Abstract
From 2006 through 2014, we conducted seroepidemiological surveys on non-human primates and sloths to investigate the possible circulation of arboviruses in Bahia Atlantic Forest, Brazil. We collected a total of 196 samples from 103 Leontopithecus chrysomelas, 7 Sapajus xanthosternos, 22 Bradypus torquatus and 7 Bradypus variegatus. Serum samples were tested using neutralization test and hemagglutination inhibition test to detect total antibodies against 26 different arboviruses. The overall prevalence of arboviruses was 36.6% (51/139), with the genus Flavivirus having the highest prevalence (33.1%; 46/139), followed by Phlebovirus (5.0%; 7/139), Orthobunyavirus (4.3%; 6/139) and Alphavirus (0.7%; 1/139). Monotypic reactions suggest that the wild animals were exposed naturally to at least twelve arboviruses. Added results from the neutralization test, animals were exposed to thirteen arboviruses. Most of these viruses are maintained in transmission cycles independent of human hosts, although antibodies against dengue virus serotypes 1, 2 and 3 were found in this study. To our knowledge, this is the first study reporting exposure to arboviruses in L. chrysomelas, S. xanthosternos and B. torquatus. Our results also highlight that the Southern Bahia Atlantic Forest has a variety of vertebrate hosts and potential vectors, which may support the emergence or re-emergence of arboviruses, including those pathogenic to humans.
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References
Alger K, Caldas M (1994) The declining cocoa economy and the Atlantic Forest of Southern Bahia, Brazil: Conservation attitudes of cocoa planters. Environmentalist 14:107–119. https://doi.org/10.1007/bf01901304
Almeida MAB, Cardoso J C, dos Santos E, da Fonseca DF, Cruz LL, Faraco FJC, Bercini MA, Vettorello KC, Porto MA, Mohrdieck R, Ranieri TMS, Schermann MT, Sperb AF, Paz FZ, Nunes ZMA, Romano APM, Costa ZG, Gomes SL, Flannery B (2014) Surveillance for Yellow Fever Virus in Non-Human Primates in Southern Brazil, 2001–2011: A Tool for Prioritizing Human Populations for Vaccination. PLoS Negl Trop Dis 8:. https://doi.org/10.1371/journal.pntd.0002741
Almeida MAB, Dos Santos E, da Cruz Cardoso J, da Fonseca DF, Noll CA, Silveira VR, Maeda AY, de Souza RP, Kanamura C, Brasil RA (2012) Yellow fever outbreak affecting Alouatta populations in southern Brazil (Rio Grande do Sul State), 2008–2009. Am J Primatol 74:68–76. https://doi.org/10.1002/ajp.21010
Al-Shorbaji F, Roche B, Gozlan R, Britton R, Andreou D (2016) The consequences of reservoir host eradication on disease epidemiology in animal communities. Emerg Microbes Infect 5:e46. https://doi.org/10.1038/emi.2016.46
Althouse BM, Vasilakis N, Sall AA, Diallo M, Weaver SC, Hanley KA (2016) Potential for Zika Virus to Establish a Sylvatic Transmission Cycle in the Americas. PLoS Negl Trop Dis 10:e0005055. https://doi.org/10.1371/journal.pntd.0005055
Azevedo R do S da S, Barros VLR de S, Martins LC, Cruz ACR, Rodrigues SG, Vasconcelos PF da C (2010) Estudo experimental sobre a patogenicidade do Vírus Ilhéus em hamsters dourados (Mesocricetus auratus). Rev Pan-Amaz Saúde 1:73–80. https://doi.org/10.5123/s2176-62232010000100011
