About the AuthorLisa A. Beltz is an Associate Professor of Natural Sciences at Malone University in Canton, Ohio, USA.

• Foreword xvA Brief Introduction to Unique Features of Bats in Relation to Infectious Diseases xvAbout the companion website xixI Introduction 11 BAT IMMUNOLOGY 31.1 Introduction to the Immune System of Bats 31.1.1 White blood cell count and other serological parameters 31.1.2 Innate versus adaptive immunity 41.1.3 MicroRNA 51.2 Viral Pattern‐Recognition Receptors and the Bat Immune Response to Microbes 51.3 Introduction to the Interferons 71.3.1 Regulation of interferon production 71.3.2 The JAK‐STAT pathway and interferon‐stimulated genes 81.3.3 Type I interferons 101.3.4 Type II interferon 121.3.5 Type III interferons 121.3.6 Viral avoidance of the host IFN response 141.4 Antibodies and B Lymphocytes 151.5 Macrophages, Dendritic Cells, and Proinflammatory Cytokines 161.6 T Lymphocytes 171.7 Other Parameters of the Immune Response 181.8 Conclusions 19References 21II Viral Infections of Bats 252 RABIES VIRUS AND OTHER BAT RHABDOVIRUSES 272.1 Introduction to the Family Rhabdoviridae 272.2 Lyssaviruses 272.2.1 Rabies virus 322.2.2 Other lyssaviruses of bats 362.2.3 Lyssavirus transmission 402.2.4 Lyssavirus sites of infection 412.2.5 Lyssavirus entry into cells 422.2.6 Prevention of lyssavirus infection 432.2.7 Immune response to lyssaviruses 442.2.8 Lyssavirus surveillance 452.3 Other Rhabdoviruses 452.3.1 The Kern Canyon serogroup of genus Vesiculovirus 462.3.2 Kumasi rhabdovirus 472.3.3 Unclassified rhabdoviruses 472.4 Conclusions 48References 493 HENIPAVIRUSES AND OTHER PARAMYXOVIRUSES OF BATS 533.1 Introduction to Paramyxoviridae 533.2 Diseases Associated with Paramyxoviridae 593.2.1 Henipaviruses and disease 593.2.2 Morbilliviruses and disease 593.2.3 Rubulaviruses and disease 603.3 Henipaviruses in Bats 603.3.1 Henipaviruses in bats from Oceania and Southeast Asia 603.3.2 Henipaviruses and bats from Africa 613.3.3 Henipaviruses in bats from Madagascar 623.3.4 Henipavirus proteins and infection of bats 623.4 Hendra Virus 643.4.1 Hendra virus in Australian bats, horses, and humans 643.4.2 Factors affecting levels of Hendra viruses in bats and the potential for zoonotic transmission 653.5 Nipah Virus 663.5.1 Nipah virus in humans and pigs 663.5.2 Nipah virus in bats from Malaysia and Indonesia 673.5.3 Nipah virus in bats from India and Bangladesh 683.5.4 Interspecies Nipah virus transmission via date palm sap and bat urine 683.6 Cedar Virus 703.7 Protective Bat Responses to Henipavirus Infection 703.7.1 The interferon/STAT pathway and henipaviruses 703.7.2 Antibodies and henipaviruses 723.7.3 Apoptosis 723.8 Methods of Preventing Henipavirus Infection 733.9 Rubulaviruses 743.9.1 Bat parainfluenza virus 743.9.2 Menangle virus in bats and domestic animals 743.9.3 Tioman virus in bats and humans 753.9.4 Tuhoko viruses in bats 753.9.5 Achimota viruses in bats 753.9.6 Sosuga virus in bats and humans 763.9.7 Jeilongvirus in bats 763.9.8 Mumps‐like bat virus 763.9.9 Mapuera virus in bats 763.10 Morbilliviruses in Bats 773.11 Belinga bat Virus 773.12 Large, Multiviral Studies of Paramyxoviruses in Bats 783.12.1 Multiviral paramyxoviruses studies in Asia 783.12.2 Multiviral paramyxoviruses studies in Africa 783.12.3 Multiviral paramyxoviruses studies in Madagascar and islands of the Southwest Indian Ocean 793.12.4 Multiviral