Into the woods: Changes in mosquito community composition and presence of key vectors at increasing distances from the urban edge in urban forest parks in Manaus, Brazil

doi:10.1016/j.actatropica.2020.105441

. 2020 Jun:206:105441.

doi: 10.1016/j.actatropica.2020.105441. Epub 2020 Mar 12.

Into the woods: Changes in mosquito community composition and presence of key vectors at increasing distances from the urban edge in urban forest parks in Manaus, Brazil

Adam Hendy ¹, Eduardo Hernandez-Acosta ², Bárbara Aparecida Chaves ³, Nelson Ferreira Fé ³, Danielle Valério ³, Claudia Mendonça ³, Marcus Vinícius Guimarães de Lacerda ³, Michaela Buenemann ⁴, Nikos Vasilakis ⁵, Kathryn A Hanley ⁶

Affiliations

¹ Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, Center for Tropical Diseases, Institute for Human Infection and Immunity, University of Texas Medical Branch, Galveston, TX 77555, USA.
² Department of Biology, New Mexico State University, Las Cruces, NM 88003, USA.
³ Fundação de Medicina Tropical Doutor Heitor Vieria Dourado, Manaus, AM 69040, Brazil.
⁴ Department of Geography, New Mexico State University, Las Cruces, NM 88003, USA.
⁵ Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, Center for Tropical Diseases, Institute for Human Infection and Immunity, University of Texas Medical Branch, Galveston, TX 77555, USA. Electronic address: nivasila@utmb.edu.
⁶ Department of Biology, New Mexico State University, Las Cruces, NM 88003, USA. Electronic address: khanley@nmsu.edu.

PMID: 32173316
PMCID: PMC7184314
DOI: 10.1016/j.actatropica.2020.105441

Into the woods: Changes in mosquito community composition and presence of key vectors at increasing distances from the urban edge in urban forest parks in Manaus, Brazil

Adam Hendy et al. Acta Trop. 2020 Jun.

. 2020 Jun:206:105441.

doi: 10.1016/j.actatropica.2020.105441. Epub 2020 Mar 12.

Authors

Adam Hendy ¹, Eduardo Hernandez-Acosta ², Bárbara Aparecida Chaves ³, Nelson Ferreira Fé ³, Danielle Valério ³, Claudia Mendonça ³, Marcus Vinícius Guimarães de Lacerda ³, Michaela Buenemann ⁴, Nikos Vasilakis ⁵, Kathryn A Hanley ⁶

Affiliations

¹ Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, Center for Tropical Diseases, Institute for Human Infection and Immunity, University of Texas Medical Branch, Galveston, TX 77555, USA.
² Department of Biology, New Mexico State University, Las Cruces, NM 88003, USA.
³ Fundação de Medicina Tropical Doutor Heitor Vieria Dourado, Manaus, AM 69040, Brazil.
⁴ Department of Geography, New Mexico State University, Las Cruces, NM 88003, USA.
⁵ Department of Pathology and Center for Biodefense and Emerging Infectious Diseases, Center for Tropical Diseases, Institute for Human Infection and Immunity, University of Texas Medical Branch, Galveston, TX 77555, USA. Electronic address: nivasila@utmb.edu.
⁶ Department of Biology, New Mexico State University, Las Cruces, NM 88003, USA. Electronic address: khanley@nmsu.edu.

