Coronaviruses and Australian bats: a review in the midst of a pandemic
Alison J. Peel A G , Hume E. Field B C , Manuel Ruiz Aravena D , Daniel Edson E , Hamish McCallum A , Raina K. Plowright D and Diana Prada FA Environmental Futures Research Institute, Griffith University, Nathan, Qld 4111, Australia.
B EcoHealth Alliance, New York, NY 10001, USA.
C School of Veterinary Science, The University of Queensland, Gatton, Qld 4343, Australia.
D Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59717, USA.
E Department of Agriculture, Water and the Environment, Canberra, ACT 2601, Australia.
F School of Veterinary Medicine, Murdoch University, Perth, WA 6150, Australia.
G Corresponding author. Email: a.peel@griffith.edu.au
Australian Journal of Zoology 67(6) 346-360 https://doi.org/10.1071/ZO20046
Submitted: 8 June 2020 Accepted: 24 July 2020 Published: 2 September 2020
Journal Compilation © CSIRO 2019 Open Access CC BY
Abstract
Australia’s 81 bat species play vital ecological and economic roles via suppression of insect pests and maintenance of native forests through pollination and seed dispersal. Bats also host a wide diversity of coronaviruses globally, including several viral species that are closely related to SARS-CoV-2 and other emergent human respiratory coronaviruses. Although there are hundreds of studies of bat coronaviruses globally, there are only three studies of bat coronaviruses in Australian bat species, and no systematic studies of drivers of shedding. These limited studies have identified two betacoronaviruses and seven alphacoronaviruses, but less than half of Australian species are included in these studies and further research is therefore needed. There is no current evidence of spillover of coronaviruses from bats to humans in Australia, either directly or indirectly via intermediate hosts. The limited available data are inadequate to determine whether this lack of evidence indicates that spillover does not occur or occurs but is undetected. Conversely, multiple international agencies have flagged the potential transmission of human coronaviruses (including SARS CoV-2) from humans to bats, and the consequent threat to bat conservation and human health. Australia has a long history of bat research across a broad range of ecological and associated disciplines, as well as expertise in viral spillover from bats. This strong foundation is an ideal platform for developing integrative approaches to understanding bat health and sustainable protection of human health.
References
Anthony, S. J., Ojeda-Flores, R., Rico-Chávez, O., Navarrete-Macias, I., Zambrana-Torrelio, C. M., Rostal, M. K., Epstein, J. H., Tipps, T., Liang, E., Sanchez-Leon, M., Sotomayor-Bonilla, J., Aguirre, A. A., Ávila-Flores, R., Medellín, R. A., Goldstein, T., Suzán, G., Daszak, P., and Lipkin, W. I. (2013). Coronaviruses in bats from Mexico. The Journal of General Virology 94, 1028–1038.| Coronaviruses in bats from Mexico.Crossref | GoogleScholarGoogle Scholar | 23364191PubMed |
Anthony, S. J., Johnson, C. K., Greig, D. J., Kramer, S., Che, X., Wells, H., Hicks, A. L., Joly, D. O., Wolfe, N. D., Daszak, P., Karesh, W., Lipkin, W. I., Morse, S. S., Consortium, P., Mazet, J. A. K., and Goldstein, T. (2017a). Global patterns in coronavirus diversity. Virus Evolution 3, vex012.
| Global patterns in coronavirus diversity.Crossref | GoogleScholarGoogle Scholar | 28630747PubMed |
Anthony, S. J., Gilardi, K., Menachery, V. D., Goldstein, T., Ssebide, B., Mbabazi, R., Navarrete-Macias, I., Liang, E., Wells, H., Hicks, A., Petrosov, A., Byarugaba, D. K., Debbink, K., Dinnon, K. H., Scobey, T., Randell, S. H., Yount, B. L., Cranfield, M., Johnson, C. K., Baric, R. S., Lipkin, W. I., and Mazet, J. A. K. (2017b). Further evidence for bats as the evolutionary source of Middle East Respiratory Syndrome coronavirus. mBio 8, e00373-–17.
| Further evidence for bats as the evolutionary source of Middle East Respiratory Syndrome coronavirus.Crossref | GoogleScholarGoogle Scholar | 28377531PubMed |
Australian Government Department of Health (2020). Coronavirus (COVID-19) at a glance. Available at: https://www.health.gov.au/resources/publications/coronavirus-covid-19-at-a-glance [accessed 4 June 2020].
Barr, J. A., Smith, C., Marsh, G. A., Field, H. E., and Wang, L. F. (2012). Evidence of bat origin for Menangle virus, a zoonotic paramyxovirus first isolated from diseased pigs. The Journal of General Virology 93, 2590–2594.
| Evidence of bat origin for Menangle virus, a zoonotic paramyxovirus first isolated from diseased pigs.Crossref | GoogleScholarGoogle Scholar | 22915696PubMed |
Becker, D. J., Crowley, D. E., Washburne, A. D., and Plowright, R. K. (2019). Temporal and spatial limitations in global surveillance for bat filoviruses and henipaviruses. Biology Letters 15, 20190423.
| Temporal and spatial limitations in global surveillance for bat filoviruses and henipaviruses.Crossref | GoogleScholarGoogle Scholar | 31822244PubMed |
Boni, M. F., Lemey, P., Jiang, X., Lam, T. T.-Y., Perry, B., Castoe, T., Rambaut, A., and Robertson, D. L. (2020). Evolutionary origins of the SARS-CoV-2 sarbecovirus lineage responsible for the COVID-19 pandemic. bioRxiv
Brook, C. E., Ranaivoson, H. C., Broder, C. C., Cunningham, A. A., Héraud, J.-M., Peel, A. J., Gibson, L., Wood, J. L. N., Metcalf, C. J., and Dobson, A. P. (2019). Disentangling serology to elucidate henipa- and filovirus transmission in Madagascar fruit bats. Journal of Animal Ecology 88, 1001–1016.
