• This record comes from PubMed

Bat species assemblage predicts coronavirus prevalence

. 2024 Apr 04 ; 15 (1) : 2887. [epub] 20240404

Language English Country Great Britain, England Media electronic

Document type Journal Article

Grant support
DFG SO 428/17-1 Deutsche Forschungsgemeinschaft (German Research Foundation)
DR 772/3-1 & 7-1 Deutsche Forschungsgemeinschaft (German Research Foundation)
KA1241/18-1 Deutsche Forschungsgemeinschaft (German Research Foundation)
TH 1420/1-1 Deutsche Forschungsgemeinschaft (German Research Foundation)

Links

PubMed 38575573
PubMed Central PMC10994947
DOI 10.1038/s41467-024-46979-1
PII: 10.1038/s41467-024-46979-1
Knihovny.cz E-resources

Anthropogenic disturbances and the subsequent loss of biodiversity are altering species abundances and communities. Since species vary in their pathogen competence, spatio-temporal changes in host assemblages may lead to changes in disease dynamics. We explore how longitudinal changes in bat species assemblages affect the disease dynamics of coronaviruses (CoVs) in more than 2300 cave-dwelling bats captured over two years from five caves in Ghana. This reveals uneven CoV infection patterns between closely related species, with the alpha-CoV 229E-like and SARS-related beta-CoV 2b emerging as multi-host pathogens. Prevalence and infection likelihood for both phylogenetically distinct CoVs is influenced by the abundance of competent species and naïve subadults. Broadly, bat species vary in CoV competence, and highly competent species are more common in less diverse communities, leading to increased CoV prevalence in less diverse bat assemblages. In line with the One Health framework, our work supports the notion that biodiversity conservation may be the most proactive measure to prevent the spread of pathogens with zoonotic potential.

See more in PubMed

Steffen W, et al. The anthropocene: from global change to planetary stewardship. Ambio. 2011;40:739–761. doi: 10.1007/s13280-011-0185-x. PubMed DOI PMC

Otto, S. P. Adaptation, speciation and extinction in the Anthropocene. Proc. Biol. Sci.285, 20182047 (2018). PubMed PMC

Tompkins DM, Carver S, Jones ME, Krkosek M, Skerratt LF. Emerging infectious diseases of wildlife: a critical perspective. Trends Parasitol. 2015;31:149–159. doi: 10.1016/j.pt.2015.01.007. PubMed DOI

Gibb R, et al. Zoonotic host diversity increases in human-dominated ecosystems. Nature. 2020;584:398. doi: 10.1038/s41586-020-2562-8. PubMed DOI

O’Hanlon SJ, et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Science. 2018;360:621–627. doi: 10.1126/science.aar1965. PubMed DOI PMC

Maas M, Keet DF, Rutten VP, Heesterbeek JA, Nielen M. Assessing the impact of feline immunodeficiency virus and bovine tuberculosis co-infection in African lions. Proc. Biol. Sci. 2012;279:4206–4214. PubMed PMC

Ithete NL, et al. Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerg. Infect. Dis. 2013;19:1697–1699. doi: 10.3201/eid1910.130946. PubMed DOI PMC

Li W, et al. Bats are natural reservoirs of SARS-like coronaviruses. Science. 2005;310:676–679. doi: 10.1126/science.1118391. PubMed DOI

Zhou P, et al. Addendum: A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020;588:E6. doi: 10.1038/s41586-020-2951-z. PubMed DOI PMC

Jones KE, et al. Global trends in emerging infectious diseases. Nature. 2008;451:990–993. doi: 10.1038/nature06536. PubMed DOI PMC

Rabinowitz P, Conti L. Links among human health, animal health, and ecosystem health. Annu Rev. Public Health. 2013;34:189–204. doi: 10.1146/annurev-publhealth-031912-114426. PubMed DOI

Carlson, C. J. et al. Climate change increases cross-species viral transmission risk. Nature607, 555–562 (2022). PubMed

Kahn LH. Confronting zoonoses, linking human and veterinary medicine. Emerg. Infect. Dis. 2006;12:556–561. doi: 10.3201/eid1204.050956. PubMed DOI PMC

Lindstrom A, Green M, Paulson G, Smith HG, Devictor V. Rapid changes in bird community composition at multiple temporal and spatial scales in response to recent climate change. Ecography. 2013;36:313–322. doi: 10.1111/j.1600-0587.2012.07799.x. DOI

