Seasonal Fluctuations of Astrovirus, But Not Coronavirus Shedding in Bats Inhabiting Human-Modified Tropical Forests

EcoHealth

Volumn 14, Issue 2, 2017, Pages 272-284

  Seltmann, Anne ^a,b   Corman, Victor M ^c,d   Rasche, Andrea ^c,d   Drosten, Christian ^c,d   Czirják, Gábor Á ^a   Bernard, Henry ^e   Struebig, Matthew J ^f   Voigt, Christian C ^a,b  

^a LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d German Center for Infection Research (DZIF)   (Germany)

^e UNIVERSITI MALAYSIA SABAH   (Malaysia)

^f UNIVERSITY OF KENT   (United Kingdom)

Author keywords

Astroviruses; Bats; Coinfection; Coronaviruses; Habitat fragmentation; Human modified landscapes

Indexed keywords

ANIMAL; ASTROVIRIDAE; BAT; CORONAVIRINAE; FOREST; PHYLOGENY; SEASON; VIROLOGY; VIRUS SHEDDING;

ANIMALS; ASTROVIRIDAE; CHIROPTERA; CORONAVIRUS; FORESTS; PHYLOGENY; SEASONS; VIRUS SHEDDING;

EID: 85019203425     PISSN: 16129202     EISSN: 16129210     Source Type: Journal    
DOI: 10.1007/s10393-017-1245-x     Document Type: Article

References (84)