Barreto FR, Teixeira MG, Costa M da CN, Carvalho MS, Barreto ML (2008) Spread pattern of the first dengue epidemic in the city of Salvador, Brazil. BMC Public Health 8:51. https://doi.org/10.1186/1471-2458-8-51
Batista PM, Andreotti R, Almeida PS, Marques AC, Rodrigues SG, Chiang JO, Vasconcelos PF da C, Batista PM, Andreotti R, Almeida PS, Marques AC, Rodrigues SG, Chiang JO, Vasconcelos PFC (2013) Detection of arboviruses of public health interest in free-living New World primates (Sapajus spp.; Alouatta caraya) captured in Mato Grosso do Sul, Brazil. Rev Soc Bras Med Trop 46:684–690. https://doi.org/10.1590/0037-8682-0181-2013
Batista PM, Andreotti R, Chiang JO, Ferreira MS, Vasconcelos PF da C (2012) Seroepidemiological monitoring in sentinel animals and vectors as part of arbovirus surveillance in the state of Mato Grosso do Sul, Brazil. Rev Soc Bras Med Trop 45:168–173. https://doi.org/10.1590/s0037-86822012000200006
Beaty BJ, Calisher CH, Shope RE (1989) Arboviruses. Diagn Proced Viral Ricketts Chlamydial Infect 797–855
Brazil (2017) Febre Amarela—Informação e orientação. In: Portal Saúde—Minist. Saúde—www.saude.gov.br. http://portalsaude.saude.gov.br/index.php/o-ministerio/principal/leia-mais-o-ministerio/619-secretaria-svs/l1-svs/27300-febre-amarela-informacao-e-orientacao. Accessed 3 March 2017
Bueno MG, Martinez N, Abdalla L, Duarte dos Santos CN, Chame M (2016) Animals in the Zika Virus Life Cycle: What to Expect from Megadiverse Latin American Countries. PLoS Negl Trop Dis 10:. https://doi.org/10.1371/journal.pntd.0005073
Canale GR, Kierulff MCM, Chivers DJ (2013) A Critically Endangered Capuchin Monkey (Sapajus xanthosternos) Living in a Highly Fragmented Hotspot. In: Marsh LK, Chapman CA (eds) Primates in Fragments. Springer New York, pp 299–311
Caron A, Cappelle J, Cumming GS, de Garine-Wichatitsky M, Gaidet N (2015) Bridge hosts, a missing link for disease ecology in multi-host systems. Vet Res 46:. https://doi.org/10.1186/s13567-015-0217-9
Cassano CR, Kierulff MCM, Chiarello AG (2011) The cacao agroforests of the Brazilian Atlantic forest as habitat for the endangered maned sloth Bradypus torquatus. Mamm Biol - Z Für Säugetierkd 76:243–250. https://doi.org/10.1016/j.mambio.2010.06.008
Casseb AR, Silva SP, Casseb LMN, Chiang JO, Martins LC, Vasconcelos PFC (2015) Prevalência de anticorpos contra arbovírus da família Bunyaviridae em búfalos de água Ciênc Anim Bras 16:428–436. https://doi.org/10.1590/1089-6891v16i327208
Catenacci LS, Pessoa MS, Nogueira-Filho SLG, Vleeschouwer KMD (2016) Diet and Feeding Behavior of Leontopithecus chrysomelas (Callitrichidae) in Degraded Areas of the Atlantic Forest of South-Bahia, Brazil. Int J Primatol 37:136–157. https://doi.org/10.1007/s10764-016-9889-x
Clarke DH, Casals J (1958) Techniques for hemagglutination and hemagglutination-inhibition with arthropod-borne viruses. The American Journal of Tropical Medicine and Hygiene 561–573
Crawley MJ (2007) The R Book. Second Edition. Imperial College London at Silwood Park, UK http://www.bio.ic.ac.uk/research/mjcraw/therbook/index.htm. A John Wiley & Sons, Ltd., 950 pp.
