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Erschienen in: EcoHealth 1/2019

18.12.2018 | Original Contribution

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

verfasst von: Thomas Hiller, 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

Erschienen in: EcoHealth | Ausgabe 1/2019

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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.
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Literatur
Zurück zum Zitat Acevedo-Whitehouse K, Duffus ALJ (2009) Effects of environmental change on wildlife health Philosophical Transactions of the Royal Society of London B: Biological Sciences 364:3429-3438CrossRefPubMed Acevedo-Whitehouse K, Duffus ALJ (2009) Effects of environmental change on wildlife health Philosophical Transactions of the Royal Society of London B: Biological Sciences 364:3429-3438CrossRefPubMed
Zurück zum Zitat 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 45:262-271CrossRef 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 45:262-271CrossRef
Zurück zum Zitat Ashby B, Gupta S (2015) Sexually transmitted infections in polygamous mating systems Philosophical Transactions of the Royal Society B: Biological Sciences 368:20120048CrossRef Ashby B, Gupta S (2015) Sexually transmitted infections in polygamous mating systems Philosophical Transactions of the Royal Society B: Biological Sciences 368:20120048CrossRef
Zurück zum Zitat Baker RJ, Clark CL (1987) Uroderma bilobatum Mammalian Species 279:1-4CrossRef Baker RJ, Clark CL (1987) Uroderma bilobatum Mammalian Species 279:1-4CrossRef
Zurück zum Zitat 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 88:427-442CrossRefPubMed 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 88:427-442CrossRefPubMed
Zurück zum Zitat Brook CE, Dobson AP (2015) Bats as ‘special’ reservoirs for emerging zoonotic pathogens Trends in microbiology 23:172-180CrossRefPubMed Brook CE, Dobson AP (2015) Bats as ‘special’ reservoirs for emerging zoonotic pathogens Trends in microbiology 23:172-180CrossRefPubMed
Zurück zum Zitat Burnham KP, Anderson DR (2003) Model selection and multimodel inference: a practical information-theoretic approach. Berlin: Springer. Burnham KP, Anderson DR (2003) Model selection and multimodel inference: a practical information-theoretic approach. Berlin: Springer.
Zurück zum Zitat Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T (2006) Bats: Important reservoir hosts of emerging viruses. Clinical Microbiology Reviews 19:531-545CrossRefPubMedPubMedCentral Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T (2006) Bats: Important reservoir hosts of emerging viruses. Clinical Microbiology Reviews 19:531-545CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 72:687-698CrossRef 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 72:687-698CrossRef
Zurück zum Zitat Chaverri G, Gamba-Rios M, Kunz TH (2007) Range overlap and association patterns in the tent-making bat Artibeus watsoni Animal Behaviour 73:157-164CrossRef Chaverri G, Gamba-Rios M, Kunz TH (2007) Range overlap and association patterns in the tent-making bat Artibeus watsoni Animal Behaviour 73:157-164CrossRef
Zurück zum Zitat 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. 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.
Zurück zum Zitat 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-S84CrossRefPubMed 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-S84CrossRefPubMed
Zurück zum Zitat 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 136:1133CrossRefPubMed 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 136:1133CrossRefPubMed
Zurück zum Zitat Cunto GC, Bernard E (2012) Neotropical bats as indicators of environmental disturbance: what is the emerging message? Acta Chiropterologica 14:143-151CrossRef Cunto GC, Bernard E (2012) Neotropical bats as indicators of environmental disturbance: what is the emerging message? Acta Chiropterologica 14:143-151CrossRef
Zurück zum Zitat 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 3:796CrossRefPubMedPubMedCentral 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 3:796CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 110:16151-16156CrossRef 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 110:16151-16156CrossRef
Zurück zum Zitat Ellis EC (2011) Anthropogenic transformation of the terrestrial biosphere Philosophical Transactions of the Royal Society of London A: Mathematical, Physical and Engineering Sciences 369:1010-1035CrossRef Ellis EC (2011) Anthropogenic transformation of the terrestrial biosphere Philosophical Transactions of the Royal Society of London A: Mathematical, Physical and Engineering Sciences 369:1010-1035CrossRef
Zurück zum Zitat Ellis EC, Klein Goldewijk K, Siebert S, Lightman D, Ramankutty N (2010) Anthropogenic transformation of the biomes, 1700 to 2000 Global ecology and biogeography 19:589-606 Ellis EC, Klein Goldewijk K, Siebert S, Lightman D, Ramankutty N (2010) Anthropogenic transformation of the biomes, 1700 to 2000 Global ecology and biogeography 19:589-606
Zurück zum Zitat ESRI (2011) ArcGIS Desktop: Release 10. CA: Environmental Systems Research Institute. ESRI (2011) ArcGIS Desktop: Release 10. CA: Environmental Systems Research Institute.
