Divergent coronaviruses detected in wild birds in Brazil, including a central park in São Paulo

  • Carla M. Barbosa
  • Edison L. Durigon
  • Luciano M. Thomazelli
  • Tatiana Ometto
  • Roberta Marcatti
  • Marcello Shiavo Nardi
  • Daniel M. de Aguiar
  • João Batista Pinho
  • Maria Virginia Petry
  • Isaac Simão Neto
  • Patrícia Serafini
  • Roberta Costa Rodrigues
  • Severino Mendes de Azevedo Junior
  • Luiz Gustavo B. Góes
  • Jansen de AraujoEmail author
Veterinary Microbiology - Research Paper


Coronaviruses are single-stranded positive-sense RNA viruses associated with important avian diseases. Their relatively high rates of mutation and recombination frequencies allow them to adapt to new hosts and ecological niches. Although Brazil has 18% of global avian species diversity, studies regarding the presence of avian viral diseases in wild birds in South America are scarce. In this study, we performed a retrospective analysis of the presence of CoVs in 746 wild birds. Oropharyngeal and cloacal swabs were obtained and placed together in vials containing VTM transport medium collected in different regions of Brazil between 2006 and 2013. Screening for viral nucleic acid was performed using conventional RT-PCR and pancoronavirus nested PCR. Positive samples were characterized by partial sequencing of the RNA-dependent RNA polymerase (RdRp) gene, and ensuing phylogenetic analysis was performed to investigate the association between virus epidemiology and bird migration routes. Coronavirus RNA were detected and sequenced from six samples, in which three were related to gammacoronaviruses group and the other three to deltacoronavirus group. Our study documents the presence of CoVs related to avian gamma- and deltacoronaviruses circulating in both urban- and poultry-farm regions of Brazil, implicating wild birds as potential carriers of CoVs which may represent a risk to poultry farms and public health in Brazil.


Gammacoronavirus Deltacoronavirus Wild birds Brazil South America 



We thank the field logistic support of field team of Microbiology Department, University of São Paulo, Wildlife Department of São Paulo (DEPAVE), and Laboratory of Ornithology and Marine Animals (LOAM), Universidade do Vale do Rio dos Sinos. We thank Diogo Fiori Ribas, Edna Maria Gomes Cavalcante, and Hiroe. Positive control was kindly provided by Professor Paulo Brandão at the Department of Preventive Veterinary Medicine and Animal Health, School of Veterinary Medicine, University of São Paulo.


This work was supported by the Fundacão de Amparo a Pesquisa do Estado de São Paulo (FAPESP) (grant numbers 2009/05994-9, 2011/13821-7, 2011/11006-0, 2013/05485-2, 2014/03172-0); the Conselho Nacional de Desenvolvimento a Pesquisa (CNPq) (grant number 477912/2007-9]; CAPES/Newton Foundation (grant number 99999.005126/2015-00); Fundação de Amparo a Pesquisa do Estado do Rio Grande do Sul (FAPERGS No. 09/0574-7); and Wildlife Conservation Society (CWS No. 2008-05 and 2009-05).

Compliance with ethical standards

Conflict of interest

The authors declared that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The procedures involving wild birds were approved by the Brazilian Society of Laboratory Animal Science (SBCAL) of the University of São Paulo, São Paulo, Brazil (protocol number 105/pg.74/book2) and licensed by the Chico Mendes Institute for Biodiversity Conservation (ICMBio/SISBIO), Ministry of the Environment (MMA), under protocol numbers 201/2006 CGFAU, 25895-1, 33602-1, 17565-1, and 14966-11.

Supplementary material

42770_2019_65_MOESM1_ESM.pdf (55 kb)
ESM 1 (PDF 54.7 kb)


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Copyright information

© Sociedade Brasileira de Microbiologia 2019

Authors and Affiliations

  • Carla M. Barbosa
    • 1
  • Edison L. Durigon
    • 1
  • Luciano M. Thomazelli
    • 1
  • Tatiana Ometto
    • 1
  • Roberta Marcatti
    • 2
  • Marcello Shiavo Nardi
    • 2
  • Daniel M. de Aguiar
    • 3
  • João Batista Pinho
    • 4
  • Maria Virginia Petry
    • 5
  • Isaac Simão Neto
    • 6
  • Patrícia Serafini
    • 7
  • Roberta Costa Rodrigues
    • 8
  • Severino Mendes de Azevedo Junior
    • 9
  • Luiz Gustavo B. Góes
    • 1
  • Jansen de Araujo
    • 1
    Email author
  1. 1.Institute of Biomedical SciencesUniversity of Sao PauloSão PauloBrazil
  2. 2.Wildlife and Green Areas DepartmentSão Paulo MunicipalitySão PauloBrazil
  3. 3.Laboratório de Virologia e Rickettsioses, Hospital VeterinárioUniversidade Federal de Mato GrossoCuiabáBrazil
  4. 4.Laboratório de Ecologia de Aves, Instituto de BiociênciasUniversidade Federal de Mato GrossoCuiabáBrazil
  5. 5.Universidade do Vale do Rio dos Sinos (UNISINOS)São LeopoldoBrazil
  6. 6.Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio)BrasíliaBrazil
  7. 7.Centro Nacional de Pesquisa e Conservação de Aves Silvestres (CEMAVE)CabedeloBrazil
  8. 8.Universidade Federal da Paraíba (UFPB)João PessoaBrazil
  9. 9.Universidade Federal Rural de Pernambuco (UFRPE)RecifeBrazil

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