozoite protein gene. Molecular Biology and Evolution, 12(4), 616–626.

    CAS  PubMed  Google Scholar 

  • Estrada, A., Garber, P., Rylands, A. B., Roos, C., Fernandez-Duque, E., et al (2017). Impending extinction crisis of the world’s primates: Why primates matter. Science Advances, 3, e1600946.

    PubMed  PubMed Central  Google Scholar 

  • Fandeur, T., Volney, B., Peneau, C., & De Thoisy, B. (2000). Monkeys of the rainforest in French Guiana are natural reservoirs for P. brasilianum/P. malariae malaria. Parasitology, 120, 11–21.

    Article  CAS  PubMed  Google Scholar 

  • Ferreira, D. R. A., Laroque, P. O., Wagner, G. C., Higino, S. S. S., Azevedo, S. S., et al (2011). Occurrence of antibodies and risk factors associated with Leptospira spp. infection in capitivity Cebus spp. from Northeast of Brazil. Pesquisa Veterinária Brasileira, 31(11), 1019–1023.

    Article  Google Scholar 

  • Ferreira, D. R. A., Ribeiro, V. O., Laroque, P. O., Wagner, P. G. C., Pinheiro Júnior, J. W., et al (2015). Risk factors associated with Toxoplasma gondii infection in captive Sapajus spp. American Journal of Primatology, 7(5), 558–562.

    Article  Google Scholar 

  • Fialho, M. S., & Gonçalves, G. F. (2008). Primatas da RPPN Gargaú, Paraíba, Brasil. Neotropical Primates, 15(2), 50–54.

    Article  Google Scholar 

  • Fialho, M. S., Valença-Montenegro, M. M., da Silva, T. C. F., Ferreira, J. G., & Laroque, P. O. (2014). Ocorrência de Sapajus flavius e Alouatta belzebul no Centro de Endemismo Pernambuco. Neotropical Primates, 21(2), 214–218.

    Article  Google Scholar 

  • Fragaszy, D. M., Visalberghi, E., & Fedigan, L. M. (2004). The complete capuchin: The biology of the genus Cebus. Cambridge: Cambridge University Press.

    Google Scholar 

  • Garcia, J. L., Svoboda, W. K., Chryssafidis, A. L., Malanski, L. S., Shiozawa, M. M., et al (2005). Sero-epidemiological survey for toxoplasmosis in wild New World monkeys (Cebus spp.; Alouatta caraya) at the Paraná river basin, Paraná State, Brazil. Veterinary Parasitology, 133, 307–311.

    Article  PubMed  Google Scholar 

  • Gibson, S. V. (1998). Bacterial and mycotic disease of nonhuman primates. In T. Bennett, C. R. Abee, & R. Henrickson (Eds.), Nonhuman primates in biomedical research, Diseases (Vol. 2, pp. 105–172). London: Elsevier Academic Press.

    Google Scholar 

  • Gicheru, M. M., Jeneby, M. M., Macharia, J. C., Carlsson, H. E., & Suleman, M. A. (2009). Prevalence of antibodies and cell mediated immune response against Leishmania major in feral nonhuman primates from Kenya. Acta Tropica, 109, 136–140.

    Article  CAS  PubMed  Google Scholar 

  • Guimarães, L. O., Wunderlich, G., Alves, J. M., Bueno, M. G., Röhe, F., et al (2015). Merozoite surface protein-1 genetic diversity in Plasmodium malariae and Plasmodium brasilianum from Brazil. BMC Infectious Diseases, 15, 529.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hayakawa, T., Nobuko, A., Toshifumi, U., Hiroshisa, H., Sattabongkot, J., et al (2009). Identification of Plasmodium malariae, a human malaria parasite, in imported chimpanzees. PLoS ONE, 4(10), e7412.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hershkovitz, P. (1987). A history of the recent mammalogy of the Neotropical region from 1492 to 1850. Fieldiana, Zoology, New Series, 39, 11–98.

    Google Scholar 

  • Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., et al (2008). Global trends in emerging infectious diseases. Nature, 451, 990–993.

    Article  CAS  PubMed  Google Scholar 

  • Karesh, W. B., Wallace, R. B., Painter, R. L. E., Rumiz, D., Braselton, W. E., et al (1998). Immobilization and health assessment of free-ranging black spider monkeys (Ateles paniscus chamek). American Journal of Primatology, 44, 107–123.