Daszak P, Tabor GM, Kilpatrick AM, Epstein J, Plowright R (2004) Conservation medicine and a new agenda for emerging diseases. Ann N Y Acad Sci 1026:1–11. https://doi.org/10.1196/annals.1307.001
de Thoisy B, Dussart P, Kazanji M (2004) Wild terrestrial rainforest mammals as potential reservoirs for flaviviruses (yellow fever, dengue 2 and St Louis encephalitis viruses) in French Guiana. Trans R Soc Trop Med Hyg 98:409–412. https://doi.org/10.1016/j.trstmh.2003.12.003
de Thoisy B, Lacoste V, Germain A, Muñoz-Jordán J, Colón C, Mauffrey J-F, Delaval M, Catzeflis F, Kazanji M, Matheus S, Dussart P, Morvan J, Setién AA, Deparis X, Lavergne A (2009) Dengue infection in neotropical forest mammals. Vector Borne Zoonotic Dis Larchmt N 9:157–170. https://doi.org/10.1089/vbz.2007.0280
Deem SL (2016) Conservation medicine: a solution-based approach for saving nonhuman primates. In: Ethnoprimatology, Waller MT (editors), Springer International Publishing, pp 63–76
Engering A, Hogerwerf L, Slingenbergh J (2013) Pathogen–host–environment interplay and disease emergence. Emerg Microbes Infect 2:e5. https://doi.org/10.1038/emi.2013.5
Faria NR, Azevedo R do S da S, Kraemer MUG, Souza R, Cunha MS, Hill SC, Thézé J, Bonsall MB, Bowden TA, Rissanen I, Rocco IM, Nogueira JS, Maeda AY, Vasami FG da S, Macedo FL de L, Suzuki A, Rodrigues SG, Cruz ACR, Nunes BT, Medeiros DB de A, Rodrigues DSG, Nunes Queiroz AL, da Silva EVP, Henriques DF, Travassos da Rosa ES, de Oliveira CS, Martins LC, Vasconcelos HB, Casseb LMN, Simith D de B, Messina JP, Abade L, Lourenço J, Carlos Junior Alcantara L, de Lima MM, Giovanetti M, Hay SI, de Oliveira RS, Lemos P da S, de Oliveira LF, de Lima CPS, da Silva SP, de Vasconcelos JM, Franco L, Cardoso JF, Vianez-Júnior JL da SG, Mir D, Bello G, Delatorre E, Khan K, Creatore M, Coelho GE, de Oliveira WK, Tesh R, Pybus OG, Nunes MRT, Vasconcelos PFC (2016) Zika virus in the Americas: Early epidemiological and genetic findings. Science 352:345–349. https://doi.org/10.1126/science.aaf5036
Ferreira MS, de Castro PHG, Silva GA, Casseb SMM, Dias Júnior AG, Rodrigues SG, Azevedo R do S da S, Silva MFC, Zauli DAG, Araújo MSS, Béla SR, Teixeira-Carvalho A, Martins-Filho OA, Vasconcelos PFC (2014) Callithrix penicillata: A feasible experimental model for dengue virus infection. Immunol Lett 158:126–133. https://doi.org/10.1016/j.imlet.2013.12.008
Figueiredo MLG, Gomes CA, Amarilla AA, Leandro SA, Orrico SA, Araujo RF, Castro JSM, Durigon EL, Aquino VH, Figueiredo LTM (2010) Mosquitoes infected with dengue viruses in Brazil. Virol J 7:152. https://doi.org/10.1186/1743-422x-7-152
Figueiredo LTM (1999) Vírus brasileiros da família Bunyaviridae. Med Ribeiräo Preto 32:154–8, https://doi.org/10.11606/issn.2176-7262.v32i2p154-158
Figueiredo LTM, Batista WC, Kashima S, Nassar ES (1998) Identification of Brazilian Flaviviruses by simplified reverse transcription-polymerase chain reaction method using Flavivirus universal primers J Trop Med Hyg 59(3): 357–362
Figueiredo LTM (2015) The recent arbovirus disease epidemic in Brazil. Rev Soc Bras Med Trop 48:233–234. https://doi.org/10.1590/0037-8682-0179-2015