PMID: 32173316
PMCID: PMC7184314
DOI: 10.1016/j.actatropica.2020.105441

Abstract

Mosquito-borne Zika virus (ZIKV) was recently introduced into the Americas and now has the potential to spill back into a sylvatic cycle in the region, likely involving non-human primates and Aedes, Haemagogus, and Sabethes species mosquitoes. We investigated potential routes of mosquito-borne virus exchange between urban and sylvatic transmission cycles by characterizing mosquito communities in three urban forest parks that receive heavy traffic from both humans and monkeys in Manaus, Brazil. Parks were stratified by both distance from the urban-forest edge (0, 50, 100, and 500 m) and relative Normalized Difference Vegetation Index (NDVI) (low, medium, or high), and mosquitoes were sampled at randomly selected sites within each stratum using BG-Sentinel traps. Additionally, temperature, relative humidity, and other environmental data were collected at each site. A total of 1,172 mosquitoes were collected from 184 sites sampled in 2018, of which 98 sites were resampled in 2019. Using park as the unit of replication (i.e. 3 replicates per sampling stratum), a two-way ANOVA showed no effect of distance or NDVI on the mean number of identified species (P > 0.05 for both comparisons) or on species diversity as measured by the Shannon-Wiener diversity index (P > 0.10 for both comparisons). However, the Morisita overlap index revealed that mosquito communities changed substantially with increasing distance from edge, with communities at 0 m and 500 m being quite distinct. Aedes albopictus and Ae. aegypti penetrated at least 100 m into the forest, while forest specialists including Haemagogus janthinomys, Sabethes glaucodaemon, and Sa. tridentatus were detected in low numbers within 100 m from the forest edge. Trichoprosopon digitatum and Psorophora amazonica were among the most abundant species collected, and both showed distributions extending from the forest edge to its interior. Our results show overlapping distributions of urban and forest mosquitoes at park edges, which highlights the risk of arbovirus exchange via multiple bridge vectors in Brazilian urban forest parks. These parks may also provide refugia for both Ae. albopictus and Ae. aegypti from mosquito control programs.

Keywords: Arbovirus; Forest edge; Mosquito; NDVI; Spillback; Zika virus.

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Conflict of interest statement

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

Fig 1.

Fig 1.

Map showing A) location of Manaus in Brazil, and B) location of urban forest parks in Manaus, with park boundaries highlighted in red. CIGS = Centro de Instrução de Guerra Na Selva; Mindu = Parque Municipal do Mindu; UFAM = Universidade Federal do Amazonas. The large natural reserve adjacent to Manaus, Reserva Florestal Adolpho Ducke, is also labeled.

Fig 2.

Fig 2.

Mean monthly temperature (red line) +/− 1 standard error (S.E.) in Manaus between January 2018 and June 2019, recorded at the INMET meteorological station ref. OMM: 82331 (Instituto Nacional de Meteorologia, 2019); cumulative monthly rainfall (blue bars) recorded at the CPRM station ref. 1499000 (Agência Nacional de Águas, 2019); and, mosquito sampling periods in 2018 and 2019.

Fig 3.

Fig 3.

Temperature (°C) and relative humidity (%) recorded at 30-minute intervals in each distance and NDVI category for the sampling duration based on 2018 BG-Sentinel trap collections.

Fig 4.

Fig 4.

Relative abundance of designated species collected using BG-Sentinel traps in the three parks at each distance sampled in 2018 (184 sites). Number of mosquitoes collected in each park at each distance listed at top of bar; 500m sites were only present at UFAM. Genus and subgenus abbreviations follow Reinert (2009); sp. = single species, spp. = potentially multiple species; *denotes species collected in 2018 only.

Fig 5.

Fig 5.

Mean number of mosquitoes +/− 1 standard error (S.E.) per site by month of collection (left columns) and percent of sites positive for mosquitoes by month of collection (right columns) based on 2018 BG-Sentinel trap collections, for A) and B) relatively abundant genera, and C) and D) relatively scarce genera (note different y-axes); bottom panels show months in which collections were made per park.

Fig 6.

Fig 6.

Mean number of A) Ae. albopictus and B) Ae. aegypti mosquitoes +/− 1 standard error (S.E.) per site by distance and NDVI across three parks (N = 3 values per mean) based on 2018 BG-Sentinel trap collections; note different axes for each species; 500m sites were only present at UFAM.

Fig 7.

Fig 7.

Mean number of mosquitoes +/− 1 standard error (S.E.) per site by distance and NDVI for Tr. digitatum and Ps. amazonica (N = 3 values per mean) based on 2018 BG-Sentinel trap collections; 500m sites were only present at UFAM.

