Advertisement

EcoHealth

, Volume 16, Issue 1, pp 82–94 | Cite as

Host Biology and Anthropogenic Factors Affect Hepadnavirus Infection in a Neotropical Bat

  • Thomas HillerEmail author
  • Andrea Rasche
  • Stefan Dominik Brändel
  • Alexander König
  • Lara Jeworowski
  • M. Teague O’Mara
  • Veronika Cottontail
  • Rachel A. Page
  • Dieter Glebe
  • Jan Felix Drexler
  • Marco Tschapka
Original Contribution

Abstract

The tent-making bat hepatitis B virus (TBHBV) is a hepadnavirus closely related to human hepatitis B virus. The ecology of TBHBV is unclear. We show that it is widespread and highly diversified in Peters’ tent-making bats (Uroderma bilobatum) within Panama, while local prevalence varied significantly between sample sites, ranging from 0 to 14.3%. Females showed significantly higher prevalence than males, and pregnant females were more often acutely infected than non-reproductive ones. The distribution of TBHBV in bats was significantly affected by forest cover, with higher infection rates in areas with lower forest cover. Our data indicate that loss of natural habitat may lead to positive feedback on the biotic factors driving infection possibility. These results underline the necessity of multidisciplinary studies for a better understanding of mechanisms in pathogen–host relationships and for predictions in disease ecology.

Keywords

Uroderma bilobatum Bat Habitat loss TBHBV Hepatitis B virus Orthohepadnavirus 

Notes

Acknowledgements

We want to thank the Smithsonian Tropical Research Institute, especially Oris Acevedo and Belkys Jimenez, for providing the infrastructure and logistics for field work. We are grateful to all people of the BCI and Gamboa BatLabs for help and assistance in the field. We further want to thank Nina Schwensow for a crash course in statistical analysis of molecular data and two anonymous reviewers who helped to improve the manuscript. This study was funded by German Research Foundation (DFG) SPP 1596 Grants DR 810/1-1, GL 595/4-1, and TS 81/6-1 (to J.F.D., M.T., and D.G.), which had no influence in study design or interpretation of the results.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10393_2018_1387_MOESM1_ESM.docx (59 kb)
Supplementary material 1 (DOCX 16 kb)
10393_2018_1387_MOESM2_ESM.docx (18 kb)
Supplementary material 2 (DOCX 17 kb)