1. Alexander J, Stimson WH (1988) Sex-hormones and the course of parasitic infection. Parasitology Today 4:189–193
2. Amman BR, Carroll SA, Reed ZD, Sealy TK, Balinandi S, Swanepoel R, Kemp A, Erickson BR, Comer JA, Campbell S, Cannon DL, Khristova ML, Atimnedi PA, Paddock CD, Kent Crockett RJ, Flietstra TD, Warfield KL, Unfer R, Katongole-Mbidde E, Downing R, Tappero JW, Zaki SR, Rollin PE, Ksiazek TG, Nichol ST, Towner JS (2012) Seasonal pulses of Marburg virus circulation in juvenile Rousettus aegyptiacus bats coincide with periods of increased risk of human infection. PLoS Pathogens 8(10):e1002877 (DOI: 10.1371/jouranl.ppat.100287) [Online October 4, 2012]
3. Annan A, Baldwin HJ, Corman VM, Klose SM, Owusu M, Nkrumah EE, Badu EK, Anti P, Agbenyega O, Meyer B, Oppong S, Sarkodie YA, Kalko EKV, Lina PHC, Godlevska EV, Reusken C, Seebens A, Gloza-Rausch F, Vallo P, Tschapka M, Drosten C, Drexler JF (2013) Human betacoronavirus 2c EMC/2012-related viruses in bats, Ghana and Europe. Emerging Infectious Diseases 19:456–459
4. Baker M, Schountz T, Wang LF (2013) Antiviral immune responses of bats: a review. Zoonoses and Public Health 60:104–116
5. Bates D, Maechler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1–48 (DOI: 10.18637/jss.v067.i01) [Online October 7, 2015]
6. Bradley CA, Gibbs SEJ, Altizer S (2008) Urban land use predicts West Nile virus exposure in songbirds. Ecological Applications 18:1083–1092
7. Brearley G, Rhodes J, Bradley A, Baxter G, Seabrook L, Lunney D, Liu Y, McAlpine C (2013) Wildlife disease prevalence in human-modified landscapes. Biological Reviews 88:427–442
8. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T (2006) Bats: important reservoir hosts of emerging viruses. Clinical Microbiology Reviews 19:531
9. Chu DKW, Poon LLM, Chan KH, Chen H, Guan Y, Yuen KY, Peiris JSM (2006) Coronaviruses in bent-winged bats (Miniopterus spp.). Journal of General Virology 87(9):2461–2466
10. Chu DKW, Poon LLM, Guan Y, Peiris JSM (2008) Novel astroviruses in insectivorous bats. Journal of Virology 82:9107–9114
11. Chu DKW, Peiris JSM, Poon LLM (2009) Novel coronaviruses and astroviruses in bats. Virologica Sinica 24(2):100–104
12. Chua KB, Chua BH, Wang CW (2002) Anthropogenic deforestation, El Niño and the emergence of Nipah virus in Malaysia. The Malaysian Journal of Pathology 24:15–21
13. Corman VM, Rasche A, Diallo TD, Cottontail VM, Stoecker A, de Carvalho Dominguez Souza BF, Correa JI, Borges Carneiro AJ, Franke CR, Nagy M, Metz M, Knoernschild M, Kalko EKV, Ghanem SJ, Sibaja Morales KD, Salsamendi E, Spinola M, Herrler G, Voigt CC, Tschapka M, Drosten C, Drexler JF (2013) Highly diversified coronaviruses in neotropical bats. Journal of General Virology 94:1984–1994
14. Corman VM, Ithete NL, Richards LR, Schoeman MC, Preiser W, Drosten C, Drexler JF (2014) Rooting the phylogenetic tree of Middle East respiratory syndrome coronavirus by characterization of a conspecific virus from an African bat. Journal of Virology 88(19):11297–11303
15. Cottontail VM, Wellinghausen N, Kalko EKV (2009) Habitat fragmentation and haemoparasites in the common fruit bat, Artibeus jamaicensis (Phyllostomidae) in a tropical lowland forest in Panama. Parasitology 136:1133–1145
16. de Souza Luna LK, Heiser V, Regamey N, Panning M, Drexler JF, Mulangu S, Poon L, Baumgarte S, Haijema BJ, Kaiser L (2007) Generic detection of coronaviruses and differentiation at the prototype strain level by reverse transcription-PCR and nonfluorescent low-density microarray. Journal of Clinical Microbiology 45:1049–1052
17. Dearing MD, Previtali MA, Jones JD, Ely PW, Wood BA (2009) Seasonal variation in Sin Nombre virus infections in deer mice: preliminary results. Journal of Wildlife Diseases 45:430–436
18. Dickens MJ, Romero LM (2013) A consensus endocrine profile for chronically stressed wild animals does not exist. General and Comparative Endocrinology 191:177–189
19. Dominguez SR, O’Shea TJ, Oko LM, Holmes KV (2007) Detection of group 1 coronaviruses in bats in North America. Emerging Infectious Diseases 13(9):1295–1300
20. Drexler JF, Corman VM, Wegner T, Tateno AF, Zerbinati RM, Gloza-Rausch F, Seebens A, Mueller MA, Drosten C (2011) Amplification of emerging viruses in a bat colony. Emerging Infectious Diseases 17:449–456