Gilmore DP, Da Costa CP, Duarte DP (2001) Sloth biology: an update on their physiological ecology, behavior and role as vectors of arthropods and arboviruses. Braz J Med Biol Res Rev Bras Pesqui Medicas E Biol 34:9–25
Gyawali N, Bradbury RS, Taylor-Robinson AW (2016) The global spread of Zika virus: is public and media concern justified in regions currently unaffected? Infect Dis Poverty 5:37. https://doi.org/10.1186/s40249-016-0132-y
Hanley KA, Monath TP, Weaver SC, Rossi SL, Richman RL, Vasilakis N (2013) Fever versus Fever: the role of host and vector susceptibility and interspecific competition in shaping the current and future distributions of the sylvatic cycles of dengue virus and yellow fever virus. Infect Genet Evol. 0:292–311. https://doi.org/10.1016/j.meegid.2013.03.008
Heymann DL, Hodgson A, Sall AA, Freedman DO, Staples JE, Althabe F, Baruah K, Mahmud G, Kandun N, Vasconcelos PFC, Bino S, Menon KU (2016) Zika virus and microcephaly: why is this situation a PHEIC? Lancet Lond Engl 387:719–721. https://doi.org/10.1016/s0140-6736(16)00320-2
Hothorn T, Bretz F, Westfall P (2008) Simultaneous Inference in General Parametric Models. Biom J 50:346–363
IUCN. International Union for Conservation of Nature (2017) The IUCN Red List of Threatened Species (cited 2017 December) Accessed on: http://www.iucnredlist.org/details/summary/3036/0.
Jansen AM, Xavier SCC, Roque ALR (2015) The multiple and complex and changeable scenarios of the Trypanosoma cruzi transmission cycle in the sylvatic environment. Acta Trop 151:1–15. https://doi.org/10.1016/j.actatropica.2015.07.018
Kading RC, Borland EM, Cranfield M, Powers AM (2013) Prevalence of antibodies to alphaviruses and flaviviruses in free-ranging game animals and nonhuman primates in the greater Congo basin. J Wildl Dis 49:587–599. https://doi.org/10.7589/2012-08-212
Lara-Ruiz P, Chiarello AG (2005) Life-history traits and sexual dimorphism of the Atlantic forest maned sloth Bradypus torquatus (Xenarthra: Bradypodidae). J Zool 267:63–73. https://doi.org/10.1017/s0952836905007259
Laroque PO, Valença-Montenegro MM, Ferreira DRA, Chiang JO, Cordeiro MT, Vasconcelos PFC, Silva JCR (2014) Epidemiologic survey for arbovirus in galician capuchin monkeys (Cebus flavius) free living in Paraíba and captive capuchin monkey (Cebus libidinosus) from northeast Brazil. Pesqui Veterinária Bras 34:462–468. https://doi.org/10.1590/s0100-736x2014000500013
Lawrence D, Brown, T, Tony Cai, Anirban DasGupta (2001) Interval Estimation for a Binomial Proportion. In: Statistical Science, 2 (may, 2001). pp 101–117
Lima MA, Romano-Lieber NS, Duarte AMR de C (2010) Circulation of antibodies against yellow fever virus in a simian population in the area of Porto Primavera Hydroelectric Plant, São Paulo, Brazil. Rev Inst Med Trop São Paulo 52:11–16. https://doi.org/10.1590/s0036-46652010000100002
Mb P, A R, Rocha TC da, Cg E, Silva MAN da, Ks W, N J, Gr S, Oc J, Fern P, Vasconcelos o da C (2015) Serosurvey of Arbovirus in Free-Living Non-Human Primates (Sapajus spp.) in Brazil. Journal of Environmental Analytical Chemistry. https://doi.org/10.4172/2380-2391.1000155