References

  1. Acevedo-Whitehouse K, Duffus ALJ (2009) Effects of environmental change on wildlife health Philosophical Transactions of the Royal Society of London B: Biological Sciences 364:3429-3438CrossRefPubMedGoogle Scholar
  2. Aide TM, Clark ML, Grau HR, López-Carr D, Levy MA, Redo D, Bonilla-Moheno M, Riner G, Andrade-Núñez MJ, Muñiz M (2013) Deforestation and reforestation of Latin America and the Caribbean. Biotropica 45:262-271CrossRefGoogle Scholar
  3. Ashby B, Gupta S (2015) Sexually transmitted infections in polygamous mating systems Philosophical Transactions of the Royal Society B: Biological Sciences 368:20120048CrossRefGoogle Scholar
  4. Baker RJ, Clark CL (1987) Uroderma bilobatum Mammalian Species 279:1-4CrossRefGoogle Scholar
  5. Barton K (2016) MuMIn: multi-model inference. R package version 1.15.6. https://cran.r-project.org/package=MuMIn. Accessed 10 Oct 2016
  6. Bates D, Sarkar D, Bates MD, Matrix LT (2007) lme4: linear mixed-effects models using S4 classes. R Package version 0.99875-9. https://cran.r-project.org/package=lme4. Accessed 10 Oct 2016
  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 88:427-442CrossRefPubMedGoogle Scholar
  8. Brook CE, Dobson AP (2015) Bats as ‘special’ reservoirs for emerging zoonotic pathogens Trends in microbiology 23:172-180CrossRefPubMedGoogle Scholar
  9. Burnham KP, Anderson DR (2003) Model selection and multimodel inference: a practical information-theoretic approach. Berlin: Springer.Google Scholar
  10. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T (2006) Bats: Important reservoir hosts of emerging viruses. Clinical Microbiology Reviews 19:531-545CrossRefPubMedGoogle Scholar
  11. Campbell P, Akbar Z, Adnan AM, Kunz TH (2006) Resource distribution and social structure in harem-forming Old World fruit bats: variations on a polygynous theme Animal Behaviour 72:687-698CrossRefGoogle Scholar
  12. Chaverri G, Gamba-Rios M, Kunz TH (2007) Range overlap and association patterns in the tent-making bat Artibeus watsoni Animal Behaviour 73:157-164CrossRefGoogle Scholar
  13. Chaverri G, Kunz TH, Regina M (2010) Ecological determinants of social systems: perspectives on the functional role of roosting ecology in the social behavior of tent-roosting bats. In: Regina M (ed) Advances in the Study of Behavior, vol 42. Academic Press, London, pp 275-318.Google Scholar
  14. Chen C-J, Yang H-I, Iloeje UH, The R-HBVSG (2009) Hepatitis B virus DNA levels and outcomes in chronic hepatitis B Hepatology 49:S72-S84CrossRefPubMedGoogle Scholar
  15. Cottontail V, Wellinghausen N, Kalko E (2009) Habitat fragmentation and haemoparasites in the common fruit bat, Artibeus jamaicensis (Phyllostomidae) in a tropical lowland forest in Panamá. Parasitology 136:1133CrossRefPubMedGoogle Scholar
  16. Cunto GC, Bernard E (2012) Neotropical bats as indicators of environmental disturbance: what is the emerging message? Acta Chiropterologica 14:143-151CrossRefGoogle Scholar
  17. Drexler JF, Corman VM, Müller MA, Maganga GD, Vallo P, Binger T, Gloza-Rausch F, Rasche A, Yordanov S, Seebens A (2012) Bats host major mammalian paramyxoviruses Nature Communications 3:796CrossRefPubMedGoogle Scholar
  18. Drexler JF, Geipel A, König A, Corman VM, van Riel D, Leijten LM, Bremer CM, Rasche A, Cottontail VM, Maganga GD, Schlegel M, Müller MA, Adam A, Klose SM, Borges Carneiro AJ, Stöcker A, Franke CR, Gloza-Rausch F, Geyer J, Annan A, Adu-Sarkodie Y, Oppong S, Binger T, Vallo P, Tschapka M, Ulrich RG, Gerlich WH, Leroy E, Kuiken T, Glebe D, Drosten C (2013) Bats carry pathogenic hepadnaviruses antigenically related to hepatitis B virus and capable of infecting human hepatocytes Proceedings of the National Academy of Sciences 110:16151-16156CrossRefGoogle Scholar
  19. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7:214.CrossRefPubMedGoogle Scholar
  20. Ellis EC (2011) Anthropogenic transformation of the terrestrial biosphere Philosophical Transactions of the Royal Society of London A: Mathematical, Physical and Engineering Sciences 369:1010-1035CrossRefGoogle Scholar
  21. Ellis EC, Klein Goldewijk K, Siebert S, Lightman D, Ramankutty N (2010) Anthropogenic transformation of the biomes, 1700 to 2000 Global ecology and biogeography 19:589-606Google Scholar
  22. ESRI (2011) ArcGIS Desktop: Release 10. CA: Environmental Systems Research Institute.Google Scholar
  23. Estrada-Peña A, Ostfeld RS, Peterson AT, Poulin R, de la Fuente J (2014) Effects of environmental change on zoonotic disease risk: an ecological primer Trends in Parasitology 30:205-214CrossRefPubMedGoogle Scholar
  24. Fahrig L (2003) Effects of Habitat Fragmentation on Biodiversity. Annual review of ecology, evolution, and systematics 34:487-515CrossRefGoogle Scholar
  25. Fleming TH, Hooper ET, Wilson DE (1972) Three central american bat communities: structure, reproductive cycles, and movement patterns. Ecology 53:555-569CrossRefGoogle Scholar
  26. Gish RG, Given BD, Lai C-L, Locarnini SA, Lau JYN, Lewis DL, Schluep T (2015) Chronic hepatitis B: Virology, natural history, current management and a glimpse at future opportunities. Antiviral Research 121:47-58CrossRefPubMedGoogle Scholar
