Skip to main content Accessibility help
×
Home

Spatiotemporal distribution of a non-haematophagous bat community and rabies virus circulation: a proposal for urban rabies surveillance in Brazil

  • R. A. Dias (a1), F. Rocha (a1), F. M. Ulloa-Stanojlovic (a1), A. Nitsche (a2), C. Castagna (a2), T. de Lucca (a3) and R. C. A. Rodrigues (a2)...

Abstract

In Brazil, rabies surveillance is based on monitoring domestic and wild animals, although the most prevalent lineage of the rabies virus (RABV) currently diagnosed in Brazil is associated with bats, particularly non-haematophagous bats. Disease control is based on the mass vaccination of dogs and cats. We used data collected by the passive surveillance system of the city of Campinas from 2011 to 2015, to describe the temporal and geographic distributions of the bat specimens and RABV and discuss the current rabies surveillance with the advent of the declaration of canine and feline rabies-free areas in Brazil. We described the species, locations and health statuses of the collected bat specimens. Moreover, all samples were submitted for RABV diagnosis. Then, we performed a time series decomposition for each bat family. Additionally, we determined the spatiotemporal relative risk for RABV infection using the ratio of the kernel-smoothed estimates of spatiotemporal densities of RABV-positive and RABV-negative bats. From the 2537 bat specimens, the most numerous family was Molossidae (72%), followed by Vespertilionidae (14%) and Phyllostomidae (13%). The bat families behaved differently in terms of seasonal and spatial patterns. The distribution of bats varied geographically in the urban environment, with Molossidae and Phyllostomidae being observed downtown and Vespertilionidae being observed in peripheral zones. Concurrently, a significant relative risk of RABV infection was observed downtown for Vespertilionidae and in peripheral zones for Molossidae. No RABV-positive sample clusters were observed. As a result of the official declaration of RABV-free areas in southern Brazil, mass dog and cat vaccinations are expected to halt in the near future. This stoppage would make most dog and cat populations susceptible to other RABV lineages, such as those maintained by non-haematophagous bats. In this scenario, all information available on bats and RABV distribution in urban areas is essential. Currently, few studies have been conducted. Some local health authorities, such as that in Campinas, are spontaneously basing their surveillance efforts on bat rabies, which is the alternative in reality scenario of increased susceptibility to bat-associated RABV that is developing in Brazil.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Spatiotemporal distribution of a non-haematophagous bat community and rabies virus circulation: a proposal for urban rabies surveillance in Brazil
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Spatiotemporal distribution of a non-haematophagous bat community and rabies virus circulation: a proposal for urban rabies surveillance in Brazil
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Spatiotemporal distribution of a non-haematophagous bat community and rabies virus circulation: a proposal for urban rabies surveillance in Brazil
      Available formats
      ×

Copyright

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.