Zurück zum Zitat 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 30:205-214CrossRefPubMed 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 30:205-214CrossRefPubMed
Zurück zum Zitat Fahrig L (2003) Effects of Habitat Fragmentation on Biodiversity. Annual review of ecology, evolution, and systematics 34:487-515CrossRef Fahrig L (2003) Effects of Habitat Fragmentation on Biodiversity. Annual review of ecology, evolution, and systematics 34:487-515CrossRef
Zurück zum Zitat Fleming TH, Hooper ET, Wilson DE (1972) Three central american bat communities: structure, reproductive cycles, and movement patterns. Ecology 53:555-569CrossRef Fleming TH, Hooper ET, Wilson DE (1972) Three central american bat communities: structure, reproductive cycles, and movement patterns. Ecology 53:555-569CrossRef
Zurück zum Zitat 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 121:47-58CrossRefPubMed 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 121:47-58CrossRefPubMed
Zurück zum Zitat 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 103-112 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 103-112
Zurück zum Zitat 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 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
Zurück zum Zitat 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 60:2-21CrossRefPubMedPubMedCentral 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 60:2-21CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 19:638-640CrossRefPubMedPubMedCentral 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 19:638-640CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 160:335-337CrossRefPubMed 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 160:335-337CrossRefPubMed
Zurück zum Zitat Jones G, Jacobs DS, Kunz TH, Willig MR, Racey PA (2009) Carpe noctem: the importance of bats as bioindicators Endangered Species Research 8:93-115CrossRef Jones G, Jacobs DS, Kunz TH, Willig MR, Racey PA (2009) Carpe noctem: the importance of bats as bioindicators Endangered Species Research 8:93-115CrossRef
Zurück zum Zitat Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases Nature 451:990-993CrossRefPubMedPubMedCentral Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases Nature 451:990-993CrossRefPubMedPubMedCentral
Zurück zum Zitat Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk Ecology Letters 9:485-498CrossRefPubMed Keesing F, Holt RD, Ostfeld RS (2006) Effects of species diversity on disease risk Ecology Letters 9:485-498CrossRefPubMed
Zurück zum Zitat 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 52:203-210CrossRef 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 52:203-210CrossRef
Zurück zum Zitat Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870-1874CrossRefPubMed Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33:1870-1874CrossRefPubMed
Zurück zum Zitat Kunz TH (1982) Roosting ecology of bats. In: Kunz TH (ed) Ecology of bats. Plenum Press, New York, pp 1 - 51.CrossRef Kunz TH (1982) Roosting ecology of bats. In: Kunz TH (ed) Ecology of bats. Plenum Press, New York, pp 1 - 51.CrossRef
Zurück zum Zitat 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 1223:1-38CrossRefPubMed 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 1223:1-38CrossRefPubMed
Zurück zum Zitat 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 144:56-67CrossRef 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 144:56-67CrossRef
Zurück zum Zitat Lewis SE (1992) Behavior of Peter’s tent-making bat, Uroderma bilobatum, at maternity roosts in Costa Rica Journal of Mammalogy 73:541-546CrossRef Lewis SE (1992) Behavior of Peter’s tent-making bat, Uroderma bilobatum, at maternity roosts in Costa Rica Journal of Mammalogy 73:541-546CrossRef
Zurück zum Zitat Liang TJ (2009) Hepatitis B: The virus and disease Hepatology 49:13-21CrossRef Liang TJ (2009) Hepatitis B: The virus and disease Hepatology 49:13-21CrossRef
Zurück zum Zitat 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:a021360CrossRefPubMedPubMedCentral 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:a021360CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 561-575 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 561-575
Zurück zum Zitat 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 280:20122753CrossRef 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 280:20122753CrossRef
Zurück zum Zitat 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 University 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 University
Zurück zum Zitat 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 13:104CrossRefPubMedPubMedCentral 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 13:104CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 41:95-102CrossRef 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 41:95-102CrossRef
Zurück zum Zitat O’Mara MT, Dechmann DKN, Page RA (2014) Frugivorous bats evaluate the quality of social information when choosing novel foods Behavioral Ecology 25:1233-1239CrossRef O’Mara MT, Dechmann DKN, Page RA (2014) Frugivorous bats evaluate the quality of social information when choosing novel foods Behavioral Ecology 25:1233-1239CrossRef