  27. Glebe D, Bremer CM (2013) The molecular virology of hepatitis B virus. In: Seminars in liver disease, vol 2. New York: Thieme Medical Publishers, pp 103-112Google Scholar
  28. Handley COW, Gardner AL (1991) Demography and natural history of the common fruit bat, Artibeus jamaicensis, on Barro Colorado Island, Panamá. Smithsonian Contributions to Zoology Google Scholar
  29. Hansen MC, Potapov PV, Moore R, Hancher M, Turubanova SA, Tyukavina A, Thau D, Stehman SV, Goetz SJ, Loveland TR, Kommareddy A, Egorov A, Chini L, Justice CO, Townshend JRG (2013) High-resolution global maps of 21st-century forest cover change. Science 342:850–853 (Data available on-line from: http://earthenginepartners.appspot.com/science-2013-global-forest)
  30. Hayman DTS, Bowen RA, Cryan PM, McCracken GF, O’Shea TJ, Peel AJ, Gilbert A, Webb CT, Wood JLN (2013) Ecology of Zoonotic Infectious Diseases in Bats: Current Knowledge and Future Directions Zoonoses and public health 60:2-21CrossRefPubMedGoogle Scholar
  31. He B, Fan Q, Yang F, Hu T, Qiu W, Feng Y, Li Z, Li Y, Zhang F, Guo H, Zou X, Tu C (2013) Hepatitis Virus in Long-Fingered Bats, Myanmar Emerging infectious diseases 19:638-640CrossRefPubMedGoogle Scholar
  32. He B, Zhang F, Xia L, Hu T, Chen G, Qiu W, Fan Q, Feng Y, Guo H, Tu C (2015) Identification of a novel orthohepadnavirus in pomona roundleaf bats in China Archives of Virology 160:335-337CrossRefPubMedGoogle Scholar
  33. Jones G, Jacobs DS, Kunz TH, Willig MR, Racey PA (2009) Carpe noctem: the importance of bats as bioindicators Endangered Species Research 8:93-115CrossRefGoogle Scholar
  34. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases Nature 451:990-993CrossRefPubMedGoogle Scholar
  35. Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk Ecology Letters 9:485-498CrossRefPubMedGoogle Scholar
  36. Kerth G, Safi K, König B (2002) Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein’s bat (Myotis bechsteinii). Behavioral Ecology and Sociobiology 52:203-210CrossRefGoogle Scholar
  37. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870-1874CrossRefPubMedGoogle Scholar
  38. Kunz TH (1982) Roosting ecology of bats. In: Kunz TH (ed) Ecology of bats. Plenum Press, New York, pp 1 - 51.CrossRefGoogle Scholar
  39. Kunz TH, Braun de Torrez E, Bauer D, Lobova T, Fleming TH (2011) Ecosystem services provided by bats Annals of the New York Academy of Sciences 1223:1-38CrossRefPubMedGoogle Scholar
  40. Laurance WF, Camargo JLC, Luizão RCC, Laurance SG, Pimm SL, Bruna EM, Stouffer PC, Bruce Williamson G, Benítez-Malvido J, Vasconcelos HL, Van Houtan KS, Zartman CE, Boyle SA, Didham RK, Andrade A, Lovejoy TE (2011) The fate of Amazonian forest fragments: a 32-year investigation. Biological Conservation 144:56-67CrossRefGoogle Scholar
  41. Lewis SE (1992) Behavior of Peter’s tent-making bat, Uroderma bilobatum, at maternity roosts in Costa Rica Journal of Mammalogy 73:541-546CrossRefGoogle Scholar
  42. Liang TJ (2009) Hepatitis B: The virus and disease Hepatology 49:13-21CrossRefGoogle Scholar
  43. Littlejohn M, Locarnini S, Yuen L (2016) Origins and evolution of hepatitis B virus and hepatitis D virus. Cold Spring Harbor Perspectives in Medicine 6:a021360CrossRefPubMedGoogle Scholar
  44. Locarnini S, Littlejohn M, Aziz MN, Yuen L (2013) Possible origins and evolution of the hepatitis B virus (HBV). In: Seminars in Cancer Biology, vol 6. Amsterdam: Elsevier, pp 561-575Google Scholar
  45. Lüdecke D (2017) ggeffects: Create Tidy Data Frames of Marginal Effects for ‘ggplot’ from Model Outputs vol R package version 0.2.1. URL https://CRAN.R-project.org/package=ggeffects. Accessed 10 Oct 2016
  46. 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 of London B: Biological Sciences 280:20122753CrossRefGoogle Scholar
  47. Mantilla-Meluk H (ed) (2014) Defining Species and Species Boundaries in Uroderma (Chiroptera: Phyllostomidae) with a Description of a New Species, vol 325. Occasional Papers of the Museum of Texas Tech University. Museum of Texas Tech UniversityGoogle Scholar
  48. Menne S, Cote PJ (2007) The woodchuck as an animal model for pathogenesis and therapy of chronic hepatitis B virus infection World Journal of Gastroenterology 13:104CrossRefPubMedGoogle Scholar
  49. Meyer CF, Kalko EKV, Kerth G (2009) Small-scale fragmentation effects on local genetic diversity in two phyllostomid bats with different dispersal abilities in Panama Biotropica 41:95-102CrossRefGoogle Scholar
  50. O’Mara MT, Dechmann DKN, Page RA (2014) Frugivorous bats evaluate the quality of social information when choosing novel foods Behavioral Ecology 25:1233-1239CrossRefGoogle Scholar
  51. O’Mara MT, Wikelski M, Voigt CC, Ter Maat A, Pollock HS, Burness G, Desantis LM, Dechmann DK (2017) Cyclic bouts of extreme bradycardia counteract the high metabolism of frugivorous bats eLife 6:e26686CrossRefPubMedGoogle Scholar
  52. Oksanen J, Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara R, Simpson G, Solymos P, Stevens M, Szoecs E, Wagner H (2016) vegan: Community ecology package. R package version 2.4-1. URL https://CRAN.R-project.org/package=vegan. Accessed 10 Oct 2016