Medlin S, Deardorff ER, Hanley CS, Vergneau-Grosset C, Siudak-Campfield A, Dallwig R, Travassos da Rosa A, Tesh RB, Pia Martin M, Weaver SC, Vaughan C, Ramirez O, Sladky KK, Paul-Murphy J (2016) Serosurvey of selected arboviral pathogens in free-ranging, two-toed sloths (Choloepus hoffmanni) and three-toed sloths (Bradypus variegatus) in Costa Rica, 2005–2007. J Wildl Dis 52:883–892. https://doi.org/10.7589/2015-02-040
Melo MSS, Barreto FR, Costa M da CN, Morato VC, Teixeira MG (2010) Progression of dengue virus circulation in the State of Bahia, Brazil, 1994–2000. Rev Soc Bras Med Trop 43:139–144. https://doi.org/10.1590/s0037-86822010000200007
Miller KE, Dietz JM (2006) Effects of Individual and Group Characteristics on Feeding Behaviors in Wild Leontopithecus rosalia. Int J Primatol 26:1291–1319. https://doi.org/10.1007/s10764-005-8854-7
Morales MA, Fabbri CM, Zunino GE, Kowalewski MM, Luppo VC, Enri DA, Levis SC, Caldero GE (2017) Detection of the mosquito-borne flaviviruses, West Nile, Dengue, Saint Louis Encephalitis, Ilheus, Bussuquara, and Yellow Fever in free ranging black howlers (Alouatta caraya) of Northeastern Argentina PLoS Negl Trop Dis 10:. https://doi.org/10.1371/journal.pntd.0005351
Moreira GV, Peixoto CMS, Ziccardi M, Oliveira RL, Castro MG, Dionisio DF, Pissinatti A (2000) Prevalência de Trypanosoma cruzi, Trypanosoma minasense e de anticorpos contra arbovírus em primatas não humanos (Callithrichidae) em cativeiro. Rev Bras Med Vet 22:252–254
Moreno ES, Spinola R, Tengan CH, Brasil RA, Siciliano MM, Coimbra TLM, Silveira VR, Rocco IM, Bisordi I, Souza RP de, Petrella S, Pereira LE, Maeda AY, Silva FG da, Suzuki A (2013) Yellow fever epizootics in non-human primates, São Paulo state, Brazil, 2008–2009. Rev Inst Med Trop São Paulo 55:45–50. https://doi.org/10.1590/s0036-46652013000100008
Nakgoi K, Nitatpattana N, Wajjwalku W, Pongsopawijit P, Kaewchot S, Yoksan S, Siripolwat V, Souris M, Gonzalez J-P (2014) Dengue, Japanese encephalitis and Chikungunya virus antibody prevalence among captive monkey (Macaca nemestrina) colonies of Northern Thailand. Am J Primatol 76:97–102. https://doi.org/10.1002/ajp.22213
Oliveira LC, Neves LG, Raboy BE, Dietz JM (2011) Abundance of Jackfruit (Artocarpus heterophyllus) Affects Group Characteristics and Use of Space by Golden-Headed Lion Tamarins (Leontopithecus chrysomelas) in Cabruca Agroforest. Environ Manage 48:248–262. https://doi.org/10.1007/s00267-010-9582-3
Oliver WLR, Santos IB (1991) Threatened endemic mammals of the Atlantic forest region of south-east Brazil. Jersey Wildlife Preservation Trust
Omatsu T, Moi ML, Takasaki T, Nakamura S, Katakai Y, Tajima S, Ito M, Yoshida T, Saito A, Akari H, Kurane I (2012) Changes in hematological and serum biochemical parameters in common marmosets (Callithrix jacchus) after inoculation with dengue virus. J Med Primatol 41:289–296. https://doi.org/10.1111/j.1600-0684.2012.00552.x
Pautasso A, Desiato R, Bertolini S, Vitale N, Radaelli MC., Mancini M, Rizzo F, Mosca A, Calzolari M, Prearo M, Mandola Ml., Maurella C, Mignone W, Chiavacci L, Casalone C (2013) Mosquito Surveillance in Northwestern Italy to Monitor the Occurrence of Tropical Vector-Borne Diseases. Transbound Emerg Dis 60:154–161. https://doi.org/10.1111/tbed.12123