Corresponding author

Author for correspondence: R. A. DIAS, E-mail: dias@vps.fmvz.usp.br

References

Hide All
1.Jung, K and Threlfall, CG (2016) Urbanisation and its effects on bats – a global meta-analysis. In Voigt, CC and Kingston, T (eds), Bats in the Anthropocene: Conservation of Bats in a Changing World. New York: Springer, pp. 1333.
2.Jung, K and Threlfall, CG (2018) Trait-dependent tolerance of bats to urbanization: a global meta-analysis. Proceedings of the Royal Society B 285, 20181222.
3.Russo, D and Ancillotto, L (2015) Sensitivity of bats to urbanization: a review. Mammalian Biology – Zeitschrift für Säugetierkunde 80, 205212.
4.Nogueira, MR et al. (2014) Checklist of Brazilian bats, with comments on original records. Check List (Luis Felipe Toledo) 10, 808821.
5.Nunes, H, Rocha, FL and Cordeiro-Estrela, P (2017) Bats in urban areas of Brazil: roosts, food sources and parasites in disturbed environments. Urban Ecosystems 20, 953969.
6.Calisher, CH et al. (2006) Bats: important reservoir hosts of emerging viruses. Clinical Microbiology Reviews 19, 531545.
7.Kesslar, MK et al. (2018) Changing resource landscapes and spillover of henipaviruses. Annals of the New York Academy of Sciences 1429, 7899.
8.United Nations, Department of Economic and Social Affairs, Population Division (2017) World population prospects: the 2017 revision, key findings and advance tables. Working Paper ESA/P/WP/248. New York: UN.
9.Cabral, CC et al. (2012) Circulation of the rabies virus in non-hematophagous bats in the city of Rio de Janeiro, Brazil, during 2001–2010. Revista da Sociedade Brasileira de Medicina Tropical de São Paulo 45, 180183.
10.World Health Organization (2013) Expert Consultation on Rabies: Second Report. WHO technical report series: 982. Geneva: WHO.
11.Favoretto, SR et al. (2002) Antigenic typing of Brazilian rabies virus samples isolated from animals and humans, 1989–2000. Revista da Sociedade Brasileira de Medicina Tropical de São Paulo 44, 9195.
12.Fisher, CR, Streicker, DG and Schnell, MJ (2018) The spread and evolution of rabies virus: conquering new frontiers. Nature Reviews Microbiology 16, 241255.
13.Sodré, MM, Gama, AR and Almeida, MF (2010) Updated list of bat species positive for rabies in Brazil. Revista da Sociedade Brasileira de Medicina Tropical de São Paulo 52, 7581.
14.Secretaria de Vigilância em Saúde (2009) Guia de Vigilância Epidemiológica, 7th Edn. Brasília: Ministério da Saúde (http://bvsms.saude.gov.br/bvs/publicacoes/guia_vigilancia_epidemiologica_7ed.pdf). Accessed 24 October 2017.
15.De Lucca, T et al. (2013) Assessing the rabies control and surveillance systems in Brazil: an experience of measures toward bats after the halt of massive vaccination of dogs and cats in Campinas, Sao Paulo. Preventive Veterinary Medicine 111, 126133.
16.Instituto Brasileiro de Geografia e Estatística (2010) Censo demográfico 2010 – Características da população e dos domiciílios – Resultados do universo. Brasília: Ministério do Planejamento (https://censo2010.ibge.gov.br). Accessed 24 October 2017.
17.De Lucca, T et al. (2017) Surveillance and control of rabies after detecting a positive case in feline in Campinas, São Paulo, Brazil. Boletim Epidemiológico Paulista 14, 2937.
18.Gehrt, SD and Chelsvig, JE (2004) Species-specific patterns of bat activity in an urban landscape. Ecological Applications 14, 625635.
19.Lindott, PR et al. (2016) Differential responses of cryptic bat species to the urban landscape. Ecology and Evolution 6, 20442052.
20.Hale, JD et al. (2015) The ecological impact of city lighting scenarios: exploring gap crossing thresholds for urban bats. Global Change Biology 21, 24672478.
21.Hariono, B, Ng, J and Sutton, RH (1993) Lead concentration in tissues of fruit bats (Pterous sp.) in urban and non-urban locations. Wildlife Research 20, 315319.
22.de Mattos, CA et al. (2000) Bat rabies in urban centers in Chile. Journal of Wildlife Diseases 36, 231240.
23.Botelho, NS et al. (2012) Candida species isolated from urban bats of Londrina-Paraná, Brazil and their potential virulence. Zoonoses and Public Health 59, 1622.
24.Bessa, TAF et al. (2010) The contribution of bats to leptospirosis transmission in Sao Paulo city, Brazil. The American Journal of Tropical Medicine and Hygiene 82, 315317.
25.Kunz, TH and Parsons, S (2009) Ecological and Behavioral Methods for the Study of Bats, 2nd Edn. Baltimore: Johns Hopkins University Press.
26.Neuweiler, G (2000) Biology of Bats. Oxford: Oxford University Press.