  53. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290CrossRefPubMedGoogle Scholar
  54. Parker J, Rambaut A, Pybus OG (2008) Correlating viral phenotypes with phylogeny: Accounting for phylogenetic uncertainty Infection, Genetics and Evolution 8:239-246CrossRefGoogle Scholar
  55. R Development Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  56. Ramakers JJ, Dechmann DK, Page RA, O’Mara MT (2016) Frugivorous bats prefer information from novel social partners Animal Behaviour 116:83-87CrossRefGoogle Scholar
  57. Rasche A, Souza BFdCD, Drexler JF (2016) Bat hepadnaviruses and the origins of primate hepatitis B viruses Current Opinion in Virology 16:86-94CrossRefPubMedGoogle Scholar
  58. Rodríguez-Herrera B, Medellín R, Timm R (eds) (2007) Murciélagos neotropicales que acampan en hojas. Neotropical tent-roosting bats. Ecosistemas de Costa Rica. INBio.Google Scholar
  59. Rønsholt L, Sörensen KJ, Bruschke CJM, Wellenberg GJ, van Oirschot JT, Johnstone P, Whitby JE, Bourhy H (1998) Clinically silent rabies infection in (zoo) bats. Veterinary Record 142:519-520CrossRefPubMedGoogle Scholar
  60. Sagot M, Rodríguez-Herrera B, Stevens RD (2013) Macro and Microhabitat Associations of the Peter’s Tent-Roosting Bat (Uroderma bilobatum): Human-Induced Selection and Colonization? Biotropica 45:511-519CrossRefGoogle Scholar
  61. Sagot M, Stevens RD (2012) The Evolution of Group Stability and Roost Lifespan: Perspectives from Tent-Roosting Bats Biotropica 44:90-97CrossRefGoogle Scholar
  62. Seeger C, Mason WS (2000) Hepatitis B virus biology Microbiology and Molecular Biology Reviews 64:51-68CrossRefPubMedGoogle Scholar
  63. Seim I, Fang X, Xiong Z, Lobanov AV, Huang Z, Ma S, Feng Y, Turanov AA, Zhu Y, Lenz TL, Gerashchenko MV, Fan D, Hee Yim S, Yao X, Jordan D, Xiong Y, Ma Y, Lyapunov AN, Chen G, Kulakova OI, Sun Y, Lee S-G, Bronson RT, Moskalev AA, Sunyaev SR, Zhang G, Krogh A, Wang J, Gladyshev VN (2013) Genome analysis reveals insights into physiology and longevity of the Brandt’s bat Myotis brandtii. Nature Communications 4:2212CrossRefPubMedGoogle Scholar
  64. Sharifi M, Mozafari F, Taghinezhad N, Javanbakht H (2008) Variation in Ectoparasite Load Reflects Life History Traits in the Lesser Mouse-eared Bat Myotis blythii (Chiroptera: Vespertilionidae) in Western Iran. Journal of Parasitology 94:622-625CrossRefPubMedGoogle Scholar
  65. Sloan RD, Ijaz S, Moore PL, Harrison TJ, Teo C-G, Tedder RS (2008) Antiviral resistance mutations potentiate hepatitis B virus immune evasion through disruption of its surface antigen a determinant Antiviral therapy 13:439PubMedGoogle Scholar
  66. Streicker DG, Recuenco S, Valderrama W, Gomez Benavides J, Vargas I, Pacheco V, Condori Condori RE, Montgomery J, Rupprecht CE, Rohani P, Altizer S (2012) Ecological and anthropogenic drivers of rabies exposure in vampire bats: implications for transmission and control Proceedings of the Royal Society of London B: Biological Sciences 279:3384Google Scholar
  67. Suzán G, Armién A, Mills JN, Marcé E, Ceballos G, Ávila M, Salazar-Bravo J, Ruedas L, Armién B, Yates TL (2008) Epidemiological Considerations of Rodent Community Composition in Fragmented Landscapes in Panama Journal of Mammalogy 89:684-690CrossRefGoogle Scholar
  68. Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behavioral Ecology and Sociobiology 65:13-21CrossRefGoogle Scholar
  69. Timm RM, Lewis SE (1991) Tent construction and use by Uroderma bilobatum in coconut palms (Cocos nucifera) in Costa Rica. Bulletin of the American Museum of Natural History 206:251-260Google Scholar
  70. Van der Poel WHM, Van der Heide R, Van Amerongen G, Van Keulen LJM, Wellenberg GJ, Bourhy H, Schaftenaar W, Groen J, Osterhaus ADME (2000) Characterisation of a recently isolated lyssavirus in frugivorous zoo bats Archives of Virology 145:1919-1931CrossRefPubMedGoogle Scholar
  71. Villalobos-Chaves D, Bonaccorso FJ, Rodríguez-Herrera B, Cordero-Schmidt E, Arias-Aguilar A, Todd CM (2016) The Influence of Sex and Reproductive Status on Foraging Behavior and Seed Dispersal by Uroderma convexum (Chiroptera: Phyllostomidae). In: Ortega J (ed) Sociality in Bats. Springer International Publishing, Cham, pp 281-301.Google Scholar
  72. Wang B-J, Tian Y-J, Meng Z-J, Jiang M, Wei B-Q, Tao Y-Q, Fan W, Li A-Y, Bao J-J, Li X-Y, Zhang Z-M, Wang Z-D, Wang H, Roggendorf M, Lu M-J, Yang D-L (2011) Establishing a new animal model for hepadnaviral infection: susceptibility of Chinese Marmota-species to woodchuck hepatitis virus infection Journal of General Virology 92:681-691CrossRefPubMedGoogle Scholar
  73. World Health Organization (2016) Hepatitis B fact sheet 2016. URL: http://www.who.int/mediacentre/factsheets/fs204/en/. Accessed July 2016
  74. World Health Organization (2017) Global Hepatitis Report 2017. GenevaGoogle Scholar
  75. Zuur AF (2010) AED: Data files used in Mixed effects models and extensions in ecology with RGoogle Scholar
  76. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems Methods in Ecology and Evolution 1:3-14CrossRefGoogle Scholar