    Article  CAS  PubMed  Google Scholar 

  • Kock, R. A., Woodford, M. H., & Rossiter, P. B. (2010). Disease risk associated with the translocation of wildlife. Revue Scientifique et Technique, 29(2), 329–350.

    Article  CAS  PubMed  Google Scholar 

  • Leighton, F. A., & Kuiken, T. (2001). Leptospirosis. In E. S. Williams & I. K. Barker (Eds.), Infectious diseases of wild mammals (pp. 498–501). Ames: Iowa State University Press.

    Google Scholar 

  • Leite, R. M. H., Thompson, I. A., Gonçalves, V. S. P., Leite, R. C., Bandeira, D. A., & Lage, A. P. (2003). A random sample survey of bovine brucellosis in the State of Paraíba, Brazil. Brazilian Journal of Veterinary Research and Animal Science, 40, 170–174.

    Article  Google Scholar 

  • Lima, P. J., & Heckendorff, W. D. (1985). Climatologia. In Governo do Estado da Paraíba, Secretaria de Educação, Universidade Federal da Paraíba (Ed.), Atlas geográfico do estado da Paraíba (pp. 34–44). João Pessoa: Grafset.

  • Lynch Alfaro, J., Silva Jr., J. S., & Rylands, A. B. (2012). How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. American Journal of Primatology, 74, 273–286.

    Article  Google Scholar 

  • Mackenstedt, U., Jenkins, D., & Romig, T. (2015). The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas. International Journal for Parasitology: Parasites and Wildlife, 4(1), 71–79.

    PubMed  PubMed Central  Google Scholar 

  • Malta, M. C., Tinoco, H. P., Xavier, M. N., Vieira, A. L., Costa, E. A., & Santos, R. L. (2010). Naturally acquired visceral leishmaniasis in non-human primates in Brazil. Veterinary Parasitology, 169, 193–197.

    Article  PubMed  Google Scholar 

  • Marcgrave, G. (1648). Historiae rerum naturalium Brasiliae, Libro VI (pp. 221–244). Leiden: Ioanes de Laet, Elzevier.

  • Mense, M. G., Borschel, R. H., Wilhelmsen, C. L., Pitt, M. L., & Hoover, D. L. (2004). Pathologic changes associated with brucellosis experimentally induced by aerosol exposure in rhesus macaques (Macaca mulatta). American Journal of Veterinary Research, 65, 644–652.

    Article  PubMed  Google Scholar 

  • Molina, C. V., Catão-Dias, J. L., Ferreira Neto, J. S., Vasconcellos, S. A., Gennari, S. M., et al (2014). Sero-epidemiological survey for brucellosis, leptospirosis, and toxoplasmosis in free-ranging Alouatta caraya and Callithrix penicillata from São Paulo state, Brazil. Journal of Medical Primatology, 43, 197–201.

    Article  PubMed  Google Scholar 

  • Monteiro, R. V., Baldez, J., Dietz, J., Baker, A., Lisboa, V. C., & Jansen, A. M. (2006). Clinical, biochemical, and electrocardiographic aspects of Trypanosoma cruzi infection in free-ranging golden lion tamarins (Leontopithecus rosalia). Journal of Medical Primatology, 135, 48–55.

    Article  Google Scholar 

  • Nunn, C. L., & Altizer, S. M. (2005). The global mammal parasite database: An online resource for infectious disease records in wild primates. Evolutionary Anthropology, 14, 1–2.

    Article  Google Scholar 

  • Nunn, C. L., & Gillespie, T. R. (2016). Infectious disease and primate conservation. In S. A. Wich & A. J. Marshall (Eds.), An introduction to primate conservation (pp. 157–173). Oxford: Oxford University Press.

    Chapter  Google Scholar 

  • Oliveira, M. M., & Langguth, A. (2006). Rediscovery of Marcgrave’s capuchin monkey and designation of a neotype for Simia flavia Schreber, 1774 (Primates, Cebidae). Boletim do Museu Nacional, 523, 1–16.

    Google Scholar 

  • Orihel, T. C., & Seibold, H. R. (1972). Nematodes of the bowel and tissues. In R. N. T. W. Fiennes (Ed.), Pathology of simian primates. Part II: Infectious and parasitic diseases (pp. 76–103). London: S. Karger.