Pereira LE, Suzuki A, Coimbra TLM, Souza RP de, Chamelet ELB (2001) Ilheus arbovirus in wild birds (Sporophila caerulescens and Molothrus bonariensis). Rev Saúde Pública 35:119–123. https://doi.org/10.1590/s0034-89102001000200003
R Core team R: A language and environment for statistical computing. In: R Found. Stat. Comput. Vienna Austria. Accessed on http://www.R-project.org
Reed, LJ, Muench, H (1938) A simple method of estimating fifty percent end points. Amer J Hyg 27:493–497
Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021
Rodrigues SG, Oliva OP, Araujo FAA, Martins LC, Chiang JO, Henriques DF, Silva EVP, Rodrigues DSG, Prazeres ASC, Tavares-Neto J, Vasconcelos PFC (2010) Epidemiologia do vírus da Encefalite de Saint Louis na Amazônia brasileira e no Estado do Mato Grosso do Sul, Brasil: elevada prevalência de anticorpos em equinos. Rev Pan-Amaz Saúde 1:81–86. https://doi.org/10.5123/s2176-62232010000100012
Seymour C, Peralta PH, Montgomery GG (1983a) Serologic evidence of natural togavirus infections in Panamanian sloths and other vertebrates. Am J Trop Med Hyg 32:854–861
Seymour C, Peralta PH, Montgomery GG (1983b) Viruses isolated from Panamanian sloths. Am J Trop Med Hyg 32:1435–1444
Sollberg I, Schiavetti A, Moraes MEB (2014) Agricultural management in the una’s wildlife refuge: a perspective of conservation by agroforestry. Rev Árvore 38:241–250. https://doi.org/10.1590/s0100-67622014000200004
Svoboda WK, Martins LC, Malanski LS, Shiozawa MM, Spohr KAH, Hilst CLS, Aguiar LM, Ludwig G, Passos FC, Silva LR, Headley SA, Navarro IT, Svoboda WK, Martins LC, Malanski LS, Shiozawa MM, Spohr KAH, Hilst CLS, Aguiar LM, Ludwig G (2014) Serological evidence for Saint Louis encephalitis virus in free-ranging New World monkeys and horses within the upper Paraná River basin region, Southern Brazil. Rev Soc Bras Med Trop 47:280–286. https://doi.org/10.1590/0037-8682-0083-2014
Tauro L, Marino B, Diaz LA, Lucca E, Gallozo D, Spinsanti L, Contigiani M (2012) Serological detection of St. Louis encephalitis virus and West Nile virus in equines from Santa Fe, Argentina. Mem Inst Oswaldo Cruz 107:553–556. https://doi.org/10.1590/s0074-02762012000400019
Teixeira MG, Barreto ML, Costa MCN, Ferreira LDA, Vasconcelos PF, Cairncross S (2002) Dynamics of dengue virus circulation: a silent epidemic in a complex urban area. Trop Med and Int Health7(9):757-762
Thompson NN, Auguste AJ, Coombs D, Blitvich BJ, Carrington CVF, Rosa APT, Wang E, Chadee DD, Drebot MA, Tesh RB, Weaver SC, Adesiyun AA (2012) Serological Evidence of Flaviviruses and Alphaviruses in Livestock and Wildlife in Trinidad. Vector Borne Zoonotic Dis 12:969–978. https://doi.org/10.1089/vbz.2012.0959
Tranquilin MV, Lehmkuhl RC, Maron A, Silva LR da, Ziliotto L, Seki MC, Salomon GR, Carrasco A de OT, Tranquilin MV, Lehmkuhl RC, Maron A, Silva LR da, Ziliotto L, Seki MC, Salomon GR, Carrasco A de OT (2013) First report of yellow fever virus in non-human primates in the State of Parana, Brazil. Rev Soc Bras Med Trop 46:522–524. https://doi.org/10.1590/0037-8682-0106-2013
Vasconcelos PF da C (2010) Yellow fever in Brazil: thoughts and hypotheses on the emergence in previously free areas. Rev Saúde Pública 44:1144–1149. https://doi.org/10.1590/s0034-89102010005000046