27.Kunz, TH and Fenton, MB (eds) (2003) Bat Ecology. Chicago: University of Chicago Press.
28.Reis, NR et al. (eds) (2007) Morcegos do Brasil. Londrina: Universidade Estadual de Londrina.
29.Myers, P et al. The Animal Diversity Web (http://animaldiversity.org). Accessed 24 October 2017.
30.Rowlinson, B and Diggle, P (2016) Splancs: spatial and space-time point pattern analysis. R package version 2.01-39. (https://CRAN.R-project.org/package=splancs). Accessed 24 October 2017.
31.Secretaria Municipal de Planejamento e Urbanismo (2017) Zoneamento do município de Campinas. Campinas: Prefeitura de Campinas (http://zoneamento.campinas.sp.gov.br). Accessed 17 April 2018.
32.Davies, TM, Marshall, JC and Hazelton, ML (2018) Tutorial on kernel estimation of continuous spatial and spatiotemporal relative risk. Statistics in Medicine 37, 11911221.
33.Kobayashi, Y et al. (2005) Molecular epidemiological analysis of bat rabies virus in Brazil. Journal of Veterinary Medical Science 67, 647652.
34.Fahl, WO et al. (2012) Desmodus rotundus and Artibeus spp. bats might present distinct rabies virus lineages. Brazilian Journal of Infectious Diseases 16, 545551.
35.Woods, M, McDonald, RA and Harris, S (2003) Predation of wildlife by domestic cats Felis catus in Great Britain. Mammal Review 33, 174188.
36.Loss, SR, Will, T and Marra, PP (2013) The impact of free-ranging domestic cats on wildlife of the United States. Nature Communications 4, 1396.
37.Asif, N, Malik, MF and Chaudhry, FN (2018) A review of on environmental pollution bioindicators. Pollution 4, 111118.
38.Bayat, S et al. (2014) Organic contaminants in bats: trends and new issues. Environment International 63, 4052.
39.Lacoeuilhe, A et al. (2014) The influence of low intensities of light pollution on bat communities in a semi-natural context. PLoS One 9, e103042.
40.Esbérard, C (2002) Composition of colony and reproduction of Molossus rufus (E. Geoffroy) (Chiroptera, Molossidae) in roost at Southeastern Brazil. Revista Brasileira de Zoologia 19, 11531160.
41.Wohlgenant, T (1994) Roost interactions between the common vampire bat (Desmodus rotundus) and two frugivorous bats (Phyllostomus discolor and Sturnira lilium) in Guanacaste, Costa Rica. Biotropica 26, 344348.
42.Avila-Flores, R, Flores-Martins, JJ and Ortega, J (2002) Nyctinomops laticaudatus. Mammalian Species 697, 16.
43.Voigt, CC and Kelm, DH (2006) Host preference of the common vampire bat (Desmodus rotundus; Chiroptera) assessed by stable isotopes. Journal of Mammalogy 87, 16.
44.Castilho, JG et al. (2010) A comparative study of rabies isolates from hematophagous bats in Brazil. Journal of Wildlife Diseases 46, 13351339.
45.Streicker, DG et al. (2012) Ecological and anthropogenic drivers of rabies exposure in vampire bats: implications for transmission and control. Proceedings of the Royal Society B 279, 33843392.
46.Hristov, NI et al. (2010) Seasonal variation in colony size of Brazilian free-tailed bats at Carlsbad cavern based on thermal imaging. Journal of Mammalogy 91, 183192.
47.Constantine, DG et al. (1968) Rabies in New Mexico cavern bats. Public Health Reports 83, 303316.
48.Turmelle, AS et al. (2010) Ecology of rabies virus exposure in colonies of Brazilian free-tailed bats (Tadarida brasiliensis) at natural and man-made roosts in Texas. Vector-Borne and Zoonotic Diseases 10, 165175.
49.Almeida, EO et al. (2002) Combate ao Desmodus rotundus (E. Geoffroy, 1810) na região cárstica de Cordisburgo e Curvelo, Minas Gerais. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 54, 117126.
50.Pacheco, SM et al. (2010) Morcegos urbanos: status do conhecimento e plano de ação para conservação no Brasil. Chiroptera Neotropical 16, 629647.
51.Rojas, D et al. (2011) When did plants become important to leaf-nosed bats? Diversification of feeding habits in the family Phyllostomidae. Molecular Ecology 20, 22172228.
52.Muñoz-Romo, M, Herrera, EA and Knut, TH (2008) Roosting behaviour and group stability of the big fruit-eating bat Artibeus lituratus (Chiroptera: Phyllostomidae). Mammalian Biology 73, 214221.
53.American Society of Mammalogists. Mammalian Species (https://academic.oup.com/mspecies). Accessed 10 November 2017.

Keywords

Related content

Powered by UNSILO

Spatiotemporal distribution of a non-haematophagous bat community and rabies virus circulation: a proposal for urban rabies surveillance in Brazil

  • R. A. Dias (a1), F. Rocha (a1), F. M. Ulloa-Stanojlovic (a1), A. Nitsche (a2), C. Castagna (a2), T. de Lucca (a3) and R. C. A. Rodrigues (a2)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.