Zurück zum Zitat 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:e26686CrossRefPubMedPubMedCentral 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:e26686CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 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
Zurück zum Zitat Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290CrossRefPubMed Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289-290CrossRefPubMed
Zurück zum Zitat Parker J, Rambaut A, Pybus OG (2008) Correlating viral phenotypes with phylogeny: Accounting for phylogenetic uncertainty Infection, Genetics and Evolution 8:239-246CrossRef Parker J, Rambaut A, Pybus OG (2008) Correlating viral phenotypes with phylogeny: Accounting for phylogenetic uncertainty Infection, Genetics and Evolution 8:239-246CrossRef
Zurück zum Zitat R Development Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. R Development Core Team (2016) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Zurück zum Zitat Ramakers JJ, Dechmann DK, Page RA, O’Mara MT (2016) Frugivorous bats prefer information from novel social partners Animal Behaviour 116:83-87CrossRef Ramakers JJ, Dechmann DK, Page RA, O’Mara MT (2016) Frugivorous bats prefer information from novel social partners Animal Behaviour 116:83-87CrossRef
Zurück zum Zitat Rasche A, Souza BFdCD, Drexler JF (2016) Bat hepadnaviruses and the origins of primate hepatitis B viruses Current Opinion in Virology 16:86-94CrossRefPubMed Rasche A, Souza BFdCD, Drexler JF (2016) Bat hepadnaviruses and the origins of primate hepatitis B viruses Current Opinion in Virology 16:86-94CrossRefPubMed
Zurück zum Zitat Rodríguez-Herrera B, Medellín R, Timm R (eds) (2007) Murciélagos neotropicales que acampan en hojas. Neotropical tent-roosting bats. Ecosistemas de Costa Rica. INBio. Rodríguez-Herrera B, Medellín R, Timm R (eds) (2007) Murciélagos neotropicales que acampan en hojas. Neotropical tent-roosting bats. Ecosistemas de Costa Rica. INBio.
Zurück zum Zitat 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 142:519-520CrossRefPubMed 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 142:519-520CrossRefPubMed
Zurück zum Zitat 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 45:511-519CrossRef 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 45:511-519CrossRef
Zurück zum Zitat Sagot M, Stevens RD (2012) The Evolution of Group Stability and Roost Lifespan: Perspectives from Tent-Roosting Bats Biotropica 44:90-97CrossRef Sagot M, Stevens RD (2012) The Evolution of Group Stability and Roost Lifespan: Perspectives from Tent-Roosting Bats Biotropica 44:90-97CrossRef
Zurück zum Zitat 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 4:2212CrossRefPubMedPubMedCentral 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 4:2212CrossRefPubMedPubMedCentral
Zurück zum Zitat 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 94:622-625CrossRefPubMed 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 94:622-625CrossRefPubMed
Zurück zum Zitat 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 13:439PubMed 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 13:439PubMed
Zurück zum Zitat 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 279:3384 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 279:3384
Zurück zum Zitat 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 89:684-690CrossRef 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 89:684-690CrossRef
Zurück zum Zitat 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 65:13-21CrossRef 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 65:13-21CrossRef
Zurück zum Zitat 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 206:251-260 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 206:251-260
Zurück zum Zitat 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 145:1919-1931CrossRefPubMed 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 145:1919-1931CrossRefPubMed
Zurück zum Zitat 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. 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.
Zurück zum Zitat 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 92:681-691CrossRefPubMed 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 92:681-691CrossRefPubMed
Zurück zum Zitat World Health Organization (2017) Global Hepatitis Report 2017. Geneva World Health Organization (2017) Global Hepatitis Report 2017. Geneva
Zurück zum Zitat Zuur AF (2010) AED: Data files used in Mixed effects models and extensions in ecology with R Zuur AF (2010) AED: Data files used in Mixed effects models and extensions in ecology with R
Zurück zum Zitat Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems Methods in Ecology and Evolution 1:3-14CrossRef Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems Methods in Ecology and Evolution 1:3-14CrossRef
Metadaten
Titel
Host Biology and Anthropogenic Factors Affect Hepadnavirus Infection in a Neotropical Bat
verfasst von
Thomas Hiller
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
Publikationsdatum
18.12.2018
Verlag
Springer US
Erschienen in
EcoHealth / Ausgabe 1/2019
Print ISSN: 1612-9202
Elektronische ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-018-1387-5

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