| Disentangling serology to elucidate henipa- and filovirus transmission in Madagascar fruit bats.Crossref | GoogleScholarGoogle Scholar | 30908623PubMed |
Chen, N., Zhou, M., Dong, X., Qu, J., Gong, F., Han, Y., Qiu, Y., Wang, J., Liu, Y., Wei, Y., Xia, J. a., Yu, T., Zhang, X., and Zhang, L. (2020). Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet 395, 507–513.
| Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study.Crossref | GoogleScholarGoogle Scholar | 32007143PubMed |
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., and Mahy, B. W. J. (2000). Nipah virus: a recently emergent deadly paramyxovirus. Science 288, 1432–1435.
| Nipah virus: a recently emergent deadly paramyxovirus.Crossref | GoogleScholarGoogle Scholar | 10827955PubMed |
Cui, J., Han, N., Streicker, D., Li, G., Tang, X., Shi, Z., Hu, Z., Zhao, G., Fontanet, A., Guan, Y., Wang, L., Jones, G., Field, H. E., Daszak, P., and Zhang, S. (2007). Evolutionary relationships between bat coronaviruses and their hosts. Emerging Infectious Diseases 13, 1526–1532.
| Evolutionary relationships between bat coronaviruses and their hosts.Crossref | GoogleScholarGoogle Scholar | 18258002PubMed |
Cui, J., Li, F., and Shi, Z.-L. (2019). Origin and evolution of pathogenic coronaviruses. Nature Reviews. Microbiology 17, 181–192.
| Origin and evolution of pathogenic coronaviruses.Crossref | GoogleScholarGoogle Scholar | 30531947PubMed |
Degeling, C., and Kerridge, I. (2012). Hendra in the news: public policy meets public morality in times of zoonotic uncertainty. Social Science & Medicine 82, 156–163.
Drexler, J. F., Gloza-Rausch, F., Glende, J., Corman, V. M., Muth, D., Goettsche, M., Seebens, A., Niedrig, M., Pfefferle, S., Yordanov, S., Zhelyazkov, L., Hermanns, U., Vallo, P., Lukashev, A., Muller, M. A., Deng, H., Herrler, G., and Drosten, C. (2010). Genomic characterization of severe acute respiratory syndrome-related coronavirus in European bats and classification of coronaviruses based on partial RNA-dependent RNA polymerase gene sequences. Journal of Virology 84, 11336–11349.
| Genomic characterization of severe acute respiratory syndrome-related coronavirus in European bats and classification of coronaviruses based on partial RNA-dependent RNA polymerase gene sequences.Crossref | GoogleScholarGoogle Scholar | 20686038PubMed |
Drexler, J. F., Corman, V. M., and Drosten, C. (2014). Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS. Antiviral Research 101, 45–56.
| Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS.Crossref | GoogleScholarGoogle Scholar | 24184128PubMed |
Eby, P., and Law, B. (2008). Ranking the feeding habitat of grey-headed flying foxes for conservation management. Department of Environment and Climate Change (NSW) and The Department of Environment, Water, Heritage and the Arts, Sydney.
Edson, D., Peel, A. J., Huth, L., Mayer, D. G., Vidgen, M. E., McMichael, L., Broos, A., Melville, D., Kristoffersen, J., de Jong, C., McLaughlin, A., and Field, H. E. (2019). Time of year, age class and body condition predict Hendra virus infection in Australian black flying foxes (Pteropus alecto). Epidemiology and Infection 147, e240.
| Time of year, age class and body condition predict Hendra virus infection in Australian black flying foxes (Pteropus alecto).Crossref | GoogleScholarGoogle Scholar | 31364577PubMed |
Fan, Y., Zhao, K., Shi, Z.-L., and Zhou, P. (2019). Bat coronaviruses in China. Viruses 11, 210.
| Bat coronaviruses in China.Crossref | GoogleScholarGoogle Scholar |
Field, H. E., Jordan, D., Edson, D., Morris, S., Melville, D., Parry-Jones, K., Broos, A., Divljan, A., McMichael, L. A., Davis, R., Kung, N., Kirkland, P., and Smith, C. (2015). Spatiotemporal aspects of Hendra virus infection in pteropid bats (flying-foxes) in eastern Australia. PLoS One 10, e0144055.
| Spatiotemporal aspects of Hendra virus infection in pteropid bats (flying-foxes) in eastern Australia.Crossref | GoogleScholarGoogle Scholar | 26060997PubMed |
Franklin, A. B., and Bevins, S. N. (2020). Spillover of SARS-CoV-2 into novel wild hosts in North America: a conceptual model for perpetuation of the pathogen. The Science of the Total Environment 733, 139358.
| Spillover of SARS-CoV-2 into novel wild hosts in North America: a conceptual model for perpetuation of the pathogen.Crossref | GoogleScholarGoogle Scholar | 32416535PubMed |
Godthelp, H., Archer, M., Cifelli, R., Hand, S. J., and Gilkeson, C. F. (1992). Earliest known Australian Tertiary mammal fauna. Nature 356, 514–516.
| Earliest known Australian Tertiary mammal fauna.Crossref | GoogleScholarGoogle Scholar |
Gould, A. R., Hyatt, A. D., Lunt, R., Kattenbelt, J. A., Hengstberger, S., and Blacksell, S. D. (1998). Characterisation of a novel lyssavirus isolated from pteropid bats in Australia. Virus Research 54, 165–187.
| Characterisation of a novel lyssavirus isolated from pteropid bats in Australia.Crossref | GoogleScholarGoogle Scholar | 9696125PubMed |
Gretebeck, L. M., and Subbarao, K. (2015). Animal models for SARS and MERS coronaviruses. Current Opinion in Virology 13, 123–129.
| Animal models for SARS and MERS coronaviruses.Crossref | GoogleScholarGoogle Scholar | 26184451PubMed |
Guan, Y., Zheng, B. J., He, Y. Q., Liu, X. L., Zhuang, Z. X., Cheung, C. L., Luo, S. W., Li, P. H., Zhang, L. J., Guan, Y. J., Butt, K. M., Wong, K. L., Chan, K. W., Lim, W., Shortridge, K. F., Yuen, K. Y., Peiris, J. S. M., and Poon, L. L. M. (2003). Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302, 276–278.
| Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China.Crossref | GoogleScholarGoogle Scholar | 12958366PubMed |
Halpin, K., Young, P. L., and Field, H. E. (2000). Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. Journal of General Virology 81, 1927–1932.
| Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus.Crossref | GoogleScholarGoogle Scholar | 10900029PubMed |
He, B., Zhang, Y., Xu, L., Yang, W., Yang, F., Feng, Y., Xia, L., Zhou, J., Zhen, W., Feng, Y., Guo, H., Zhang, H., and Tu, C. (2014). Identification of diverse alphacoronaviruses and genomic characterization of a novel severe acute respiratory syndrome-like coronavirus from bats in China. Journal of Virology 88, 7070–7082.
| Identification of diverse alphacoronaviruses and genomic characterization of a novel severe acute respiratory syndrome-like coronavirus from bats in China.Crossref | GoogleScholarGoogle Scholar | 24719429PubMed |
Holz, P. H., Lumsden, L. F., Druce, J., Legione, A. R., Vaz, P., Devlin, J. M., and Hufschmid, J. (2018). Virus survey in populations of two subspecies of bent-winged bats (Miniopterus orianae bassanii and oceanensis) in south-eastern Australia reveals a high prevalence of diverse herpesviruses. PLoS One 13, e0197625.
| Virus survey in populations of two subspecies of bent-winged bats (Miniopterus orianae bassanii and oceanensis) in south-eastern Australia reveals a high prevalence of diverse herpesviruses.Crossref | GoogleScholarGoogle Scholar | 30303979PubMed |
Hosken, D. J., and Withers, P. C. (1997). Temperature regulation and metabolism of an Australian bat, Chalinolobus gouldii (Chiroptera: Vespertilionidae) when euthermic and torpid. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 167, 71–80.
| Temperature regulation and metabolism of an Australian bat, Chalinolobus gouldii (Chiroptera: Vespertilionidae) when euthermic and torpid.Crossref | GoogleScholarGoogle Scholar | 9051907PubMed |
Hu, B., Zeng, L.-P., Yang, X.-L., Ge, X.-Y., Zhang, W., Li, B., Xie, J.-Z., Shen, X.-R., Zhang, Y.-Z., Wang, N., Luo, D.-S., Zheng, X.-S., Wang, M.-N., Daszak, P., Wang, L.-F., Cui, J., and Shi, Z.-L. (2017). Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus. PLoS Pathogens 13, e1006698.
| Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus.Crossref | GoogleScholarGoogle Scholar | 29190287PubMed |
IUCN Bat Specialist Group (2020). IUCN SSC Bat Specialist Group (BSG) recommendations to reduce the risk of transmission of SARS-CoV-2 from humans to bats in bat rescue and rehabilitation centers. MAP: Minimize, Assess, Protect. Living Document Version 1.1, released 15 July 2020. Available at: https://www.iucnbsg.org/bsg-publications.html [accessed 15 July 2020].
Jayme, S. I., Field, H. E., de Jong, C., Olival, K. J., Marsh, G., Tagtag, A. M., Hughes, T., Bucad, A. C., Barr, J. A., Azul, R. R., Retes, L. M., Foord, A., Yu, M., Cruz, M. S., Santos, I. J., Lim, T. M. S., Benigno, C. C., Epstein, J. H., Wang, L.-F., Daszak, P., and Newman, S. H. (2015). Molecular evidence of Ebola Reston virus infection in Philippine bats. Virology Journal 12, 107.
| Molecular evidence of Ebola Reston virus infection in Philippine bats.Crossref | GoogleScholarGoogle Scholar | 26184657PubMed |
Jeong, J, Smith, C. S., Peel, A. J., Plowright, R. K., Kerlin, D. H., McBroom, J, and McCallum, H (2017). Persistent infections support maintenance of a coronavirus in a population of Australian bats (Myotis macropus). Epidemiology and Infection 145, 2053–2061.
| 28528587PubMed |
Joffrin, L., Goodman, S. M., Wilkinson, D. A., Ramasindrazana, B., Lagadec, E., Gomard, Y., Minter, G. L., Santos, A. D., Schoeman, M. C., Sookhareea, R., Tortosa, P., Julienne, S., Gudo, E. S., Mavingui, P., and Lebarbenchon, C. (2020). Bat coronavirus phylogeography in the western Indian Ocean. Scientific Reports 10, 6873.
| Bat coronavirus phylogeography in the western Indian Ocean.Crossref | GoogleScholarGoogle Scholar | 32327721PubMed |
Johnson, C. K., Hitchens, P. L., Pandit, P. S., Rushmore, J., Evans, T. S., Young, C. C. W., and Doyle, M. M. (2020). Global shifts in mammalian population trends reveal key predictors of virus spillover risk. Proceedings of the Royal Society B: Biological Sciences 287, 20192736.
| 32259475PubMed |
Jung, K., and Saif, L. J. (2015). Porcine epidemic diarrhea virus infection: etiology, epidemiology, pathogenesis and immunoprophylaxis. Veterinary Journal 204, 134–143.
| Porcine epidemic diarrhea virus infection: etiology, epidemiology, pathogenesis and immunoprophylaxis.Crossref | GoogleScholarGoogle Scholar |
Kan, B., Wang, M., Jing, H., Xu, H., Jiang, X., Yan, M., Liang, W., Zheng, H., Wan, K., Liu, Q., Cui, B., Xu, Y., Zhang, E., Wang, H., Ye, J., Li, G., Li, M., Cui, Z., Qi, X., Chen, K., Du, L., Gao, K., Zhao, Y.-t., Zou, X.-z., Feng, Y.-J., Gao, Y.-F., Hai, R., Yu, D., Guan, Y., and Xu, J. (2005). Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms. Journal of Virology 79, 11892–11900.
| Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms.Crossref | GoogleScholarGoogle Scholar | 16140765PubMed |
Kessler, M. K., Becker, D. J., Peel, A. J., Justice, N. V., Lunn, T., Crowley, D. E., Jones, D. N., Eby, P., Sánchez, C. A., and Plowright, R. K. (2018). Changing resource landscapes and spillover of henipaviruses. Annals of the New York Academy of Sciences 1429, 78–99.
| Changing resource landscapes and spillover of henipaviruses.Crossref | GoogleScholarGoogle Scholar | 30138535PubMed |
Kissler, S. M., Tedijanto, C., Goldstein, E., Grad, Y. H., and Lipsitch, M. (2020). Projecting the transmission dynamics of SARS-CoV-2 through the postpandemic period. Science 368, 860–868.
| Projecting the transmission dynamics of SARS-CoV-2 through the postpandemic period.Crossref | GoogleScholarGoogle Scholar | 32291278PubMed |
Kolkert, H., Andrew, R., Smith, R., Rader, R., and Reid, N. (2020). Insectivorous bats selectively source moths and eat mostly pest insects on dryland and irrigated cotton farms. Ecology and Evolution 10, 371–388.
| Insectivorous bats selectively source moths and eat mostly pest insects on dryland and irrigated cotton farms.Crossref | GoogleScholarGoogle Scholar | 31988733PubMed |
Ksiazek, T. G., Erdman, D., Goldsmith, C. S., Zaki, S. R., Peret, T., Emery, S., Tong, S., Urbani, C., Comer, J. A., Lim, W., Rollin, P. E., Dowell, S. F., Ling, A.-E., Humphrey, C. D., Shieh, W.-J., Guarner, J., Paddock, C. D., Rota, P., Fields, B., DeRisi, J., Yang, J.-Y., Cox, N., Hughes, J. M., LeDuc, J. W., Bellini, W. J., Anderson, L. J., and Group, S. W. (2003). A novel coronavirus associated with severe acute respiratory syndrome. The New England Journal of Medicine 348, 1953–1966.
| A novel coronavirus associated with severe acute respiratory syndrome.Crossref | GoogleScholarGoogle Scholar | 12690092PubMed |
Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.
| MEGA X: molecular evolutionary genetics analysis across computing platforms.Crossref | GoogleScholarGoogle Scholar | 29722887PubMed |
Kung, N. Y., Field, H. E., McLaughlin, A., Edson, D., and Taylor, M. (2015). Flying-foxes in the Australian urban environment – community attitudes and opinions. One Health 1, 24–30.
| Flying-foxes in the Australian urban environment – community attitudes and opinions.Crossref | GoogleScholarGoogle Scholar | 28616461PubMed |
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., and Buchy, P. (2017). Genetic diversity of coronaviruses in bats in Lao PDR and Cambodia. Infection, Genetics and Evolution 48, 10–18.
| Genetic diversity of coronaviruses in bats in Lao PDR and Cambodia.Crossref | GoogleScholarGoogle Scholar | 27932284PubMed |
Latinne, A., Hu, B., Olival, K. J., Zhu, G., Zhang, L., Li, H., Chmura, A. A., Field, H. E., Zambrana-Torrelio, C., Epstein, J. H., Li, B., Zhang, W., Wang, L.-F., Shi, Z., and Daszak, P. (2020). Origin and cross-species transmission of bat coronaviruses in China. bioRxiv
Lau, S. K. P., Woo, P. C. Y., Li, K. S. M., Huang, Y., Tsoi, H. W., Wong, B. H. L., Wong, S. S. Y., Leung, S. Y., Chan, K. H., and Yuen, K. Y. (2005). Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proceedings of the National Academy of Sciences of the United States of America 102, 14040–14045.
| Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats.Crossref | GoogleScholarGoogle Scholar |
Law, B. S., and Lean, M. (1999). Common blossom bats (Syconycteris australis) as pollinators in fragmented Australian tropical rainforest. Biological Conservation 91, 201–212.
| Common blossom bats (Syconycteris australis) as pollinators in fragmented Australian tropical rainforest.Crossref | GoogleScholarGoogle Scholar |
Li, W., Shi, Z., Yu, M., Ren, W., Smith, C., Epstein, J. H., Wang, H., Crameri, G., Hu, Z., Zhang, H., Zhang, J., McEachern, J., Field, H. E., Daszak, P., Eaton, B. T., Zhang, S., and Wang, L.-F. (2005). Bats are natural reservoirs of SARS-like coronaviruses. Science 310, 676–679.
| Bats are natural reservoirs of SARS-like coronaviruses.Crossref | GoogleScholarGoogle Scholar | 16195424PubMed |
Li, Q., Guan, X., Wu, P., Wang, X., Zhou, L., Tong, Y., Ren, R., Leung, K. S. M., Lau, E. H. Y., Wong, J. Y., Xing, X., Xiang, N., Wu, Y., Li, C., Chen, Q., Li, D., Liu, T., Zhao, J., Liu, M., Tu, W., Chen, C., Jin, L., Yang, R., Wang, Q., Zhou, S., Wang, R., Liu, H., Luo, Y., Liu, Y., Shao, G., Li, H., Tao, Z., Yang, Y., Deng, Z., Liu, B., Ma, Z., Zhang, Y., Shi, G., Lam, T. T. Y., Wu, J. T., Gao, G. F., Cowling, B. J., Yang, B., Leung, G. M., and Feng, Z. (2020). Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia. The New England Journal of Medicine 382, 1199–1207.
| Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia.Crossref | GoogleScholarGoogle Scholar | 31995857PubMed |
Lindahl, J. F., and Grace, D. (2015). The consequences of human actions on risks for infectious diseases: a review. Infection Ecology & Epidemiology 5, 30048.