  • Osofsky, S. A., Kock, R. A., Kock, M. D., Kalema-Zikusoka, G., Grahn, R., et al. (2005). Building support for protected areas using a ‘one health’ perspective. In J. A. McNeely (Ed.), Friends for life: New partners in support of protected areas (pp. 65–79). Gland: IUCN.

  • Percy, D. H., Egwu, N., & Jonas, A. M. (1972). Experimental Brucella canis infection in the monkey (Macaca arctoides). Canadian Journal of Comparative Medicine, 36, 221–225.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perkins, S. L., & Schall, J. J. (2002). A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. Journal of Parasitology, 88, 972–978.

    Article  CAS  PubMed  Google Scholar 

  • Perolat, P., Poingt, J. P., Vie, J. C., Jouaneau, C., Baranton, G., et al (1992). Occurrence of severe leptospirosis in a breeding colony of squirrel monkeys. The American Journal of Tropical Medicine and Hygiene, 46, 538–545.

    Article  CAS  PubMed  Google Scholar 

  • Pina-Costa, A., Brasil, P., Di Santi, S. M., Araujo, M. P., Suárez-Mutis, M. C., et al (2014). Malaria in Brazil: What happens outside the Amazonian endemic region. Memórias do Instituto Oswaldo Cruz, 109(5), 618–633.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pontes, A. R. M., Malta, A., & Asfora, P. H. (2006). A new species of capuchin monkey, genus Cebus erxleben (Cebidae, Primates): Found at the very brink of extinction in the Pernambuco Endemism Centre. Zootaxa, 1220, 1–12.

    Google Scholar 

  • R Core Team. (2015). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org/ (Accessed May 20, 2016).

  • Resing, S., & Oerke, A. K. (2005). Husbandry and management of New World species: Marmosets and tamarins. In S. Wolfe-Coote (Ed.), The laboratory primate (pp. 145–162). London: Elsevier Academic Press.

    Google Scholar 

  • Robert-Gangneux, F., & Dardé, M. L. (2012). Epidemiology of and diagnostic strategies for toxoplasmosis. Clinical Microbiology Reviews, 25, 264–296.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues, K. C. (2013). Padrão de atividades, comportamento alimentar, exploração de habitat e área de vida de Um grupo de Sapajus flavius (Schreber, 1774) (Primates, Cebidae). Dissertation, Universidade Federal da Paraíba. http://tede.biblioteca.ufpb.br:8080/handle/tede/7631 (Accessed May 10, 2016).

  • Santos, S. V., Strefezzi, R. F., Pissinatti, A., Kanamura, C. T., Takakura, C. F. H., et al (2014). Detection of Toxoplasma gondii in two southern wooly spider monkeys (Brachyteles arachnoides – Geoffroy, 1806) from the Rio de Janeiro Primate Center, Brazil. Journal of Medical Primatology, 43, 125–129.

    Article  CAS  PubMed  Google Scholar 

  • Schlabritz-Loutsevitch, N. E., Whatmore, A. M., Quance, C. R., Koylass, M. S., Cummins, L. M., et al (2009). A novel Brucella isolate in association with two cases of still-birth in non-human primates: First report. Journal of Medical Primatology, 38, 70–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schreber, J. C. D. (1774). Die Säugthiere in Abbildungen nach der Natur mit Beschreibungen. Erlangen: Theil 1, Heft 4, pp. 57–64, pls. 27–34.

  • Shikanai-Yasuda, M. A., Marcondes, C. B., Guedes, L. A., Siqueira, G. S., Barone, A. A., et al (1991). Possible oral transmission of acute Chagas’ disease in Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 33(5), 351–357.

    Article  CAS  PubMed  Google Scholar 

  • Silveira, T. F., Moraes, M. A. P., Lainson, R., & Shaw, J. J. (1990). Leishmaniose cutânea experimental III: Aspectos histopatológicos do comportamento evolutivo da lesão cutânea produzida em Cebus apella (Primates: Cebidae) por Leishmania (Viannia) lainsoni, L. (V.) braziliensis e L. (Leishmania) amazonensis. Revista de Medicina Tropical, 32(6), 387–394.

