Distribution of bat-borne viruses and environment patterns

Aneta Afelt, Audrey Lacroix, Urszula Zawadzka-Pawlewska, Wojciech Pokojski, Philippe Buchy, Roger Frutos, Aneta Afelt, Audrey Lacroix, Urszula Zawadzka-Pawlewska, Wojciech Pokojski, Philippe Buchy, Roger Frutos

Abstract

Environmental modifications are leading to biodiversity changes, loss and habitat disturbance. This in turn increases contacts between wildlife and hence the risk of transmission and emergence of zoonotic diseases. We analyzed the environment and land use using remote spatial data around the sampling locations of bats positive for coronavirus (21 sites) and astrovirus (11 sites) collected in 43 sites. A clear association between viruses and hosts was observed. Viruses associated to synanthropic bat genera, such as Myotis or Scotophilus were associated to highly transformed habitats with human presence while viruses associated to fruit bat genera were correlated with natural environments with dense forest, grassland areas and regions of high elevation. In particular, group C betacoronavirus were associated with mosaic habitats found in anthropized environments.

Keywords: Bat viruses; Cambodia; Emerging diseases; Environmental analysis; Evolution of environment; Lao PDR; South East Asia.

Copyright © 2017 Elsevier B.V. All rights reserved.

Figures

Graphical abstract
Graphical abstract
Fig. 1
Fig. 1
Location of the sampling points in Cambodia and Lao PDR. White circle: Sites with coronavirus- and astrovirus-negative bats. Red circle: Sites with both coronavirus- and astrovirus-positive bats. Blue circle: Sites with astrovirus-positive bats only. Yellow circle: Sites with coronavirus-positive bats only. Dark green: Forest; light green: grassland; orange: cropland; red: human settlements; blue: wetland; dark blue: water. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 2
Fig. 2
Closer landscape view of the areas of interest. White circle: Sites with coronavirus- and astrovirus-negative bats. Red circle: Sites with both coronavirus- and astrovirus-positive bats. Blue circle: Sites with astrovirus-positive bats only. Yellow circle: Sites with coronavirus-positive bats only. Dark green: forest; light green: grassland; orange: cropland; red: human settlements; blue: wetland; dark blue: water. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 3
Fig. 3
Hierarchical classification of landscapes and definition of areas of interest (AOI). Orange: cropland; dark green: forest; light green: grassland; red: human settlements; blue: wetland; dark blue: water. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 4
Fig. 4
Principal component analysis of the distribution of viruses with respect to environment types. a. Distribution of coronaviruses. b. Distribution of astroviruses.
Fig. 5
Fig. 5
Principal component analysis of the distribution of bats genera with respect to environment types.