21. Drexler JF, Corman VM, Drosten C (2014) Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS. Antiviral Research 101:45–56
22. Epstein J, Field H (2015) Anthropogenic epedemics: the ecology of bat-borne viruses and our role in their emergence. In: Bats and Viruses: A New Frontier of Emerging Infectious Diseases, Wang LF, Cowled C (editors), Hoboken, NJ: Wiley, pp 249–280
23. Fischer K, Zeus V, Kwasnitschka L, Kerth G, Haase M, Groschup MH, Balkema-Buschmann A (2016) Insectivorous bats carry host specific astroviruses and coronaviruses across different regions in Germany. Infection Genetics and Evolution 37:108–116
24. Fitzherbert EB, Struebig MJ, Morel A, Danielsen F, Brühl CA, Donald PF, Phalan B (2008) How will oil palm expansion affect biodiversity? Trends in Ecology andEvolution 23:538–545
25. Fox J, Weisberg S (2011) An R Companion to Applied Regression, Thousand Oaks: SAGE
26. Gaveau DLA, Sloan S, Molidena E, Yaen H, Sheil D, Abram NK, Ancrenaz M, Nasi R, Quinones M, Wielaard N, Meijaard E (2014) Four decades of forest persistence, clearance and logging on Borneo. PLoS ONE 9(7):e101654 (DOI: 10.1371/journal.pone.0101654) [Online July 16, 2014]
27. Ge X-Y, Hu B, Shi Z (2015) Bat coronaviruses. In: Bats and Viruses: A New Frontier of Emerging Infectious Diseases, Wang LF, Cowled C (editors), Hoboke, New Jersey: Wiley, pp 127–156
28. George DB, Webb CT, Farnsworth ML, O’Shea TJ, Bowen RA, Smith DL, Stanley TR, Ellison LE, Rupprecht CE (2011). Host and viral ecology determine bat rabies seasonality and maintenance. Proceedings of the National Academy of Sciences 108(25):10208–10213
29. Gibbs SEJ, Wimberly MC, Madden M, Masour J, Yabsley MJ, Stallknecht DE (2006) Factors affecting the geographic distribution of West Nile virus in Georgia, USA: 2002–2004. Vector-Borne and Zoonotic Diseases 6:73–82
30. Gloza-Rausch F, Ipsen A, Seebens A, Goettsche M, Panning M, Drexler JF, Petersen N, Annan A, Grywna K, Mueller M, Pfefferle S, Drosten C (2008) Detection and prevalence patterns of group I coronaviruses in bats, northern Germany. Emerging Infectious Diseases 14:626–631
31. Hayman DTS, Fooks AR, Rowcliffe JM, McCrea R, Restif O, Baker KS, Horton DL, Suu-Ire R, Cunningham AA, Wood JLN (2012) Endemic Lagos bat virus infection in Eidolon helvum. Epidemiology and infection 140(12):2163–2171
32. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical Journal 50:346–363
33. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993
34. Kemenesi G, Dallos B, Goerfoel T, Boldogh S, Estók P, Kurucz K, Kutas A, Foeldes F, Oldal M, Németh V, Martella V, Bányai K, Jakab F (2014) Molecular survey of RNA viruses in Hungarian bats: discovering novel astroviruses, coronaviruses, and caliciviruses. Vector-Borne and Zoonotic Diseases 14(12): 846–855
35. Kingston T, Lim BL, Akbar Z (2006) Bats of Krau wildlife reserve, Penerbit UKM, Bangi: University Kebangsaan Malaysia
36. Kunz TH, Anthony THP (1982) Age estimation and post-natal growth in the bat Myotis lucifugus. Journal of Mammology 63(1):23–32
37. Kunz TH, Hodgkinson R, Weise CD (2009) Methods of Capturing and handling Bats. In: Ecological and Behavioral Methods for the Study of Bats, Kunz TH, Parsons S (editors), Baltimore, USA: The Johns Hopkins University Press, pp 3–35
38. Kunz TH, Weise CD (2009) Methods and devices for marking bats In: Ecological and Behavioral Methods for the Study of Bats, Kunz TH, Parsons S (editors), Baltimore, USA: The Johns Hopkins University Press, pp 36–56
39. Langlois JP, Fahrig L, Merriam G, Artsob H (2001) Landscape structure influences continental distribution of hantavirus in deer mice. Landscape Ecology 16:255–266
40. Langwig KE, Frick WF, Reynolds R, Parise KL, Drees KP, Hoyt JR, Tina LC, Kunz TH, Foster JT, Kilpatrick AM (2015) Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proceedings of the Royal Society of London B: Biological Sciences, 282:20142335 (DOI: 10.1098/rsb.2014.2335) [Online December 3, 2014]
41. Lau SKP, Li KSM, Huang Y, Shek C-T, Tse H, Wang M, Choi GKY, Xu H, Lam CSF, Guo R, Chan K-H, Zheng B-J, Woo PCY, Yuen K-Y (2010) Ecoepidemiology and complete genome comparison of different strains of severe acute respiratory syndrome-related Rhinolophus bat coronavirus in China reveal bats as a reservoir for acute, self-limiting infection that allows recombination events. Journal of Virology 84:2808–2819