| The consequences of human actions on risks for infectious diseases: a review.Crossref | GoogleScholarGoogle Scholar |
Lumsden, L. F., and Bennett, A. F. (2005). Scattered trees in rural landscapes: foraging habitat for insectivorous bats in south-eastern Australia. Biological Conservation 122, 205–222.
| Scattered trees in rural landscapes: foraging habitat for insectivorous bats in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |
McKenzie, N. L., and Rolfe, J. K. (1986). Structure of bat guilds in the Kimberley mangroves, Australia. Journal of Animal Ecology 55, 401.
| Structure of bat guilds in the Kimberley mangroves, Australia.Crossref | GoogleScholarGoogle Scholar |
Montecino-Latorre, D., Goldstein, T., Gilardi, K., Wolking, D., Wormer, E. V., Kazwala, R., Ssebide, B., Nziza, J., Sijali, Z., Cranfield, M., Consortium, P., and Mazet, J. A. K. (2020). Reproduction of East-African bats may guide risk mitigation for coronavirus spillover. One Health Outlook 2, 2.
| Reproduction of East-African bats may guide risk mitigation for coronavirus spillover.Crossref | GoogleScholarGoogle Scholar |
Moran, C., Catterall, C. P., and Kanowski, J. (2009). Reduced dispersal of native plant species as a consequence of the reduced abundance of frugivore species in fragmented rainforest. Biological Conservation 142, 541–552.
| Reduced dispersal of native plant species as a consequence of the reduced abundance of frugivore species in fragmented rainforest.Crossref | GoogleScholarGoogle Scholar |
Moreira-Soto, A., Taylor-Castillo, L., Vargas-Vargas, N., Rodríguez-Herrera, B., Jiménez, C., and Corrales-Aguilar, E. (2015). Neotropical bats from Costa Rica harbour diverse coronaviruses. Zoonoses and Public Health 62, 501–505.
| Neotropical bats from Costa Rica harbour diverse coronaviruses.Crossref | GoogleScholarGoogle Scholar | 25653111PubMed |
Olival, K. J., Cryan, P. M., Amman, B. R., Baric, R. S., Blehert, D. S., Brook, C. E., Calisher, C. H., Castle, K. T., Coleman, J. T. H., Daszak, P., Epstein, J. H., Field, H., Frick, W. F., Gilbert, A. T., Hayman, D. T. S., Ip, H. S., Karesh, W. B., Johnson, C. K., Kading, R. C., Kingston, T., Lorch, J. M., Mendenhall, I. H., Peel, A. J., Phelps, K. L., Plowright, R. K., Reeder, D. M., Reichard, J. D., Sleeman, J. M., Streicker, D. G., Towner, J. S., and Wang, L.-F. (2020). Possible risks of SARS-CoV-2 spillover from humans to free-ranging wildlife: a case study of bats. PLoS Pathogens 16, e1008758.
| Possible risks of SARS-CoV-2 spillover from humans to free-ranging wildlife: a case study of bats.Crossref | GoogleScholarGoogle Scholar |
Paez, D. J., Giles, J., McCallum, H., Field, H. E., Jordan, D., Peel, A. J., and Plowright, R. K. (2017). Conditions affecting the timing and magnitude of Hendra virus shedding across pteropodid bat populations in Australia. Epidemiology and Infection 145, 3143–3153.
| Conditions affecting the timing and magnitude of Hendra virus shedding across pteropodid bat populations in Australia.Crossref | GoogleScholarGoogle Scholar | 28942750PubMed |
Peel, A. J., Wells, K., Giles, J., Boyd, V., Burroughs, A., Edson, D., Crameri, G., Baker, M. L., Field, H., Wang, L.-F., McCallum, H., Plowright, R. K., and Clark, N. (2019). Synchronous shedding of multiple bat paramyxoviruses coincides with peak periods of Hendra virus spillover. Emerging Microbes & Infections 8, 1314–1323.
| Synchronous shedding of multiple bat paramyxoviruses coincides with peak periods of Hendra virus spillover.Crossref | GoogleScholarGoogle Scholar |
Pfefferle, S., Oppong, S., Drexler, J. F., Gloza-Rausch, F., Ipsen, A., Seebens, A., Müller, M. A., Annan, A., Vallo, P., Adu-Sarkodie, Y., Kruppa, T. F., and Drosten, C. (2009). Distant relatives of severe acute respiratory syndrome coronavirus and close relatives of human coronavirus 229E in bats, Ghana. Emerging Infectious Diseases 15, 1377–1384.
| Distant relatives of severe acute respiratory syndrome coronavirus and close relatives of human coronavirus 229E in bats, Ghana.Crossref | GoogleScholarGoogle Scholar | 19788804PubMed |
Philbey, A. W., Kirkland, P. D., Ross, A. D., Davis, R. J., Gleeson, A. B., Love, R. J., Daniels, P. W., Gould, A. R., and Hyatt, A. D. (1998). An apparently new virus (family Paramyxoviridae) infectious for pigs, humans, and fruit bats. Emerging Infectious Diseases 4, 269–271.
| An apparently new virus (family Paramyxoviridae) infectious for pigs, humans, and fruit bats.Crossref | GoogleScholarGoogle Scholar | 9621197PubMed |
Plowright, R. K., Field, H. E., Smith, C., Divljan, A., Palmer, C., Tabor, G., Daszak, P., and Foley, J. E. (2008). Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proceedings of the Royal Society B: Biological Sciences 275, 861–869.
| Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus).Crossref | GoogleScholarGoogle Scholar | 18198149PubMed |
Plowright, R. K., Eby, P., Hudson, P. J., Smith, I. L., Westcott, D. A., Bryden, W. L., Middleton, D., Reid, P. A., McFarlane, R. A., Martin, G., Tabor, G. M., Skerratt, L. F., Anderson, D. L., Crameri, G., Quammen, D., Jordan, D., Freeman, P., Wang, L.-F., Epstein, J. H., Marsh, G. A., Kung, N. Y., and McCallum, H. (2015). Ecological dynamics of emerging bat virus spillover. Proceedings of the Royal Society B: Biological Sciences 282, 20142124.