References

    1. Achard F., Eva H.D., Stibig H.J., Mayaux P., Gallego J., Richards T., Malingreau J.P. Determination of deforestation rates of the world's humid tropical forests. Science. 2002;297:999–1002.
    1. Bates P., Bumrungsri S., Francis C., Csorba G. Hipposideros armiger. IUCN Red List Threat. Species 2008 ET10110A3162617. 2008. Available: (WWW Document)
    1. Bates P., Kingston T., Francis C., Rosell-Ambal G., Heaney L., Gonzales J.C., Molur S., Srinivasulu C. Scotophilus kuhlii. IUCN Red List Threat. Species 2008 ET20068A9142479. 2008. Available: (WWW Document)
    1. Calisher C.H., Childs J.E., Field H.E., Holmes K.V., Schountz T. Bats: important reservoir hosts of emerging viruses. Clin. Microbiol. Rev. 2006;19:531–545.
    1. Chhay S. Cambodian bats: a review of farming practices and economic value of lesser Asiatic yellow house bat Scotophilus kuhlii (Leach, 1821), in Kandal and Takeo Provinces, Cambodia. Camb. J. Nat. Hist. 2012;2012:164.
    1. Chu D.K.W., Poon L.L.M., Guan Y., Peiris J.S.M. Novel astroviruses in insectivorous bats. J. Virol. 2008;82:9107–9114.
    1. Chua K.B., Bellini W.J., Rota P.A., Harcourt B.H., Tamin A., Lam S.K., Ksiazek T.G., Rollin P.E., Zaki S.R., Shieh W.J., Goldsmith C.S., Gubler D.J., Roehrig J.T., Eaton B., Gould A.R., Olson J., Field H., Daniels P., Ling A.E., Peters C.J., Anderson L.J., Mahy B.W.J. Nipah virus: a recently emergent deadly paramyxovirus. Science. 2000;288:1432–1435.
    1. Clare E.L., Lim B.K., Fenton M.B., Hebert P.D.N. Neotropical bats: estimating species diversity with DNA barcodes. PLoS One. 2011;6
    1. Costenbader J., Broadhead J., Yasmi Y., Durst P.B. FAO, USAID and LEAF; Bangkok: 2015. Drivers Affecting Forest Change in the Greater Mekong Subregion (GMS): An Overview.
    1. Csorba G., Bates P., Furey N., Bumrungsri S., Molur S., Srinivasulu C. Pipistrellus coromandra (Coromandel Pipistrelle, Indian Pipistrelle, Little Indian Bat). IUCN Red List Threat. Species 2008 ET17335A6996860. 2008. Available:
    1. DeFries R.S., Rudel T., Uriarte M., Hansen M. Deforestation driven by urban population growth and agricultural trade in the twenty-first century. Nat. Geosci. 2010;3:178–181.
    1. Field H.E. Bats and emerging zoonoses: henipaviruses and SARS. Zoonoses Public Health. 2009;56:278–284.
    1. Flemming T.H., Eby P. Ecology of bat migration. In: Kunz T.H., Fenton M.B., editors. Bat Ecology. University of Chicago Press; Chicago: 2003. pp. 156–208.
    1. Flint E.P. Changes in land use in South and Southeast Asia from 1880 to 1980: a data base prepared as part of a coordinated research program on carbon fluxes in the tropics. Chemosphere. 1994;29:1015–1062.
    1. Food and Agriculture Organization, World Bank Forest area (% of land area) 2016. Available:
    1. Fortin M.J., Keitt T.H., Maurer B.A., Taper M.L., Kaufman D.M., Blackburn T.M. Species' geographic ranges and distributional limits: pattern analysis and statistical issues. Oikos. 2005;108:7–17.
    1. Gay N., Olival K.J., Bumrungsri S., Siriaroonrat B., Bourgarel M., Morand S. Parasite and viral species richness of Southeast Asian bats: fragmentation of area distribution matters. Int. J. Parasitol. 2014;3:161–170.
    1. Han H.J., Wen H.L., Zhou C.M., Chen F.F., Luo L.M., Liu J.W., Yu X.J. Bats as reservoirs of severe emerging infectious diseases. Virus Res. 2015;205:1–6.
    1. Henle K., Davies K.F., Kleyer M., Margules C., Settele J. Predictors of species sensitivity to fragmentation. Biodivers. Conserv. 2004;13:207–251.
    1. Hutson A.M., Suyanto A., Kingston T., Bates P., Francis C., Molur S., Srinivasulu C. Macroglossus sobrinus. IUCN Red List Threat. Species 2008 ET12595A3363666. 2008. Available:
    1. IUCN IUCN Red List of Threatened Species. Version 2.1 < >. 2017. Available:
    1. Jones K.E., Patel N.G., Levy M.A., Storeygard A., Balk D., Gittleman J.L., Daszak P. Global trends in emerging infectious diseases. Nature. 2008;451:990–993.
    1. Jung K., Threlfall C.G. Urbanisation and its effects on bats—a global meta-analysis. In: Voigt C.C., Kingston T., editors. Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer International Publishing; 2016. pp. 13–33.
    1. Kingston T. Research priorities for bat conservation in Southeast Asia: a consensus approach. Biodivers. Conserv. 2010;19:471–484.
    1. Korstian J.M., Hale A.M., Bennett V.J., Williams D.A. Using DNA barcoding to improve bat carcass identification at wind farms in the United States. Conserv. Genet. Resour. 2016;8:27–34.
    1. Kunz T.H., Fenton M.B. University of Chicago Press; 2005. Bat Ecology.