42. Lehmer EM, Clay CA, Pearce-Duvet J, Jeor SS, Dearing MD (2008) Differential regulation of pathogens: the role of habitat disturbance in predicting prevalence of Sin Nombre virus. Oecologia 155:429–439
43. Li L, Victoria JG, Wang C, Jones M, Fellers GM, Kunz TH, Delwart E (2010) Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. Journal of Virology 84:6955–6965
44. Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang L-F (2005) Bats are natural reservoirs of SARS-like coronaviruses. Science 310:676–679
45. Luis AD, Hayman DTS, O’Shea TJ, Cryan PM, Gilbert AT, Pulliam JRC, Mills JN, Timonin ME, Willis CKR, Cunningham AA, Fooks AR, Rupprecht CE, Wood JLN, Webb CT (2013) A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proceedings of the Royal Society Biological Sciences Series B 280:20122753 (DOI: 10.1098/rspb.2012.2753) [Online February 1, 2013]
46. Mackelprang R, Dearing MD, St Jeor S (2001) High prevalence of Sin Nombre virus in rodent populations, central Utah: a consequence of human disturbance? Emerging Infectious Diseases 7:480–482
47. Marlier ME, DeFries RS, Kim PS, Koplitz SN, Jacob DJ, Mickley LJ, Myers SS (2015) Fire emissions and regional air quality impacts from fires in oil palm, timber, and logging concessions in Indonesia. Environmental Research Letters 10:085005 (DOI: 10.1088/1748-9326/10/8/085005) [Online August 12, 2015]
48. Meyer CF, Struebig MJ, Willig MR (2016) Responses of tropical bats to habitat fragmentation, logging, and deforestation. In: Bats in the Anthropocene: Conservation of Bats in a Changing World, Voigt CC, Kingston T (editors), Springer, pp 63–103
49. Morse SS, Mazet JAK, Woolhouse M, Parrish CR, Carroll D, Karesh WB, Zambrana-Torrelio C, Lipkin WI, Daszak P (2012) Prediction and prevention of the next pandemic zoonosis. Lancet 380:1956–1965
50. Nelson RJ, Demas GE, Klein SL, Kriegsfeld LJ (1995) The influence of season, photoperiod, and pineal melatonin on immune function. Journal of Pineal Research 19:149–165
51. Olival KJ, Weekley C & Daszak P (2015) Are bats really “special” as viral reservoirs? What we know and need to know. In: Bats and Viruses: a New Frontier of Emerging Infectious Diseases, Wang LF, Cowled C (editors), Hoboken, New Jersey: Wiley, pp 281–294
52. Payne J, Francis C, Phillipps K (1985) Field Guide to the Mammals of Borneo, Kota Kinabalu: Sabah Society, World Wildlife Fund Malaysia
53. Pernet O, Schneider BS, Beaty SM, LeBreton M, Yun TE, Park A, Zachariah TT, Bowden TA, Hitchens P, Ramirez CM, Daszak P, Mazet J, Freiberg AN, Wolfe ND, Lee B (2014) Evidence for henipavirus spillover into human populations in Africa. Nature Communications 5:5342 (DOI: 10.1038/ncomms6342) [Online November 18, 2014]
54. Pfefferle S, Oppong S, Drexler JF, Gloza-Rausch F, Ipsen A, Seebens A, Mueller MA, Annan A, Vallo P, Adu-Sarkodie Y, Kruppa TF, 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
55. Plowright RK, Field HE, Smith C, Divljan A, Palmer C, Tabor G, Daszak P, Foley JE (2008) Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proceedings of the Royal Society Biological Sciences Series B 275:861–869
56. Poon LLM, Chu DKW, Chan KH, Wong OK, Ellis TM, Leung YHC, Lau SKP, Woo PCY, Suen KY,Yuen KY, Guan Y, Peiris JSM (2005) Identification of a novel coronavirus in bats. Journal of Virology 79(4):2001–2009
57. Queen K, Shi M, Anderon LJ, Tong S (2015) Other bat-borne viruses. In: Bats and Viruses: A New Frontier of Emerging Infectious Diseases, Wang LF, Cowled C (editors), Hoboken, New Jersey: Wiley, pp 217–248
58. Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. General and Comparative Endocrinology 128:1–24
59. Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends in Ecology & Evolution 19:249–255
60. R Core Team (2015) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org (last accessed 22 February 2016)
61. Safronetz D, Lindsay R, Hjelle B, Medina RA, Mirowsky-Garcia K, Drebot MA (2006) Use of IgG avidity to indirectly monitor epizootic transmission of Sin Nombre virus in deer mice (Peromyscus maniculatus). American Journal of Tropical Medicine and Hygiene 75:1135–1139
62. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21:55–89
63. Schneeberger K, Voigt CC (2016) Zoonotic viruses and conservation of bats. In: Bats in the Anthropocene: Conservation of Bats in a Changing World, Voigt CC & Kingston T (editors), Springer, pp 263–292