| Ecological dynamics of emerging bat virus spillover.Crossref | GoogleScholarGoogle Scholar | 25392474PubMed |
Plowright, R. K., Parrish, C. R., McCallum, H., Hudson, P. J., Ko, A. I., Graham, A. L., and Lloyd-Smith, J. O. (2017). Pathways to zoonotic spillover. Nature Reviews. Microbiology 15, 502–510.
| Pathways to zoonotic spillover.Crossref | GoogleScholarGoogle Scholar | 28555073PubMed |
Plowright, R. K., Becker, D. J., McCallum, H., and Manlove, K. (2019). Sampling to elucidate the dynamics of infections in reservoir hosts. Philosophical Transactions of the Royal Society B: Biological Sciences 374, 20180336.
| Sampling to elucidate the dynamics of infections in reservoir hosts.Crossref | GoogleScholarGoogle Scholar |
Poon, L. L. M., Chu, D. K. W., Chan, K. H., Wong, O. K., Ellis, T. M., Leung, Y. H. C., Lau, S. K. P., Woo, P. C. Y., Suen, K. Y., Yuen, K. Y., Guan, Y., and Peiris, J. S. M. (2005). Identification of a novel coronavirus in bats. Journal of Virology 79, 2001–2009.
| Identification of a novel coronavirus in bats.Crossref | GoogleScholarGoogle Scholar |
Prada, D., Boyd, V., Baker, M. L., O’Dea, M., and Jackson, B. (2019). Viral diversity of microbats within the South West Botanical Province of Western Australia. Viruses 11, 1157.
| Viral diversity of microbats within the South West Botanical Province of Western Australia.Crossref | GoogleScholarGoogle Scholar |
Quan, P.-L., Firth, C., Street, C., Henriquez, J. A., Petrosov, A., Tashmukhamedova, A., Hutchison, S. K., Egholm, M., Osinubi, M. O. V., Niezgoda, M., Ogunkoya, A. B., Briese, T., Rupprecht, C. E., and Lipkin, W. I. (2010). Identification of a severe acute respiratory syndrome coronavirus-like virus in a leaf-nosed bat in Nigeria. mBio 1, e00208-10.
| Identification of a severe acute respiratory syndrome coronavirus-like virus in a leaf-nosed bat in Nigeria.Crossref | GoogleScholarGoogle Scholar | 21063474PubMed |
Reardon, T. B., Armstrong, K. N., and Jackson, S. M. (2015). A current taxonomic list of Australian Chiroptera. Australasian Bat Society. Available at: http://ausbats.org.au/taxonomic-list/4589345107 [accessed 4 June 2020].
Rimmer, M. (2020). ‘Bat people’ say the unique mammals need to be respected, not feared. SBS The Feed. Available at: https://www.sbs.com.au/news/the-feed/bat-people-say-the-unique-mammals-need-to-be-respected-not-feared [accessed 4 June 2020].
Runge, M. C., Grant, E. H. C., Coleman, J. T. H., Reichard, J. D., Gibbs, S. E. J., Cryan, P. M., Olival, K. J., Walsh, D. P., Blehert, D. S., Hopkins, M. C., and Sleeman, J. M. (2020). Assessing the risks posed by SARS-CoV-2 in and via North American bats – decision framing and rapid risk assessment. U.S. Geological Survey Open-File Report 2020-1060. Available at: http://pubs.er.usgs.gov/publication/ofr20201060 [accessed 4 June 2020].
Schountz, T., Baker, M. L., Butler, J., and Munster, V. (2017). Immunological control of viral infections in bats and the emergence of viruses highly pathogenic to humans. Frontiers in Immunology 8, 1098.
| Immunological control of viral infections in bats and the emergence of viruses highly pathogenic to humans.Crossref | GoogleScholarGoogle Scholar | 28959255PubMed |
Selvey, L., Taylor, R., Arklay, A., and Gerrard, J. (1996). Screening of bat carers for antibodies to equine morbillivirus. Communicable Diseases Intelligence 20, 477–478.
Shi, Z., and Hu, Z. (2008). A review of studies on animal reservoirs of the SARS coronavirus. Virus Research 133, 74–87.
| A review of studies on animal reservoirs of the SARS coronavirus.Crossref | GoogleScholarGoogle Scholar | 17451830PubMed |
Shi, J., Wen, Z., Zhong, G., Yang, H., Wang, C., Huang, B., Liu, R., He, X., Shuai, L., Sun, Z., Zhao, Y., Liu, P., Liang, L., Cui, P., Wang, J., Zhang, X., Guan, Y., Tan, W., Wu, G., Chen, H., and Bu, Z. (2020). Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2. Science 368, 1016–1020.
| Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2.Crossref | GoogleScholarGoogle Scholar | 32269068PubMed |
Simmons, N. B., and Cirranello, A. L. (2020). Bat species of the world: a taxonomic and geographic database. Available at: www.batnames.org [accessed 4 June 2020].
Smith, C. (2015). Australian bat coronaviruses. Ph.D. Thesis, University of Queensland, Brisbane, Australia.