Vasconcelos PFC, Calisher CH (2016) Emergence of Human Arboviral Diseases in the Americas, 2000–2016. Vector Borne Zoonotic Dis Larchmt N 16:295–301. https://doi.org/10.1089/vbz.2016.1952
Vasconcelos PFC, Rosa AAPT, Rodrigues SG, Rosa SET, Dégallier N, Rosa SJFT (2001) Inadequate management of natural ecosystem in the Brazilian Amazon region results in the emergence and reemergence of arboviruses. Cad Saúde Pública 17:S155–S164. https://doi.org/10.1590/s0102-311x2001000700025
Vaz SM (2005) Mamíferos colecionados pelo Serviço de Estudos e Pesquisas sobre a Febre Amarela nos municípios de Ilhéus e Buerarema, estado da Bahia, Brasil. Arq Mus Nac 63:21–28
Vorou R (2016) Zika virus, vectors, reservoirs, amplifying hosts, and their potential to spread worldwide: what we know and what we should investigate urgently. Int J Infect Dis. 48:85–90. https://doi.org/10.1016/j.ijid.2016.05.014
Weaver SC (2013) Urbanization and geographic expansion of zoonotic arboviral diseases: mechanisms and potential strategies for prevention. Trends Microbiol 21:360–363. https://doi.org/10.1016/j.tim.2013.03.003
Weaver SC, Reisen WK (2010) Present and future arboviral threats. Antiviral Res 85:328–345. https://doi.org/10.1016/j.antiviral.2009.10.008
Zarnke RL, Calisher CH, Kerschner J (1983) Serologic evidence of arbovirus infections in humans and wild animals in Alaska. J Wildl Dis 19:175–179
Acknowledgements
The authors thank the important contributions of the Municipal and Bahia State Health Department and the colleagues from the Evandro Chagas Institute for assistance with the laboratory diagnostics and logistical support in the field. Additional thanks go to Project BioBrasil/Centre for Research and Conservation, ICMBio and the Bicho-da mata NGO for their logistical support and ICMBio for permits to conduct research in the Una Biological Reserve and Una Wildlife Refuge. We also thank the owners of the private areas (Almada, Santa Rita, Ribeiro, Ozawa, Manoel Rosa and São José, Ecoparque de Una, Bonfim) and the Zoobotanical Reserve Rehabilitation Center for permit to conduct the research. We also thank the sponsoring institutions that made this project possible: Saint Louis Zoo WildCare Institute (USA), The Wild Animal Fund, from the American Association of Zoological Veterinarians (USA), CNPq (Brazil), the Center for Research and Conservation of the Royal Zoological Society of Antwerp (Belgium), Lion Tamarins of Brazil Fund, National Lottery of Belgium, Primate Action Fund, Zoological Society of London, Conservação Internacional, Fundação o Boticário de Proteção a Natureza. The Flemish Ministry of Science (Belgium) provided structural support to the Center for Research and Conservation of the Royal Zoological Society of Antwerp.
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Catenacci, L.S., Ferreira, M., Martins, L.C. et al. Surveillance of Arboviruses in Primates and Sloths in the Atlantic Forest, Bahia, Brazil. EcoHealth 15, 777–791 (2018). https://doi.org/10.1007/s10393-018-1361-2
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DOI: https://doi.org/10.1007/s10393-018-1361-2