Copyright information

© EcoHealth Alliance 2018

Authors and Affiliations

  • Thomas Hiller
    • 1
    • 2
    Email author
  • Andrea Rasche
    • 3
    • 4
    • 5
  • Stefan Dominik Brändel
    • 1
    • 2
  • Alexander König
    • 6
    • 7
    • 8
  • Lara Jeworowski
    • 9
  • M. Teague O’Mara
    • 2
    • 10
    • 11
  • Veronika Cottontail
    • 1
  • Rachel A. Page
    • 2
  • Dieter Glebe
    • 6
    • 7
    • 8
  • Jan Felix Drexler
    • 3
    • 4
    • 5
    • 9
  • Marco Tschapka
    • 1
    • 2
  1. 1.Institute for Evolutionary Ecology and Conservation GenomicsUniversity of UlmUlmGermany
  2. 2.Smithsonian Tropical Research InstituteBalboa, AnconRepublic of Panama
  3. 3.Corporate Member of Freie Universität Berlin, Humboldt-Universität zu BerlinCharité – Universitätsmedizin BerlinBerlinGermany
  4. 4.Berlin Institute of Health, Institute of VirologyBerlinGermany
  5. 5.German Center for Infection Research (DZIF), Partner Site Bonn-CologneCologneGermany
  6. 6.Institute of Medical VirologyJustus Liebig UniversityGiessenGermany
  7. 7.German Reference Center for Hepatitis B and D VirusesJustus Liebig UniversityGiessenGermany
  8. 8.German Center for Infection Research (DZIF), Partner Site Giessen-Marburg-LangenGiessenGermany
  9. 9.Institute of VirologyUniversity of Bonn Medical CentreBonnGermany
  10. 10.Department of Migration and Immuno-EcologyMax Planck Institute for OrnithologyRadolfzellGermany
  11. 11.Department of BiologyUniversity of KonstanzConstanceGermany

Personalised recommendations