Farneda FZ, Meyer CFJ, Grelle CEV. Effects of land-use change on functional and taxonomic diversity of Neotropical batsPalavras-chave. Biotropica. 2020;52:120–128. doi: 10.1111/btp.12736. DOI

Johnson, C. K. et al. Global shifts in mammalian population trends reveal key predictors of virus spillover risk. P Roy Soc B-Biol Sci.287, 20192736 (2020). PubMed PMC

Hoberg, E. P. & Brooks, D. R. Evolution in action: climate change, biodiversity dynamics and emerging infectious disease. Philos T R Soc B370, 20130553 (2015). PubMed PMC

Johnson, P. T. J., De Roode, J. C. & Fenton, A. Why infectious disease research needs community ecology. Science349, 1259504 (2015). PubMed PMC

Keesing F, Holt RD, Ostfeld RS. Effects of species diversity on disease risk. Ecol. Lett. 2006;9:485–498. doi: 10.1111/j.1461-0248.2006.00885.x. PubMed DOI

Randolph SE, Dobson ADM. Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology. 2012;139:847–863. doi: 10.1017/S0031182012000200. PubMed DOI

Voigt, C. C. & Kingston, T. (eds) Bats in the Anthropocene: Conservation of Bats in a Changing World (Springer, 2016).

Frick WF, Kingston T, Flanders J. A review of the major threats and challenges to global bat conservation. Ann. Ny. Acad. Sci. 2020;1469:5–25. doi: 10.1111/nyas.14045. PubMed DOI

Anti P, et al. Human-Bat Interactions in Rural West Africa. Emerg. Infect. Dis. 2015;21:1418–1421. doi: 10.3201/eid2108.142015. PubMed DOI PMC

Akem ES, Pemunta NV. The bat meat chain and perceptions of the risk of contracting Ebola in the Mount Cameroon region. BMC Public Health. 2020;20:593. doi: 10.1186/s12889-020-08460-8. PubMed DOI PMC

de Oliveira HFM, Silva DC, Zangrandi PL, Domingos F. Brazil opens highly protected caves to mining, risking fauna. Nature. 2022;602:386. doi: 10.1038/d41586-022-00406-x. PubMed DOI

Ramírez-Fráncel LA, et al. Bats and their vital ecosystem services: a global review. Integr. Zool. 2022;17:2–23. doi: 10.1111/1749-4877.12552. PubMed DOI

Medellin RA, Wiederholt R, Lopez-Hoffman L. Conservation relevance of bat caves for biodiversity and ecosystem services. Biol. Conserv. 2017;211:45–50. doi: 10.1016/j.biocon.2017.01.012. DOI

Eby P, et al. Pathogen spillover driven by rapid changes in bat ecology. Nature. 2022 doi: 10.1038/s41586-022-05506-2. PubMed DOI PMC

Olivero, J. et al. Recent loss of closed forests is associated with Ebola virus disease outbreaks. Sci. Rep.-Uk7, 14291 (2017). PubMed PMC

Corman VM, et al. Evidence for an Ancestral Association of Human Coronavirus 229E with Bats. J. Virol. 2015;89:11858–11870. doi: 10.1128/JVI.01755-15. PubMed DOI PMC

Huynh J, et al. Evidence supporting a zoonotic origin of human coronavirus strain NL63. J. Virol. 2012;86:12816–12825. doi: 10.1128/JVI.00906-12. PubMed DOI PMC

Letko M, Seifert SN, Olival KJ, Plowright RK, Munster VJ. Bat-borne virus diversity, spillover and emergence. Nat. Rev. Microbiol. 2020;18:461–471. doi: 10.1038/s41579-020-0394-z. PubMed DOI PMC

Mollentze N, Streicker DG. Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts. P Natl Acad. Sci. USA. 2020;117:9423–9430. doi: 10.1073/pnas.1919176117. PubMed DOI PMC

Olival, K. J., Weekley, C. C. & Daszak, P. in Bats and Viruses: A New Frontier of Emerging Infectious Diseases (eds L. F. Wang & C. Cowled) Ch. 11, 281–294 (John Wiley & Sons, Inc., 2015).

Weber N, et al. Robust evidence for bats as reservoir hosts is lacking in most African virus studies: a review and call to optimize sampling and conserve bats. Biol. Lett. 2023;19:20230358. doi: 10.1098/rsbl.2023.0358. PubMed DOI PMC

Moreno Santillan DD, et al. Large-scale genome sampling reveals unique immunity and metabolic adaptations in bats. Mol. Ecol. 2021;30:6449–6467. doi: 10.1111/mec.16027. PubMed DOI

Pavlovich SS, et al. The Egyptian Rousette Genome Reveals Unexpected Features of Bat Antiviral Immunity. Cell. 2018;173:1098–1110 e1018. doi: 10.1016/j.cell.2018.03.070. PubMed DOI PMC

Dejosez M, et al. Bat pluripotent stem cells reveal unusual entanglement between host and viruses. Cell. 2023;186:957. doi: 10.1016/j.cell.2023.01.011. PubMed DOI PMC

O’Shea TJ, et al. Bat flight and zoonotic viruses. Emerg. Infect. Dis. 2014;20:741–745. doi: 10.3201/eid2005.130539. PubMed DOI PMC

Colombi, D. et al. Mechanisms for lyssavirus persistence in non-synanthropic bats in Europe: insights from a modeling study. Sci. Rep-Uk9, 537 (2019). PubMed PMC

Amorim F, Pita R, Mata VA, Beja P, Rebelo H. Crowding after sudden habitat loss affects demography and social structure in a bat population. J. Anim. Ecol. 2022;91:668–680. doi: 10.1111/1365-2656.13659. PubMed DOI

Cappelle, J. et al. Longitudinal monitoring in Cambodia suggests higher circulation of alpha and betacoronaviruses in juvenile and immature bats of three species. Sci. Rep.-Uk11, 24145 (2021). PubMed PMC

Wacharapluesadee, S. et al. Longitudinal study of age-specific pattern of coronavirus infection in Lyle’s flying fox (Pteropus lylei) in Thailand. Virol. J.15, 38 (2018). PubMed PMC

Herkt KMB, Barnikel G, Skidmore AK, Fahr J. A high-resolution model of bat diversity and endemism for continental Africa. Ecol. Model. 2016;320:9–28. doi: 10.1016/j.ecolmodel.2015.09.009. DOI

Amankwah, A. A. et al. Deforestation in forest-savannah transition zone of Ghana: Boabeng-Fiema monkey sanctuary. Glob. Ecol. Conserv.25, e01440 (2021).

Emmanuel AY, Jerry CS, Dzigbodi DA. Review of Environmental and Health Impacts of Mining in Ghana. J. Health Pollut. 2018;8:43–52. doi: 10.5696/2156-9614-8.17.43. PubMed DOI PMC

Nkrumah, E. E. et al. Diversity and Conservation of Cave-Roosting Bats in Central Ghana. Trop. Conserv. Sci.14, 1940-0829 (2021).

Tanalgo KC, Oliveira HFM, Hughes AC. Mapping global conservation priorities and habitat vulnerabilities for cave-dwelling bats in a changing world. Sci. Total Environ. 2022;843:156909. doi: 10.1016/j.scitotenv.2022.156909. PubMed DOI

Monadjem A, et al. Diversity of Hipposideridae in the Mount Nimba massif, West Africa, and the taxonomic status of Hipposideros lamottei. Acta Chiropterol. 2013;15:341–352. doi: 10.3161/150811013X678964. DOI

Patterson BD, et al. Evolutionary relationships and population genetics of the Afrotropical leaf-nosed bats (Chiroptera, Hipposideridae) Zookeys. 2020;929:117–161. doi: 10.3897/zookeys.929.50240. PubMed DOI PMC

Vallo P, Guillen-Servent A, Benda P, Pires DB, Koubek P. Variation of mitochondrial DNA in the Hipposideros caffer complex (Chiroptera: Hipposideridae) and its taxonomic implications. Acta Chiropterol. 2008;10:193–206. doi: 10.3161/150811008X414782. DOI

Baldwin HJ, et al. Concordant patterns of genetic, acoustic, and morphological divergence in the West African Old World leaf-nosed bats of the Hipposideros caffer complex. J. Zool. Syst. Evol. Res. 2021;59:1390–1407. doi: 10.1111/jzs.12506. DOI

Baldwin HJ, et al. Isolation and characterization of 11 novel microsatellite loci in a West African leaf-nosed bat, Hipposideros aff. ruber. BMC Res Notes. 2014;7:607. doi: 10.1186/1756-0500-7-607. PubMed DOI PMC

Pfefferle S, et al. Distant Relatives of Severe Acute Respiratory Syndrome Coronavirus and Close Relatives of Human Coronavirus 229E in Bats, Ghana. Emerg. Infect. Dis. 2009;15:1377–1384. doi: 10.3201/eid1509.090224. PubMed DOI PMC

Schmid DW, et al. MHC class II genes mediate susceptibility and resistance to coronavirus infections in bats. Mol. Ecol. 2023;32:3989–4002. doi: 10.1111/mec.16983. PubMed DOI

Annan A, et al. Human Betacoronavirus 2c EMC/2012-related Viruses in Bats, Ghana and Europe. Emerg. Infect. Dis. 2013;19:456–459. doi: 10.3201/eid1903.121503. PubMed DOI PMC

Foley NM, Goodman SM, Whelan CV, Puechmaille SJ, Teeling E. Towards navigating the Minotaur’s labyrinth: cryptic diversity and taxonomic revision within the speciose genus Hipposideros (Hipposideridae) Acta Chiropterol. 2017;19:1–18. doi: 10.3161/15081109ACC2017.19.1.001. DOI

Tao, Y. et al. Surveillance of Bat Coronaviruses in Kenya Identifies Relatives of Human Coronaviruses NL63 and 229E and Their Recombination History. J. Virol.91, e01953-16 (2017). PubMed PMC

Bourgarel M, et al. Circulation of Alphacoronavirus, Betacoronavirus and Paramyxovirus in Hipposideros bat species in Zimbabwe. Infect. Genet Evol. 2018;58:253–257. doi: 10.1016/j.meegid.2018.01.007. PubMed DOI PMC

Maganga, G. D. et al. Genetic diversity and ecology of coronaviruses hosted by cave-dwelling bats in Gabon. Sci. Rep.-Uk10, 7314 (2020). PubMed PMC

Joffrin, L. et al. Bat coronavirus phylogeography in the Western Indian Ocean. Sci. Rep.-Uk10, 6873 (2020). PubMed PMC

Ntumvi, N. F. et al. Wildlife in Cameroon harbor diverse coronaviruses, including many closely related to human coronavirus 229E. Virus Evol.8, veab110 (2022). PubMed PMC

Latinne, A. et al. Origin and cross-species transmission of bat coronaviruses in China. Nat. Commun.11, 4235 (2020). PubMed PMC

Montecino-Latorre, D. et al. Reproduction of East-African bats may guide risk mitigation for coronavirus spillover. One Health Outlook2, 2 (2020). PubMed PMC

Tao, Y. & Tong, S. X. Complete Genome Sequence of a Severe Acute Respiratory Syndrome-Related Coronavirus from Kenyan Bats. Microbiol. Resour. Ann.8, e00548-19 (2019). PubMed PMC

Tong SX, et al. Detection of Novel SARS-like and Other Coronaviruses in Bats from Kenya. Emerg. Infect. Dis. 2009;15:482–485. doi: 10.3201/eid1503.081013. PubMed DOI PMC

Anthony, S. J. et al. Global patterns in coronavirus diversity. Virus Evol.3, vex012 (2017). PubMed PMC

Hu, B. et al. Discovery of a rich gene pool of bat SARS-related coronaviruses provides new insights into the origin of SARS coronavirus. Plos Pathog.13, e1006698 (2017). PubMed PMC

Wang J, et al. Individual bat virome analysis reveals co-infection and spillover among bats and virus zoonotic potential. Nat. Commun. 2023;14:4079. doi: 10.1038/s41467-023-39835-1. PubMed DOI PMC

Powers RP, Jetz W. Global habitat loss and extinction risk of terrestrial vertebrates under future land-use-change scenarios. Nat. Clim. Change. 2019;9:323. doi: 10.1038/s41558-019-0406-z. DOI

Di Ponzio R, et al. Aerial insectivorous bat responses to 30 years of forest insularization in a dam-created Amazonian archipelagic landscape. Biol. Conserv. 2023;285:110222. doi: 10.1016/j.biocon.2023.110222. DOI

Nkrumah EE, et al. Estimating bat abundance and diversity in a modified tropical environment in central Ghana. Trop. Ecol. 2017;58:751–759.

Schwensow NI, et al. Disentangling direct from indirect effects of habitat disturbance on multiple components of biodiversity. J. Anim. Ecol. 2022;91:2220–2234. doi: 10.1111/1365-2656.13802. PubMed DOI

Keesing, F. & Ostfeld, R. S. Impacts of biodiversity and biodiversity loss on zoonotic diseases. P Natl Acad Sci USA118, e2023540118 (2021). PubMed PMC

Halliday FW, Rohr JR, Laine AL. Biodiversity loss underlies the dilution effect of biodiversity. Ecol. Lett. 2020;23:1611–1622. doi: 10.1111/ele.13590. PubMed DOI PMC

Ostfeld RS, LoGiudice K. Community disassembly, biodiversity loss, and the erosion of an ecosystem service. Ecology. 2003;84:1421–1427. doi: 10.1890/02-3125. DOI

Johnson PTJ, Preston DL, Hoverman JT, Richgels KLD. Biodiversity decreases disease through predictable changes in host community competence. Nature. 2013;494:230–233. doi: 10.1038/nature11883. PubMed DOI

Johnson PTJ, Thieltges DW. Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J. Exp. Biol. 2010;213:961–970. doi: 10.1242/jeb.037721. PubMed DOI

Civitello DJ, et al. Biodiversity inhibits parasites: Broad evidence for the dilution effect. Proc. Natl Acad. Sci. USA. 2015;112:8667–8671. doi: 10.1073/pnas.1506279112. PubMed DOI PMC

Ostfeld RS, Keesing F. Effects of Host Diversity on Infectious Disease. Annu Rev. Ecol. Evol. S. 2012;43:157–182. doi: 10.1146/annurev-ecolsys-102710-145022. DOI

Keesing F, et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature. 2010;468:647–652. doi: 10.1038/nature09575. PubMed DOI PMC

Ostfeld R, Keesing F. The function of biodiversity in the ecology of vector-borne zoonotic diseases. Can. J. Zool. 2000;78:2061–2078. doi: 10.1139/z00-172. DOI

Clay, C. A., Lehmer, E. M., Jeor, S. S. & Dearing, M. D. Sin Nombre Virus and Rodent Species Diversity: A Test of the Dilution and Amplification Hypotheses. Plos One4, e6467 (2009). PubMed PMC

Khalil, H., Ecke, F., Evander, M., Magnusson, M. & Hornfeldt, B. Declining ecosystem health and the dilution effect. Sci. Rep.-Uk6, 3131 (2016). PubMed PMC

Fearon, M. L. & Tibbetts, E. A. Pollinator community species richness dilutes prevalence of multiple viruses within multiple host species. Ecology102, e03305 (2021). PubMed

Suzan, G. et al. Experimental Evidence for Reduced Rodent Diversity Causing Increased Hantavirus Prevalence. Plos One4, e5461 (2009). PubMed PMC

Logiudice K, et al. Impact of Host Community Composition on Lyme Disease Risk. Ecology. 2008;89:2841–2849. doi: 10.1890/07-1047.1. PubMed DOI

Pilosof, S. et al. Host-parasite network structure is associated with community-level immunogenetic diversity. Nature Communications5, 5172 (2014). PubMed

Kocher A, et al. Biodiversity and vector-borne diseases: Host dilution and vector amplification occur simultaneously for Amazonian leishmaniases. Mol. Ecol. 2023;32:1817–1831. doi: 10.1111/mec.16341. PubMed DOI

Ferraguti, M. et al. A field test of the dilution effect hypothesis in four avian multi-host pathogens. Plos Pathog.17, e1009637 (2021). PubMed PMC

Young H, Griffin RH, Wood CL, Nunn CL. Does habitat disturbance increase infectious disease risk for primates? Ecol. Lett. 2013;16:656–663. doi: 10.1111/ele.12094. PubMed DOI

Gottdenker, N. L., Chaves, L. F., Calzada, J. E., Saldana, A. & Carroll, C. R. Host Life History Strategy, Species Diversity, and Habitat Influence Trypanosoma cruzi Vector Infection in Changing Landscapes. Plos. Neglect. Trop. D6, e1884 (2012). PubMed PMC

Ezenwa VO, Godsey MS, King RJ, Guptill SC. Avian diversity and West Nile virus: testing associations between biodiversity and infectious disease risk. P R. Soc. B-Biol. Sci. 2006;273:109–117. PubMed PMC

Occhibove, F., Kenobi, K., Swain, M. & Risley, C. An eco-epidemiological modeling approach to investigate dilution effect in two different tick-borne pathosystems. Ecol. Appl.32, e2550 (2022). PubMed PMC

Strauss AT, Civitello DJ, Caceres CE, Hall SR. Success, failure and ambiguity of the dilution effect among competitors. Ecol. Lett. 2015;18:916–926. doi: 10.1111/ele.12468. PubMed DOI

Huang ZYX, Van Langevelde F, Estrada-Pena A, Suzan G, De Boer WF. The diversity-disease relationship: evidence for and criticisms of the dilution effect. Parasitology. 2016;143:1075–1086. doi: 10.1017/S0031182016000536. PubMed DOI

Schmid J, et al. Ecological drivers of Hepacivirus infection in a neotropical rodent inhabiting landscapes with various degrees of human environmental change. Oecologia. 2018;188:289–302. doi: 10.1007/s00442-018-4210-7. PubMed DOI

Loss SR, et al. Avian host community structure and prevalence of West Nile virus in Chicago, Illinois. Oecologia. 2009;159:415–424. doi: 10.1007/s00442-008-1224-6. PubMed DOI

Luis AD, Kuenzi AJ, Mills JN. Species diversity concurrently dilutes and amplifies transmission in a zoonotic host-pathogen system through competing mechanisms. P Natl Acad. Sci. USA. 2018;115:7979–7984. doi: 10.1073/pnas.1807106115. PubMed DOI PMC

Ruiz-Aravena M, et al. Ecology, evolution and spillover of coronaviruses from bats. Nat. Rev. Microbiol. 2022;20:299. doi: 10.1038/s41579-021-00652-2. PubMed DOI PMC

Fleischer R, et al. Interaction between MHC diversity and constitution, gut microbiota and Astrovirus infections in a neotropical bat. Mol. Ecol. 2022;31:3342–3359. doi: 10.1111/mec.16491. PubMed DOI

Wasimuddin, et al. Astrovirus infections induce age-dependent dysbiosis in gut microbiomes of bats. Isme J. 2018;12:2883–2893. doi: 10.1038/s41396-018-0239-1. PubMed DOI PMC

Plowright, R. K. et al. Ecological countermeasures to prevent pathogen spillover and subsequent pandemics. Nat. Commun.15, 2577 (2024). PubMed PMC

MacFarlane, D. & Rocha, R. Guidelines for communicating about bats to prevent persecution in the time of COVID-19. Bio. Conserv.248, 108650 (2020). PubMed PMC

Ranger S, et al. Forming shared values in conservation management: An interpretive-deliberative-democratic approach to including community voices. Ecosyst. Serv. 2016;21:344–357. doi: 10.1016/j.ecoser.2016.09.016. DOI

Lepp A, Holland S. A comparison of attitudes toward state-led conservation and community-based conservation in the village of Bigodi, Uganda. Soc. Nat. Resour. 2006;19:609–623. doi: 10.1080/08941920600742377. DOI

Ayivor JS, Lawson ET, Ohemeng F, Ntiamoa-Baidu Y. Conservation perspectives and perception of bats as reservoirs of zoonotic diseases in Ghana. Hum. Dimens Wildl. 2023;28:516–530. doi: 10.1080/10871209.2022.2120650. DOI

Drexler JF, Corman VM, Drosten C. Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS. Antivir. Res. 2014;101:45–56. doi: 10.1016/j.antiviral.2013.10.013. PubMed DOI PMC

R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2023).

Halliday, F. W. & Rohr, J. R. Measuring the shape of the biodiversity-disease relationship across systems reveals new findings and key gaps. Nat. Commun.10, 5032 (2019). PubMed PMC

Bartoń, K. MuMIn: multi-model inference. https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf (2009).

Burnham KP, Anderson DR. Multimodel inference - understanding AIC and BIC in model selection. Socio. Method Res. 2004;33:261–304. doi: 10.1177/0049124104268644. DOI

Lüdecke D, Ben-Shachar MS, Patil I, Waggoner P, Makowski D. performance: An R Package for Assessment, Comparison and Testing of Statistical Models. J. Open Source Softw. 2021;6:3139. doi: 10.21105/joss.03139. DOI

Newest 20 citations...

See more in
Medvik | PubMed

Hibecovirus (genus Betacoronavirus) infection linked to gut microbial dysbiosis in bats

. 2025 Jan ; 5 (1) : ycae154. [epub] 20241216

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...