    Article  CAS  Google Scholar 

  • Siqueira, D. B., Aléssio, F. M., Mauffrey, J. F., Marvulo, M. F., Ribeiro, V. O., et al (2013). Seroprevalence of Toxoplasma gondii in wild marsupials and rodents from the Atlantic Forest of Pernambuco state, Northeastern Region, Brazil. Journal of Parasitology, 99(6), 1140–1143.

    Article  CAS  PubMed  Google Scholar 

  • Smith, K. F., Acevedo-Whitehouse, K., & Pedersen, A. B. (2009). The role of infectious diseases in biological conservation. Animal Conservation, 12, 1–12.

    Article  Google Scholar 

  • Souza Jr., M. F., Lobato, Z. I. P., Lobato, F. C. F., Moreira, E. C., Oliveira, R. R., et al (2006). Presença de anticorpos da classe IgM de Leptospira interrogans em animais silvestres do Estado do Tocantins. Revista da Sociedade Brasileira de Medicina Tropical, 39(3), 292–294.

    Article  Google Scholar 

  • Suzán, G., Esponda, F., Carrasco-Hernández, R., & Aguirre, A. (2012). Habitat fragmentation and infection disease ecology. In A. A. Aguirre, R. O. Ostfeld, & P. Daszak (Eds.), New directions in conservation medicine, applied cases of ecological health (pp. 135–150). Oxford: Oxford University Press.

    Google Scholar 

  • Tabarelli, M., Melo, M. D. V. C., & Lira, O. C. (2006). Nordeste e Estados do Nordeste, menos Sergipe. In M. Campanili & M. Prochnow (Eds.), Mata Atlântica: Uma rede pela floresta (pp. 149–164). Brasília: Rede de ONGs da Mata Atlântica (RMA).

  • Tazi, L., & Ayala, F. J. (2011). Unresolved direction of host transfer of Plasmodium vivax v. P. simium and P. malariae v. P. brasilianum. Infection. Genetics and Evolution, 11, 209–221.

    Article  Google Scholar 

  • Thorne, E. T. (2001). Brucellosis. In E. S. Williams & I. K. Barker (Eds.), Infectious diseases of wild mammals (pp. 372–395). Ames: Iowa State University Press.

    Chapter  Google Scholar 

  • Toft, J. D., & Eberhard, M. L. (1998). Parasitic diseases. In T. Bennett, C. R. Abee, & R. Henrickson. Nonhuman primates in biomedical research, Vol. 2: Diseases (pp. 111–206). London: Elsevier Academic Press.

  • Umezawa, E. S., Nascimento, M. S., Kesper, J. R., Coura, J. R., Borges-Pereira, J., et al (1996). Immunoblot assay using excreted-secreted antigens of Trypanosoma cruzi in serodiagnosis of congenital, acute, and chronic Chagas’ disease. Journal of Clinical Microbiology, 34(9), 2143–2147.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Valença-Montenegro, M. (2011). Ecologia de Cebus flavius (Schreber, 1774) em Remanescentes de Mata Atlântica no Estado da Paraíba. Doctoral dissertation, Universidade de São Paulo, Piracicaba. http://www.teses.usp.br/teses/disponiveis/91/91131/tde-20122011-143229/pt-br.php (Accessed Mar 14, 2016).

  • Valença-Montenegro, M. M., Bezerra, B. M., Martins, A. B., & Fialho, M. S. (2015). Avaliação do Risco de Extinção de Sapajus flavius (Schreber, 1774) no Brasil. Processo de avaliação do risco de extinção da fauna brasileira. ICMBio. http://www.icmbio.gov.br/portal/biodiversidade/fauna-brasileira/lista-de-especies/7272-mamiferos-sapajus-flavius-macaco-prego-galego.html (Accessed Feb 24, 2017).

  • Verona, C. E. S. (2008). Parasitos em sagüi-de-tufo-branco (Callithrix jacchus) no Rio de Janeiro. Doctoral dissertation, Fundação Oswaldo Cruz, Escola Nacional de Saúde Pública Sérgio Arouca, Rio de Janeiro. http://arca.icict.fiocruz.br/handle/icict/4462 (Accessed Mar 14, 2016).

  • WHO. (2010). Control of the leishmaniases: Report of a meeting of the WHO Expert Committee on the Control of Leishmaniasis, Geneva, 22–26 March. Rome: World Health Organization (WHO). http://whqlibdoc.who.int/trs/WHO_TRS_949_eng.pdf (Accessed Mar 17, 2016).