    1. Lacroix A., Duong V., Hul V., San S., Davun H., Omaliss K., Chea S., Hassanin A., Theppangna W., Silithammavong S., Khammavong K., Singhalath S., Greatorex Z., Fine A.E., Goldstein T., Olson S., Joly D.O., Keatts L., Dussart P., Afelt A., Frutos R., Buchy P. Genetic diversity of coronaviruses in bats in Lao PDR and Cambodia. Infect. Genet. Evol. 2017;48:10–18.
    1. Lacroix A., Duong V., Hul V., San S., Davun H., Omaliss K., Chea S., Hassanin A., Theppangna W., Silithammavong S., Khammavong K., Singhalath S., Afelt A., Greatorex Z., Fine A.E., Goldstein T., Olson S., Joly D.O., Keatts L., Dussart P., Frutos R., Buchy P. Diversity of bat astroviruses in Lao PDR and Cambodia. Infect. Genet. Evol. 2017;48:41–50.
    1. Lipkin W.I., Anthony S.J. Virus hunting. Virology. 2015;479:194–199.
    1. Meyer C.F.J., Fründ J., Lizano W.P., Kalko E.K.V. Ecological correlates of vulnerability to fragmentation in Neotropical bats. J. Appl. Ecol. 2008;45:381–391.
    1. Mildenstein T., Tanshi I., Racey P.A. Exploitation of bats for bushmeat and medicine. In: Voigt C.C., Kingston T., editors. Bats in the Anthropocene: Conservation of Bats in a Changing World. Springer International Publishing; 2016. pp. 325–375.
    1. Morse S.S. Public health surveillance and infectious disease detection. Biosecurity Bioterrorism Biodefense Strategy Pract. Sci. 2012;10:6–16.
    1. National Geomatics Center of China NGCC 30 meter Global Land Cover Dataset, product description. 2014.
    1. Olson J.G., Rupprecht C., Rollin P.E., An U.S., Niezgoda M., Clemins T., Walston J., Ksiazek T.G. Antibodies to Nipah-like virus in bats (Pteropus lylei), Cambodia. Emerg. Infect. Dis. 2002;8:987–988.
    1. Omrani A.S., Al-Tawfiq J.A., Memish Z.A. Middle East respiratory syndrome coronavirus (MERS-CoV): animal to human interaction. Pathog. Glob. Health. 2015;109:354–362.
    1. Osborne J.C., Rupprecht C.E., Olson J.G., Ksiazek T.G., Rollin P.E., Niezgoda M., Goldsmith C.S., An U.S., Nichol S.T. Isolation of Kaeng Khoi virus from dead Chaerephon plicata bats in Cambodia. J. Gen. Virol. 2003;8:2685–2689.
    1. Reynes J.M., Molia S., Audry L., Hout S., Ngin S., Walston J., Bourhy H. Serologic evidence of lyssavirus infection in bats, Cambodia. Emerg. Infect. Dis. 2004;10:2231–2234.
    1. Reynes J.M., Counor D., Ong S., Faure C., Seng V., Molia S., Walston J., Georges-Courbot M.C., Deubel V., Sarthou J.L. Nipah virus in Lyle's flying foxes, Cambodia. Emerg. Infect. Dis. 2005;11:1042–1047.
    1. Rosell-Ambal G., Tabaranza B., Heaney L., Gonzales J.C., Molur S., Srinivasulu C. Myotis horsfieldii. IUCN Red List Threat. Species 2008 ET14166A4413659. 2008. Available:
    1. Salaün J.J., Klein J.M., Hebrad G. A new virus, Phnom-Penh bat virus, isolated in Cambodia from a short-nosed fruit bat, Cynopterus brachyotis angulatus. Ann. Microbiol. Inst. Pasteur. 1974;125A:485–495.
    1. Save Cambodia's Wildlife . Save Cambodia's Wildlife; Phnom Penh: 2014. Atlas of Cambodia. Maps on Socio-economic Development and Environment.
    1. Sisouphanthong B., Taillard C. St. Martin's Press; 2000. Atlas of Laos: The Spatial Structures of Economic and Social Development of the Lao People's Democratic Republic.
    1. Smith A.C., Fahrig L., Francis C.M. Landscape size affects the relative importance of habitat amount, habitat fragmentation, and matrix quality on forest birds. Ecography. 2011;34:103–113.
    1. Sodhi N.S., Koh L.P., Brook B.W., Ng P.K.L. Southeast Asian biodiversity: an impending disaster. Trends Ecol. Evol. 2004;19:654–660.
    1. Song D., Moon H., Kang B. Porcine epidemic diarrhea: a review of current epidemiology and available vaccines. Clin. Exp. Vaccine Res. 2015;4:166–176.
    1. Stibig H.J., Stolle F., Dennis R., Feldkotter C. JRC Scientific and Technical Reports, EUR, 22896. 2007. Forest cover change in Southeast Asia–the regional pattern.
    1. Walston, J., Kingston, T., Hutson, A.M., 2008. Rhinolophus affinis. Red List Threat. Species 2008 ET19522A8952553. Available: e.T19522A8952553. Accessed September 21, 2016.
    1. Wang L., Shi Z., Zhang S., Field H., Daszak P., Eaton B.T. Review of bats and SARS. Emerg. Infect. Dis. 2006;12:18–34.
    1. Watanabe S., Masangkay J.S., Nagata N., Morikawa S., Mizutani T., Fukushi S., Alviola P., Omatsu T., Ueda N., Iha K., Taniguchi S., Fujii H., Tsuda S., Endoh M., Kato K., Tohya Y., Kyuwa S., Yoshikawa Y., Akashi H. Bat coronaviruses and experimental infection of bats, the Philippines. Emerg. Infect. Dis. 2010;16:1217–1223.
    1. World Development Indicators World Development Indicators: poverty & equity. 2016. Available:
    1. WWF . World Wide Fund For Nature, Greater Mekong; Bangkok, Thailand: 2013. Ecosystems in the Greater Mekong: Past Trends, Current Status, Possible Futures.

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere