Bats act as reservoirs for a variety of zoonotic viruses, sometimes leading to spillover into humans and potential risks of global transmission. Viral shedding from bats is an essential prerequisite to bat-to-human viral transmission and understanding the timing and intensity of viral shedding from bats is critical to mitigate spillover risks. However, there are limited investigations on bats’ seasonal viral shedding patterns and their related risk factors. We conducted a comprehensive review of longitudinal studies on bat viruses with spillover potential to synthesize patterns of seasonal viral shedding and explore associated risk factors.
Methods:
We extracted data from 60 reviewed articles and obtained 1085 longitudinal sampling events. We analyzed viral shedding events using entropy values to quantitatively assess whether they occur in a consistent, pulsed pattern in a given season.
Results:
We found that clear seasonal shedding patterns were common in bats. Eight out of seventeen species-level analyses presented clear seasonal patterns. Viral shedding pulses often coincide with bats’ life cycles, especially in weaning and parturition seasons. Juvenile bats with waning maternal antibodies, pregnant bats undergoing immunity changes, and hibernation periods with decreased immune responses could be potential risk factors influencing seasonal shedding patterns.
Conclusion:
Based on our findings, we recommend future longitudinal studies on bat viruses that combine direct viral testing and serological testing, prioritize longitudinal research following young bats throughout their developmental stages, and broaden the geographical range of longitudinal studies on bat viruses based on current surveillance reports. Our review identified critical periods with heightened viral shedding for some viruses in bat species, which would help promote efforts to minimize spillovers and prevent outbreaks.
Get full access to this article
View all access options for this article.
References
1.
AguillonS, Le MinterG, LebarbenchonC, et al.A population in perpetual motion: Highly dynamic roosting behavior of a tropical island endemic bat. Ecol Evol, 2023; 13(2):e9814; doi: 10.1002/ece3.9814
2.
AmmanBR, CarrollSA, ReedZD, et al.Seasonal pulses of marburg virus circulation in juvenile rousettus aegyptiacus bats coincide with periods of increased risk of human infection. PLoS Pathog, 2012; 8(10):e1002877; doi: 10.1371/journal.ppat.1002877
3.
BakerKS, ToddS, MarshG, et al.Co-circulation of diverse paramyxoviruses in an urban African fruit bat population. J Gen Virol, 2012; 93(Pt 4):850–856; doi: 10.1099/vir.0.039339-0
4.
BanyardAC, EvansJS, LuoTR, FooksAR. Lyssaviruses and bats: Emergence and zoonotic threat. Viruses, 2014; 6(8):2974–2990; doi: 10.3390/v6082974
5.
BeckerDJ, BroosA, BergnerLM, et al.Temporal patterns of vampire bat rabies and host connectivity in Belize. Transbounding Emerging Dis, 2021; 68(2):870–879; doi: 10.1111/tbed.13754
6.
BeckerDJ, CrowleyDE, WashburneAD, PlowrightRK. Temporal and spatial limitations in global surveillance for bat filoviruses and henipaviruses. Biol Lett, 2019; 15(12):20190423; doi: 10.1098/rsbl.2019.0423
7.
BeckerDJ, EbyP, MaddenW, et al.Ecological conditions predict the intensity of Hendra virus excretion over space and time from bat reservoir hosts. Ecol Lett, 2023; 26(1):23–36; doi: 10.1111/ele.14007
8.
BeckerDJ, StreickerDG, AltizerS. Linking anthropogenic resources to wildlife–pathogen dynamics: A review and meta-analysis. Ecol Lett, 2015; 18(5):483–495; doi: 10.1111/ele.12428
9.
BoardmanWSJ, BakerML, BoydV, et al.Seroprevalence of three paramyxoviruses; Hendra virus, Tioman virus, Cedar virus and a rhabdovirus, Australian bat lyssavirus, in a range expanding fruit bat, the Grey-headed flying fox (Pteropus poliocephalus). PLoS One, 2020; 15(5):e0232339; doi: 10.1371/journal.pone.0232339
10.
BreedAC, BreedMF, MeersJ, FieldHE. Evidence of endemic Hendra virus infection in flying-foxes (Pteropus conspicillatus)—implications for disease risk management. PLoS One, 2011; 6(12):e28816; doi: 10.1371/journal.pone.0028816
11.
BrookCE, RanaivosonHC, BroderCC, et al.Disentangling serology to elucidate henipa- and filovirus transmission in Madagascar fruit bats. J Anim Ecol, 2019; 88(7):1001–1016; doi: 10.1111/1365-2656.12985
12.
CappelleJ, FureyN, HoemT, et al.Longitudinal monitoring in Cambodia suggests higher circulation of alpha and betacoronaviruses in juvenile and immature bats of three species. Sci Rep, 2021; 11(1):24145; doi: 10.1038/s41598-021-03169-z
13.
ChangulaK, KajiharaM, Mori-KajiharaA, et al.Seroprevalence of filovirus infection of rousettus aegyptiacus bats in Zambia. J Infect Dis, 2018; 218(Suppl 5):S312–S317; doi: 10.1093/infdis/jiy266
14.
CohenLE, FagreAC, ChenB, et al.Coronavirus sampling and surveillance in bats from 1996–2019: A systematic review and meta-analysis. Nat Microbiol, 2023; 8(6):1176–1186; doi: 10.1038/s41564-023-01375-1
15.
CrowleyD, BeckerD, WashburneA, PlowrightR. Identifying suspect bat reservoirs of emerging infections. Vaccines (Basel), 2020; 8(2); doi: 10.3390/vaccines8020228
16.
da RosaEST, KotaitI, BarbosaTFS, et al.Bat-transmitted human rabies outbreaks, Brazilian Amazon. Emerg Infect Dis, 2006; 12(8):1197–1202; doi: 10.3201/1208.050929
17.
HortonDL, BreedAC, ArnoldME, et al.Between roost contact is essential for maintenance of European bat lyssavirus type-2 in Myotis daubentonii bat reservoir: The Swarming Hypothesis. Sci Rep, 2020; 10(1):1740.
18.
DovihP, LaingED, ChenY, et al.Filovirus-reactive antibodies in humans and bats in Northeast India imply zoonotic spillover. PLoS Negl Trop Dis, 2019; 13(10):e0007733; doi: 10.1371/journal.pntd.0007733
19.
DrexlerJF, CormanVM, Gloza-RauschF, et al.Henipavirus RNA in African bats. PLoS One, 2009; 4(7):e6367; doi: 10.1371/journal.pone.0006367
20.
DrexlerJF, CormanVM, MüllerMA, et al.Bats host major mammalian paramyxoviruses. Nat Commun, 2012; 3:796; doi: 10.1038/ncomms1796
21.
EbyP, PeelAJ, HoeghA, et al.Pathogen spillover driven by rapid changes in bat ecology. Nature, 2023; 613(7943):340–344; doi: 10.1038/s41586-022-05506-2
22.
EpsteinJH, AnthonySJ, IslamA, et al.Nipah virus dynamics in bats and implications for spillover to humans. Proc Natl Acad Sci U S A, 2020; 117(46):29190–29201.
23.
EpsteinJH, BakerML, Zambrana-TorrelioC, et al.Duration of maternal antibodies against canine distemper virus and Hendra virus in pteropid bats. PLoS One, 2013; 8(6):e67584; doi: 10.1371/journal.pone.0067584
24.
FieldH, JongC D, MelvilleD, et al.Hendra virus infection dynamics in Australian fruit bats. PLoS One, 2011; 6(12):e28678; doi: 10.1371/journal.pone.0028678
25.
FischerK, Pinho dos ReisV, Balkema-BuschmannA. Bat astroviruses: Towards understanding the transmission dynamics of a neglected virus family. Viruses, 2017; 9(2); doi: 10.3390/v9020034
26.
FrenchSS, MooreMC, DemasGE. Ecological immunology: The organism in context. Integr Comp Biol, 2009; 49(3):246–253; doi: 10.1093/icb/icp032
27.
Garland-LewisG, WhittierC, MurrayS, et al.Occupational risks and exposures among wildlife health professionals. Ecohealth, 2017; 14(1):20–28; doi: 10.1007/s10393-017-1208-2
28.
GerowCM, RapinN, VoordouwMJ, et al.Arousal from hibernation and reactivation of Eptesicus fuscus gammaherpesvirus (EfHV) in big brown bats. Transbound Emerg Dis, 2019; 66(2):1054–1062; doi: 10.1111/tbed.13102
29.
HarrisSL, BrookesSM, JonesG, et al.European bat lyssaviruses: Distribution, prevalence and implications for conservation. Biol Conserv, 2006; 131(2):193–210; doi: 10.1016/j.biocon.2006.04.006
30.
HaymanDTS. Biannual birth pulses allow filoviruses to persist in bat populations. Proc Biol Sci, 2015; 282(1803):20142591; doi: 10.1098/rspb.2014.2591
31.
HoarauAO, KösterM, DietrichM, et al.Synchronicity of viral shedding in molossid bat maternity colonies. Epidemiol Infect, 2023; 151:e47.
32.
HurmeE, FahrJ, NetworkEM, et al.;Eidolon Monitoring Network. Fruit bat migration matches green wave in seasonal landscapes. Functional Ecology, 2022; 36(8):2043–2055; doi: 10.1111/1365-2435.14097
33.
JoffrinL, HoarauAOG, LagadecE, et al.Astrovirus in reunion free-tailed bat (Mormopterus francoismoutoui). Viruses, 2021; 13(8); doi: 10.3390/v13081524
34.
JoffrinL, HoarauAO, LagadecE, et al.Seasonality of coronavirus shedding in tropical bats. R Soc Open Sci, 2022; 9(2):211600.
35.
KesslerMK, BeckerDJ, PeelAJ, et al.Changing resource landscapes and spillover of henipaviruses. Annals of the New York Academy of Sciences, 2018; 1429(1):78–99; doi: 10.1111/nyas.13910
36.
KimY, LeopardiS, ScaravelliD, et al.Transmission dynamics of lyssavirus in Myotis myotis: Mechanistic modelling study based on longitudinal seroprevalence data. Proc Biol Sci, 2023; 290(1997):20230183.
37.
KrochmalAR, SparksDW. Timing of birth and estimation of age of juvenile myotis septentrionalis and myotis lucifugus in West-Central Indiana. Journal of Mammalogy, 2007; 88(3):649–656; doi: 10.1644/06-MAMM-A-140R.1
38.
KunzTH, Braun de TorrezE, BauerD, et al.Ecosystem services provided by bats. Annals of the New York Academy of Sciences, 2011; 1223:1–38; doi: 10.1111/j.1749-6632.2011.06004.x
39.
LeendertzSAJ, GogartenJF, DüxA, et al.Assessing the evidence supporting fruit bats as the primary reservoirs for ebola viruses. Ecohealth, 2016; 13(1):18–25; doi: 10.1007/s10393-015-1053-0
40.
LetkoM, SeifertSN, OlivalKJ, et al.Bat-borne virus diversity, spillover and emergence. Nat Rev Microbiol, 2020; 18(8):461–471; doi: 10.1038/s41579-020-0394-z
41.
LilleyTM, ProkkolaJM, JohnsonJS, et al.Immune responses in hibernating little brown myotis (Myotis lucifugus) with white-nose syndrome. Proc R Soc B, 2017; 284(1848):20162232; doi: 10.1098/rspb.2016.2232
42.
LiuZ, LiuQ, WangH, YaoX. Severe zoonotic viruses carried by different species of bats and their regional distribution. Clin Microbiol Infect, 2024; 30(2):206–210; doi: 10.1016/j.cmi.2023.09.025
43.
LiuD, ShiW, ShiY, et al.Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: Phylogenetic, structural, and coalescent analyses. Lancet, 2013; 381(9881):1926–1932; doi: 10.1016/S0140-6736(13)60938-1
44.
MaderaS, KistlerA, RanaivosonHC, et al.Discovery and genomic characterization of a Novel henipavirus, Angavokely virus, from fruit bats in Madagascar. J Virol, 2022; 96(18):e00921–e00922; doi: 10.1128/jvi.00921-22
45.
MagangaGD, BourgarelM, ValloP, et al.Bat distribution size or shape as determinant of viral richness in african bats. PLoS One, 2014; 9(6):e100172; doi: 10.1371/journal.pone.0100172
46.
MeteyerCU, BarberD, MandlJN. Pathology in euthermic bats with white nose syndrome suggests a natural manifestation of immune reconstitution inflammatory syndrome. Virulence, 2012; 3(7):583–588; doi: 10.4161/viru.22330
47.
MoherD, LiberatiA, TetzlaffJ, AltmanDG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Bmj, 2009; 339:b2535; doi: 10.1136/bmj.b2535
48.
Montecino-LatorreD, GoldsteinT, GilardiK, et al.;PREDICT Consortium. Reproduction of East-African bats may guide risk mitigation for coronavirus spillover. One Health Outlook, 2020; 2:2.
49.
MortlockM, DietrichM, WeyerJ, et al.Co-circulation and excretion dynamics of diverse rubula-and related viruses in Egyptian rousette bats from South Africa. Viruses, 2019; 11(1); doi: 10.3390/v11010037
50.
MortlockM, GeldenhuysM, DietrichM, et al.Seasonal shedding patterns of diverse henipavirus-related paramyxoviruses in Egyptian rousette bats. Sci Rep, 2021; 11(1):24262.
51.
MuzeniekT, PereraT, SiriwardanaS, et al.Paramyxovirus diversity within one population of miniopterus fuliginosus bats in Sri Lanka. Pathogens, 2022; 11(4); doi: 10.3390/pathogens11040434
52.
OlivalKJ, HaymanDTS. Filoviruses in bats: Current knowledge and future directions. Viruses, 2014; 6(4):1759–1788; doi: 10.3390/v6041759
53.
OlivalKJ, HosseiniPR, Zambrana-TorrelioC, et al.Host and viral traits predict zoonotic spillover from mammals. Nature, 2017; 546(7660):646–650; doi: 10.1038/nature22975
54.
OrłowskaA, SmreczakM, FreulingCM, et al.Serological survey of lyssaviruses in polish bats in the frame of passive rabies surveillance using an enzyme-linked immunosorbent assay. Viruses, 2020; 12(3); doi: 10.3390/v12030271
55.
PawcskaJT, van VurenPJ, KempA, StormN. Marburg Virus Infection in Egyptian Rousette Bats, South Africa, 2013–20141. Emerging Infect Dis, 2018.
56.
PeelAJ, BakerKS, HaymanDTS, et al.Support for viral persistence in bats from age-specific serology and models of maternal immunity. Sci Rep, 2018; 8(1):3859; doi: 10.1038/s41598-018-22236-6
57.
PeelAJ, WellsK, GilesJ, et al.Synchronous shedding of multiple bat paramyxoviruses coincides with peak periods of Hendra virus spillover. Emerg Microbes Infect, 2019; 8(1):1314–1323; doi: 10.1080/22221751.2019.1661217
58.
PlowrightRK, BeckerDJ, CrowleyDE, et al.Prioritizing surveillance of Nipah virus in India. PLoS Negl Trop Dis, 2019; 13(6):e0007393; doi: 10.1371/journal.pntd.0007393
59.
PlowrightRK, EbyP, HudsonPJ, et al.Ecological dynamics of emerging bat virus spillover. Proc Biol Sci, 2015; 282(1798):20142124; doi: 10.1098/rspb.2014.2124
60.
PlowrightRK, ParrishCR, McCallumH, et al.Pathways to zoonotic spillover. Nat Rev Microbiol, 2017; 15(8):502–510; doi: 10.1038/nrmicro.2017.45
61.
RahmanSA, HassanL, EpsteinJH, et al.;Henipavirus Ecology Research Group. Risk factors for Nipah virus infection among pteropid bats, Peninsular Malaysia. Emerg Infect Dis, 2013; 19(1):51–60; doi: 10.3201/eid1901.120221
62.
RamanantsalamaRV, GoodmanSM, DietrichM, LebarbenchonC. Interaction between Old World fruit bats and humans: From large scale ecosystem services to zoonotic diseases. Acta Trop, 2022; 231:106462; doi: 10.1016/j.actatropica.2022.106462
63.