See this image and copyright information in PMC

References

1. Agência Nacional de Águas, 2019. HIDROWEB - Sistema de informações hidrológicas. Accessed 19 July 2019 http://www.snirh.gov.br/hidroweb/publico/apresentacao.jsf
1. Althouse BM, Vasilakis N, Sall AA, Diallo M, Weaver SC and Hanley KA, 2016. Potential for Zika virus to establish a sylvatic transmission cycle in the Americas. PLoS Negl. Trop. Dis 10 (12), e0005055 10.1371/journal.pntd.0005055. - DOI - PMC - PubMed
1. Anderson CR, Aitken TH, Downs WG and Spence L, 1957. The isolation of St. Louis virus from Trinidad mosquitoes. Am. J. Trop. Med. Hyg 6 (4), 688–692. 10.4269/ajtmh.19576688. - DOI - PubMed
1. Arnell JH, 1973. Mosquito studies (Diptera, Culicidae) XXXII. A revision of the genus Haemagogus. Contrib. Am. Entomol. Inst 10 (2), 1–174.
1. Azar SR, Roundy CM, Rossi SL, Huang JH, Leal G, Yun R, et al., 2017. Differential vector competency of Aedes albopictus populations from the Americas for Zika virus. Am. J. Trop. Med. Hyg 97 (2), 330–339. 10.4269/ajtmh.16-0969. - DOI - PMC - PubMed

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[1] Agência Nacional de Águas, 2019. HIDROWEB - Sistema de informações hidrológicas. Accessed 19 July 2019 http://www.snirh.gov.br/hidroweb/publico/apresentacao.jsf

[2] Agência Nacional de Águas, 2019. HIDROWEB - Sistema de informações hidrológicas. Accessed 19 July 2019 http://www.snirh.gov.br/hidroweb/publico/apresentacao.jsf

[3] Althouse BM, Vasilakis N, Sall AA, Diallo M, Weaver SC and Hanley KA, 2016. Potential for Zika virus to establish a sylvatic transmission cycle in the Americas. PLoS Negl. Trop. Dis 10 (12), e0005055 10.1371/journal.pntd.0005055. - DOI - PMC - PubMed

[4] Althouse BM, Vasilakis N, Sall AA, Diallo M, Weaver SC and Hanley KA, 2016. Potential for Zika virus to establish a sylvatic transmission cycle in the Americas. PLoS Negl. Trop. Dis 10 (12), e0005055 10.1371/journal.pntd.0005055. - DOI - PMC - PubMed

[5] Anderson CR, Aitken TH, Downs WG and Spence L, 1957. The isolation of St. Louis virus from Trinidad mosquitoes. Am. J. Trop. Med. Hyg 6 (4), 688–692. 10.4269/ajtmh.19576688. - DOI - PubMed

[6] Anderson CR, Aitken TH, Downs WG and Spence L, 1957. The isolation of St. Louis virus from Trinidad mosquitoes. Am. J. Trop. Med. Hyg 6 (4), 688–692. 10.4269/ajtmh.19576688. - DOI - PubMed

[7] Arnell JH, 1973. Mosquito studies (Diptera, Culicidae) XXXII. A revision of the genus Haemagogus. Contrib. Am. Entomol. Inst 10 (2), 1–174.

[8] Arnell JH, 1973. Mosquito studies (Diptera, Culicidae) XXXII. A revision of the genus Haemagogus. Contrib. Am. Entomol. Inst 10 (2), 1–174.

[9] Azar SR, Roundy CM, Rossi SL, Huang JH, Leal G, Yun R, et al., 2017. Differential vector competency of Aedes albopictus populations from the Americas for Zika virus. Am. J. Trop. Med. Hyg 97 (2), 330–339. 10.4269/ajtmh.16-0969. - DOI - PMC - PubMed

[10] Azar SR, Roundy CM, Rossi SL, Huang JH, Leal G, Yun R, et al., 2017. Differential vector competency of Aedes albopictus populations from the Americas for Zika virus. Am. J. Trop. Med. Hyg 97 (2), 330–339. 10.4269/ajtmh.16-0969. - DOI - PMC - PubMed

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Into the woods: Changes in mosquito community composition and presence of key vectors at increasing distances from the urban edge in urban forest parks in Manaus, Brazil

Affiliations

Into the woods: Changes in mosquito community composition and presence of key vectors at increasing distances from the urban edge in urban forest parks in Manaus, Brazil

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Medical