Smith, C. S., de Jong, C. E., Meers, J., Henning, J., Wang, L. F., and Field, H. E. (2016). Coronavirus infection and diversity in bats in the Australasian region. EcoHealth 13, 72–82.
| Coronavirus infection and diversity in bats in the Australasian region.Crossref | GoogleScholarGoogle Scholar | 27048154PubMed |
Su, S., Wong, G., Shi, W., Liu, J., Lai, A. C. K., Zhou, J., Liu, W., Bi, Y., and Gao, G. F. (2016). Epidemiology, genetic recombination, and pathogenesis of coronaviruses. Trends in Microbiology 24, 490–502.
| Epidemiology, genetic recombination, and pathogenesis of coronaviruses.Crossref | GoogleScholarGoogle Scholar | 27012512PubMed |
Tang, X. C., Zhang, J. X., Zhang, S. Y., Wang, P., Fan, X. H., Li, L. F., Li, G., Dong, B. Q., Liu, W., Cheung, C. L., Xu, K. M., Song, W. J., Vijaykrishna, D., Poon, L. L. M., Peiris, J. S. M., Smith, G. J. D., Chen, H., and Guan, Y. (2006). Prevalence and genetic diversity of coronaviruses in bats from China. Journal of Virology 80, 7481–7490.
| Prevalence and genetic diversity of coronaviruses in bats from China.Crossref | GoogleScholarGoogle Scholar | 16840328PubMed |
Tong, S., Conrardy, C., Ruone, S., Kuzmin, I. V., Guo, X., Tao, Y., Niezgoda, M., Haynes, L., Agwanda, B., Breiman, R. F., Anderson, L. J., and Rupprecht, C. E. (2009). Detection of novel SARS-like and other coronaviruses in bats from Kenya. Emerging Infectious Diseases 15, 482–485.
| Detection of novel SARS-like and other coronaviruses in bats from Kenya.Crossref | GoogleScholarGoogle Scholar | 19239771PubMed |
Tsuda, S., Watanabe, S., Masangkay, J. S., Mizutani, T., Alviola, P., Ueda, N., Iha, K., Taniguchi, S., Fujii, H., Kato, K., Horimoto, T., Kyuwa, S., Yoshikawa, Y., and Akashi, H. (2012). Genomic and serological detection of bat coronavirus from bats in the Philippines. Archives of Virology 157, 2349–2355.
| Genomic and serological detection of bat coronavirus from bats in the Philippines.Crossref | GoogleScholarGoogle Scholar | 22833101PubMed |
Tu, C., Crameri, G., Kong, X., Chen, J., Sun, Y., Yu, M., Xiang, H., Xia, X., Liu, S., Ren, T., Yu, Y., Eaton, B. T., Xuan, H., and Wang, L.-F. (2004). Antibodies to SARS coronavirus in civets. Emerging Infectious Diseases 10, 2244–2248.
| Antibodies to SARS coronavirus in civets.Crossref | GoogleScholarGoogle Scholar | 15663874PubMed |
US Department of Agriculture Animal and Plant Health Inspection Service (2020). USDA statement on the confirmation of COVID-19 in a tiger in New York. United States Department of Agriculture, Animal and Plant Health Inspection Service. Available at: https://www.aphis.usda.gov/aphis/newsroom/news/sa_by_date/sa-2020/ny-zoo-covid-19 [accessed 4 June 2020].
Vijaykrishna, D., Smith, G. J. D., Zhang, J. X., Peiris, J. S. M., Chen, H., and Guan, Y. (2007). Evolutionary insights into the ecology of coronaviruses. Journal of Virology 81, 4012–4020.
| Evolutionary insights into the ecology of coronaviruses.Crossref | GoogleScholarGoogle Scholar | 17267506PubMed |
Wacharapluesadee, S., Sintunawa, C., Kaewpom, T., Khongnomnan, K., Olival, K. J., Epstein, J. H., Rodpan, A., Sangsri, P., Intarut, N., Chindamporn, A., Suksawa, K., and Hemachudha, T. (2013). Group C betacoronavirus in bat guano fertilizer, Thailand. Emerging Infectious Diseases 19, 1349–1351.
| Group C betacoronavirus in bat guano fertilizer, Thailand.Crossref | GoogleScholarGoogle Scholar | 23880503PubMed |
Wacharapluesadee, S., Duengkae, P., Chaiyes, A., Kaewpom, T., Rodpan, A., Yingsakmongkon, S., Petcharat, S., Phengsakul, P., Maneeorn, P., and Hemachudha, T. (2018). Longitudinal study of age-specific pattern of coronavirus infection in Lyle’s flying fox (Pteropus lylei) in Thailand. Virology Journal 15, 38.
| Longitudinal study of age-specific pattern of coronavirus infection in Lyle’s flying fox (Pteropus lylei) in Thailand.Crossref | GoogleScholarGoogle Scholar | 29463282PubMed |
Wang, N., Li, S.-Y., Yang, X.-L., Huang, H.-M., Zhang, Y.-J., Guo, H., Luo, C.-M., Miller, M., Zhu, G., Chmura, A. A., Hagan, E., Zhou, J.-H., Zhang, Y.-Z., Wang, L.-F., Daszak, P., and Shi, Z.-L. (2018). Serological evidence of bat SARS-related coronavirus infection in humans, China. Virologica Sinica 33, 104–107.
| Serological evidence of bat SARS-related coronavirus infection in humans, China.Crossref | GoogleScholarGoogle Scholar | 29500691PubMed |
Webb, N., and Tidemann, C. R. (1996). Mobility of Australian flying-foxes, Pteropus spp. (Megachiroptera): evidence from genetic variation. Proceedings of the Royal Society B: Biological Sciences 263, 497–502.
| Mobility of Australian flying-foxes, Pteropus spp. (Megachiroptera): evidence from genetic variation.Crossref | GoogleScholarGoogle Scholar | 8637931PubMed |
Welbergen, J. A., Klose, S. M., Markus, N., and Eby, P. (2008). Climate change and the effects of temperature extremes on Australian flying-foxes. Proceedings of the Royal Society B: Biological Sciences 275, 419–425.
| Climate change and the effects of temperature extremes on Australian flying-foxes.Crossref | GoogleScholarGoogle Scholar | 18048286PubMed |
Willoughby, A., Phelps, K., Consortium, P., and Olival, K. (2017). A comparative analysis of viral richness and viral sharing in cave-roosting bats. Diversity 9, 35.
| A comparative analysis of viral richness and viral sharing in cave-roosting bats.Crossref | GoogleScholarGoogle Scholar |
Wong, A., Li, X., Lau, S., and Woo, P. (2019). Global epidemiology of bat coronaviruses. Viruses 11, 174.