64. Schneeberger K, Czirják GÁ, Voigt CC (2013) Measures of the constitutive immune system are linked to diet and roosting habits of neotropical bats. PLoS ONE 8: e54023 (DOI: 10.1371/journal.pone.0054023) [Online January 14, 2013]
65. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11:317–321
66. Shi Z (2010) Bat and virus. Protein & Cell 1(2):109–114
67. Smith I, Wang LF (2013) Bats and their virome: an important source of emerging viruses capable of infecting humans. Current Opinion in Virology 3:84–91
68. Steece R, Altenbach JS (1989) Prevalence of rabies specific antibodies in the Mexican free-tailed bat (Tadarida brasiliensis mexicana) at Lava Cave, New Mexico. Journal of Wildlife Diseases 25:490–496
69. Struebig MJ, Sujarno R (2006) Forest bat surveys using harp traps—a practical manual and identification key for the bats of Kalimantan, Indonesia, Balikpapan, Indonesia: The Kalimantan Bat Conservation Project and Bat Conservation International
70. Struebig MJ, Kingston T, Petit EJ, Le Comber SC, Zubaid A, Mohd-Adnan A, Rossiter SJ (2011) Parallel declines in species and genetic diversity in tropical forest fragments. Ecology Letters 14(6):582–590
71. Struebig MJ, Turner A, Giles E, Lasmana F, Tollington S, Bernard H, Bell D (2013) Quantifying the biodiversity value of repeatedly logged rainforests: gradient and comparative approaches from Borneo. Advances in Ecological Research 48:183–224
72. Suorsa P, Helle H, Koivunen V, Huhta E, Nikula A, Hakkarainen H (2004) Effects of forest patch size on physiological stress and immunocompetence in an area-sensitive passerine, the Eurasian treecreeper (Certhia familiaris): an experiment. Proceedings of the Royal Society B-Biological Sciences 271:435–440
73. Tang XC, Zhang JX, Zhang SY, Wang P, Fan XH, Li LF, Li G, Dong BQ, Liu W, Cheung CL, Xu KM, Song WJ, Vijaykrishna D, Poon LLM, Peiris JSM, Smith GJD, Chen H, Guan Y (2006) Prevalence and genetic diversity of coronaviruses in bats from China. Journal of Virology 80(15):7481–7490
74. Taylor LH, Latham SM, Woolhouse MEJ (2001) Risk factors for human disease emergence. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 356:983–989
75. Telfer S, Lambin X, Birtles R, Beldomenico P, Burthe S, Pterson S, Begon M (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science 330:243–246
76. Turmelle AS, Allen LC, Jackson FR, Kunz TH, Rupprecht CE, McCracken GF (2010) Ecology of rabies virus exposure in colonies of Brazilian free-tailed bats (Tadarida brasiliensis) at natural and man-made roosts in Texas. Vector-Borne and Zoonotic Diseases 10:165–175
77. Wacharapluesadee S, Boongird K, Wanghongsa S, Ratanasetyuth N, Supavonwong P, Saengsen D, Gongal GN, Hemachudha T (2010) A longitudinal study of the prevalence of Nipah virus in Pteropus lylei bats in Thailand: evidence for seasonal preference in disease transmission. Vector-Borne and Zoonotic Diseases 10:183–190
78. Wang LF, Walker PJ, Poon LLM (2011) Mass extinctions, biodiversity and mitochondrial function: are bats ‘special’ as reservoirs for emerging viruses? Current Opinion in Virology 1:649–657
79. Wikelski M, Cooke SJ (2006) Conservation physiology. Trends in Ecology & Evolution 21:38–46
80. Wingfield JC (2005) The concept of allostasis: coping with a capricious environment. Journal of Mammalogy 86:248–254
81. Woo PCY, Lau SKP, Huang Y, Yuen K-Y (2009) Coronavirus diversity, phylogeny and interspecies jumping. Experimental Biology and Medicine 234:1117–1127
82. Wood JLN, Leach M, Waldman L, MacGregor H, Fooks AR, Jones KE, Restif O, Dechmann D, Hayman DTS, Baker KS, Peel AJ, Kamins AO, Fahr J, Ntiamoa-Baidu Y, Suu-Ire R, Breiman RF, Epstein JH, Field HE, Cunningham AA (2012) A framework for the study of zoonotic disease emergence and its drivers: spillover of bat pathogens as a case study. Philosophical Transactions of the Royal Society B-Biological Sciences 367:2881–2892
83. Xiao J, Li J, Hu G, Chen Z, Wu Y, Chen Y, Chen Z, Liao Y, Zhou J, Ke X, Ma L, Liu S, Zhou J, Dai Y, Chen H, Yu S, Chen Q (2011) Isolation and phylogenetic characterization of bat astroviruses in southern China. Archives of Virology 156(8):1415–1423
84. Young CCW, Olival KJ (2016) Optimizing viral discovery in bats. PLoS ONE 11(2) (DOI: 10.1371/journal.pone.0149237) [Online February 11, 2016]