  • Wilson, D. E. (1936). The pathogenicity of Tanganyika strains of Brucella abortus and B. melitensis for a local species of monkey (Cercopithecus sp.) Journal of Hygiene, 36(1), 125–127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolfe, N. D., Escalante, A. A., Karesh, W. B., Kilbourn, A., Spielman, A., & Lal, A. A. (1998). Wild primate populations in emerging infectious disease research: The missing link? Emerging Infectious Diseases, 4, 149–158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yingst, S. L., Huzella, L. M., Chuvala, L., & Wolcott, M. (2010). A rhesus macaque (Macaca mulatta) model of aerosol-exposure brucellosis (Brucella suis): Pathology and diagnostic implications. Journal of Medical Microbiology, 59, 724–730.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zanette, M. F., Lima, V. M. F., Laurenti, M. D., Rossi, C. N., Vides, J. P., et al (2014). Serological cross-reactivity of Trypanosoma cruzi, Ehrlichia canis, Toxoplasma gondii, Neospora caninum and Babesia canis to Leishmania infantum chagasi tests in dogs. Revista da Sociedade Brasileira de Medicina Tropical, 47(1), 105–107.

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors thank the financial support by Fundação de Amparo à Pesquisa do Estado de São Paulo-FAPESP (09/51466-4; 09/53561-4) and Instituto Chico Mendes de Conservação da Biodiversidade (ICMBIO/CPB). We are grateful to Livia Abdalla (Programa Institucional Biodiversidade e Saúde, Fundação Oswaldo Cruz) for creating the map (Fig. 1). J. L. Catão-Dias, M. D. Laurenti, and S. M. Gennari are recipients of a fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). We are also grateful for the constructive comments made by the editor and reviewer and for the corrections and suggestions made by Dr. Anthony B. Rylands (Conservation International) for improving the paper.

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Authors and Affiliations

  1. Fundação Oswaldo Cruz – Plataforma Institucional Biodiversidade e Saúde Silvestre - Presidência, Rio de Janeiro, 21.040-361, Brasil

    Marina Galvão Bueno

  2. Instituto de Desenvolvimento Sustentável Mamirauá – IDSM/MCTI, Tefé, Amazonas, 69.553-225, Brasil

    Marina Galvão Bueno & Heloise Julião Pavanato

  3. Laboratório de Patologia Comparada de Animais Selvagens – LAPCOM, Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, 05.508-270, Brasil

    José Luiz Catão-Dias

  4. Centro Nacional de Pesquisa e Conservação de Primatas Brasileiros – CPB, Instituto Chico Mendes de Conservação da Biodiversidade, João Pessoa, Paraíba, 58.010-480, Brasil

    Plautino de Oliveira Laroque & Mônica Mafra Valença-Montenegro

  5. Departamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, 05.508-270, Brasil

    Silvio Arruda Vasconcellos, José Soares Ferreira Neto, Solange Maria Gennari & Fernando Ferreira

  6. Laboratório de Patologia de Moléstias Infecciosas, Faculdade de Medicina, Universidade de São Paulo, São Paulo, 01.246-903, Brasil

    Marcia Dalastra Laurenti

  7. Laboratório de Protozoologia, Instituto de Medicina Tropical, Universidade de São Paulo, São Paulo, 05.403-000, Brasil

    Eufrosina Setsu Umezawa & Norival Kesper

  8. Núcleo de Estudos em Malária, Superintendência de Controle de Endemias/Instituto de Medicina Tropical, Universidade de São Paulo, São Paulo, 05.403-000, Brasil

    Karin Kirchgatter & Lilian Oliveira Guimarães

  9. Department of Mathematics and Statistics, University of Otago, PO Box 56, Dunedin, 9054, New Zealand

    Heloise Julião Pavanato

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  1. Marina Galvão Bueno
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  2. José Luiz Catão-Dias
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  14. Mônica Mafra Valença-Montenegro
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Correspondence to Marina Galvão Bueno.

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Bueno, M.G., Catão-Dias, J.L., de Oliveira Laroque, P. et al. Infectious Diseases in Free-Ranging Blonde Capuchins, Sapajus flavius, in Brazil. Int J Primatol 38, 1017–1031 (2017). https://doi.org/10.1007/s10764-017-9994-5

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