RobardetE, BorelC, MoinetM, et al.Longitudinal survey of two serotine bat (Eptesicus serotinus) maternity colonies exposed to EBLV-1 (European Bat Lyssavirus type 1): Assessment of survival and serological status variations using capture-recapture models. PLoS Negl Trop Dis, 2017; 11(11):e0006048; doi: 10.1371/journal.pntd.0006048
64.
RochaR, AzizSA, BrookCE, et al.Bat conservation and zoonotic disease risk: A research agenda to prevent misguided persecution in the aftermath of COVID-19. Animal Conservation, 2021; 24(3):303–307; doi: 10.1111/acv.12636
65.
Ruiz-AravenaM, McKeeC, GambleA, et al.Ecology, evolution and spillover of coronaviruses from bats. Nat Rev Microbiol, 2022; 20(5):299–314; doi: 10.1038/s41579-021-00652-2
66.
RungeMC, GrantEHC, ColemanJTH, et al.Assessing the risks posed by SARS-CoV-2 in and via North American bats—Decision framing and rapid risk assessment. U.S. Geological Survey, 2020.
67.
SeltmannA, CormanVM, RascheA, et al.Seasonal fluctuations of astrovirus, but not coronavirus shedding in bats inhabiting human-modified tropical forests. Ecohealth, 2017; 14(2):272–284; doi: 10.1007/s10393-017-1245-x
68.
SharpPM, HahnBH. Origins of HIV and the AIDS pandemic. Cold Spring Harb Perspect Med, 2011; 1(1):a006841; doi: 10.1101/cshperspect.a006841
69.
ShivaprakashKN, SenS, PaulS, et al.Mammals, wildlife trade, and the next global pandemic. Curr Biol, 2021; 31(16):3671–3677.e3; doi: 10.1016/j.cub.2021.06.006
70.
SohayatiAR, HassanL, SharifahSH, et al.;Henipavirus Ecology Research Group. Evidence for Nipah virus recrudescence and serological patterns of captive Pteropus vampyrus. Epidemiol Infect, 2011; 139(10):1570–1579; doi: 10.1017/S0950268811000550
71.
SubudhiS, RapinN, MisraV. Immune system modulation and viral persistence in bats: Understanding viral spillover. Viruses, 2019; 11(2):192; doi: 10.3390/v11020192
72.
TurmelleAS, AllenLC, JacksonFR, et al.Ecology of rabies virus exposure in colonies of Brazilian free-tailed bats (Tadarida brasiliensis) at natural and man-made roosts in Texas. Vector Borne Zoonotic Dis, 2010a;10(2):165–175; doi: 10.1089/vbz.2008.0163
73.
TurmelleAS, JacksonFR, GreenD, et al.Host immunity to repeated rabies virus infection in big brown bats. J Gen Virol, 2010b;91(Pt 9):2360–2366; doi: 10.1099/vir.0.020073-0
74.
WacharapluesadeeS, BoongirdK, WanghongsaS, et al.A longitudinal study of the prevalence of Nipah virus in Pteropus lylei bats in Thailand: Evidence for seasonal preference in disease transmission. Vector Borne Zoonotic Dis, 2010; 10(2):183–190.
75.
WacharapluesadeeS, DuengkaeP, ChaiyesA, et al.Longitudinal study of age-specific pattern of coronavirus infection in Lyle’s flying fox (Pteropus lylei) in Thailand. Virol J, 2018; 15(1):38–10.
76.
WangL-F, AndersonDE. Viruses in bats and potential spillover to animals and humans. Curr Opin Virol, 2019; 34:79–89; doi: 10.1016/j.coviro.2018.12.007
77.
WeberMN, da SilvaMS. Corona- and paramyxoviruses in bats from Brazil: A matter of concern? Animals (Basel), 2023; 14(1):88; doi: 10.3390/ani14010088
78.
YangXL, ZhangYZ, JiangRD, GuoH. Genetically diverse filoviruses in Rousettus and Eonycteris spp. bats, China, 2009 and 2015. Emerging Infect Dis, 2017.
79.
ZhouH, JiJ, ChenX, et al.Identification of novel bat coronaviruses sheds light on the evolutionary origins of SARS-CoV-2 and related viruses. Cell, 2021; 184(17):4380–4391.e14; doi: 10.1016/j.cell.2021.06.008
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