| Global epidemiology of bat coronaviruses.Crossref | GoogleScholarGoogle Scholar |
Woo, P. C. Y., Lau, S. K. P., Huang, Y., and Yuen, K.-Y. (2009). Coronavirus diversity, phylogeny and interspecies jumping. Experimental Biology and Medicine 234, 1117–1127.
| Coronavirus diversity, phylogeny and interspecies jumping.Crossref | GoogleScholarGoogle Scholar |
Woo, P. C. Y., Huang, Y., Lau, S. K. P., and Yuen, K.-Y. (2010). Coronavirus genomics and bioinformatics analysis. Viruses 2, 1804–1820.
| Coronavirus genomics and bioinformatics analysis.Crossref | GoogleScholarGoogle Scholar |
Zhang, G., Cowled, C., Shi, Z., Huang, Z., Bishop-Lilly, K. A., Fang, X., Wynne, J. W., Xiong, Z., Baker, M. L., Zhao, W., Tachedjian, M., Zhu, Y., Zhou, P., Jiang, X., Ng, J., Yang, L., Wu, L., Xiao, J., Feng, Y., Chen, Y., Sun, X., Zhang, Y., Marsh, G. A., Crameri, G., Broder, C. C., Frey, K. G., Wang, L.-F., and Wang, J. (2013). Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 339, 456–460.
| Comparative analysis of bat genomes provides insight into the evolution of flight and immunity.Crossref | GoogleScholarGoogle Scholar | 23258410PubMed |
Zhang, T., Wu, Q., and Zhang, Z. (2020). Probable pangolin origin of SARS-CoV-2 associated with the COVID-19 outbreak. Current Biology 30, 1346–1351.e2.
| Probable pangolin origin of SARS-CoV-2 associated with the COVID-19 outbreak.Crossref | GoogleScholarGoogle Scholar | 32197085PubMed |
Zhou, P., Chionh, Y. T., Irac, S. E., Ahn, M., Ng, J. H. J., Fossum, E., Bogen, B., Ginhoux, F., Irving, A. T., Dutertre, C.-A., and Wang, L.-F. (2016). Unlocking bat immunology: establishment of Pteropus alecto bone marrow-derived dendritic cells and macrophages. Scientific Reports 6, 38597.
| Unlocking bat immunology: establishment of Pteropus alecto bone marrow-derived dendritic cells and macrophages.Crossref | GoogleScholarGoogle Scholar | 27934903PubMed |
Zhou, P., Fan, H., Lan, T., Yang, X.-L., Shi, W.-F., Zhang, W., Zhu, Y., Zhang, Y.-W., Xie, Q.-M., Mani, S., Zheng, X.-S., Li, B., Li, J.-M., Guo, H., Pei, G.-Q., An, X.-P., Chen, J.-W., Zhou, L., Mai, K.-J., Wu, Z.-X., Li, D., Anderson, D. E., Zhang, L.-B., Li, S.-Y., Mi, Z.-Q., He, T.-T., Cong, F., Guo, P.-J., Huang, R., Luo, Y., Liu, X.-L., Chen, J., Huang, Y., Sun, Q., Zhang, X.-L.-L., Wang, Y.-Y., Xing, S.-Z., Chen, Y.-S., Sun, Y., Li, J., Daszak, P., Wang, L.-F., Shi, Z.-L., Tong, Y.-G., and Ma, J.-Y. (2018). Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature 556, 255–258.
| Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin.Crossref | GoogleScholarGoogle Scholar | 29618817PubMed |
Zhou, H., Chen, X., Hu, T., Li, J., Song, H., Liu, Y., Wang, P., Liu, D., Yang, J., Holmes, E. C., Hughes, A. C., Bi, Y., and Shi, W. (2020). A novel bat coronavirus closely related to SARS-CoV-2 contains natural insertions at the S1/S2 cleavage site of the spike protein. Current Biology 30, 2196–2203.e3.
| A novel bat coronavirus closely related to SARS-CoV-2 contains natural insertions at the S1/S2 cleavage site of the spike protein.Crossref | GoogleScholarGoogle Scholar | 32416074PubMed |
Zhou, P., Yang, X.-L., Wang, X.-G., Hu, B., Zhang, L., Zhang, W., Si, H.-R., Zhu, Y., Li, B., Huang, C.-L., Chen, H.-D., Chen, J., Luo, Y., Guo, H., Jiang, R.-D., Liu, M.-Q., Chen, Y., Shen, X.-R., Wang, X., Zheng, X.-S., Zhao, K., Chen, Q.-J., Deng, F., Liu, L.-L., Yan, B., Zhan, F.-X., Wang, Y.-Y., Xiao, G.-F., and Shi, Z.-L. (2020a). Discovery of a novel coronavirus associated with the recent pneumonia outbreak in humans and its potential bat origin. bioRxiv
Zhou, P., Yang, X.-L., Wang, X.-G., Hu, B., Zhang, L., Zhang, W., Si, H.-R., Zhu, Y., Li, B., Huang, C.-L., Chen, H.-D., Chen, J., Luo, Y., Guo, H., Jiang, R.-D., Liu, M.-Q., Chen, Y., Shen, X.-R., Wang, X., Zheng, X.-S., Zhao, K., Chen, Q.-J., Deng, F., Liu, L.-L., Yan, B., Zhan, F.-X., Wang, Y.-Y., Xiao, G.-F., and Shi, Z.-L. (2020b). A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579, 270–273.
| A pneumonia outbreak associated with a new coronavirus of probable bat origin.Crossref | GoogleScholarGoogle Scholar | 32015507PubMed |
Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., Shi, W., Lu, R., Niu, P., Zhan, F., Ma, X., Wang, D., Xu, W., Wu, G., Gao, G. F., and Tan, W. (2020). A novel coronavirus from patients with pneumonia in China, 2019. The New England Journal of Medicine 382, 727–733.
| A novel coronavirus from patients with pneumonia in China, 2019.Crossref | GoogleScholarGoogle Scholar | 31978945PubMed |