paramyxoviruses studies in Oceania 793.13 Conclusions 80References 824 FILOVIRUSES AND BATS 894.1 Filoviruses 894.1.1 History of filovirus infection 904.1.2 Filovirus disease 914.1.3 The roles of viral proteins 914.2 Marburg Virus 964.2.1 Marburg virus in humans and bats 964.2.2 Experimental infection of bats with Marburg virus 984.3 Ebola Virus 994.3.1 Ebola virus in humans and bats 994.3.2 Ebola virus and bats prior to the 2014 outbreak 994.3.3 EBOV incidence in bats during and after the 2014 outbreak 1004.4 Lloviu and Related Filoviruses in Bats 1014.5 Seasonality of Filovirus Infection in Bats 1014.6 Factors Affecting Zoonotic Infection by Filoviruses 1024.7 Filoviruses in Animals Other Than Bats 1034.8 Conclusions 104References 1065 BATS AND CORONAVIRUSES 1115.1 Introduction 1115.2 SARS Coronavirus 1145.2.1 The history of SARS 1145.2.2 SARS pathology 1155.2.3 Viral and cellular proteins and their role in entry into the host cells 1165.2.4 SARS in civits and raccoon dogs 1185.2.5 Relatedness of bat SARS‐like CoV to SARS‐CoV 1195.3 MERS Coronavirus 1225.3.1 MERS pathology 1225.3.2 Viral and cellular proteins and their role in entry into the host cells 1235.3.3 MERS‐CoV and spillover from domestic livestock 1245.3.4 Relatedness of bat‐CoV to MERS‐CoV 1265.3.5 Transmission of MERS‐CoV 1305.4 Other Coronaviruses of Bats 1315.5 Conclusions 133References 1346 OTHER RNA VIRUSES AND BATS 1396.1 Introduction 1396.2 Baltimore Class III Viruses and Bats 1396.2.1 Orbiviruses 1406.2.2 Rotaviruses 1406.2.3 Pteropine orthomyxovirus group 1406.2.4 Mammalian orthoreoviruses 1546.3 Baltimore Class IV Viruses 1566.3.1 Astroviruses 1566.3.2 Flaviviruses 1586.3.3 Hepeviruses 1646.3.4 Picornaviruses 1646.4 Baltimore Class V Viruses 1656.4.1 Bunyaviridae 1656.4.2 Orthomyxoviruses 1686.4.3 Arenaviridae 1706.5 Large, Multi‐Virus Studies 1716.6 Conclusions 171References 1747 BALTIMORE CLASS I AND CLASS II DNA VIRUSES OF BATS 1817.1 Introduction to Double‐ and Single‐ Stranded DNA Viruses 1817.2 Baltimore Class I Viruses 1817.2.1 Poxviruses 1907.2.2 Adenoviruses 1917.2.3 Herpesviruses 1927.2.4 Papillomaviruses 1947.2.5 Polyomaviruses 1947.3 Baltimore Class II Viruses 1967.3.1 Parvoviruses 1967.3.2 Dependoviruses 1977.3.3 Circular replication‐associated protein encoding single‐stranded DNA viruses 1977.4 Conclusions 199References 2018 REVERSE‐TRANSCRIBING BAT VIRUSES AND LARGE‐SCALE BAT VIROME STUDIES 2058.1 Baltimore Class VI Retroviruses 2058.1.1 Exogenous and endogenous retroviruses and their life‐cycles 2058.1.2 Viral polyproteins 2088.1.3 Retroviral genera 2098.1.4 Endogenous gammaretroviruses of bats and other mammals 2098.1.5 Betaretroviruses of bats and other mammals 2108.2 Evidence of Ancient Endogenous Virus Genomic Elements in Bat Chromosomes 2118.2.1 Endogenous bornavirus genomic elements in bat chromosomes 2128.2.2 Endogenous Ebola and Marburg virus genomic elements in bat chromosomes 2128.3 Hepadnaviruses – Baltimore Class VII Reverse‐Transcribing DNA Viruses 2138.3.1 Human hepatitis B virus 2138.3.2 Orthohepadnaviruses and bats 2148.4 Large‐Scale Bat Virome Studies 2158.4.1 Bat virome studies in North America 2158.4.2 Bat virome studies in Europe 2158.4.3 Bat virome studies in Asia and Southeast Asia 2168.4.4 Bat virome studies in Oceania 2178.5 Conclusions 217References 218III Bacterial Infections of Bats 2219 ARTHROPOD‐BORNE BACTERIAL INFECTIONS OF BATS 2239.1 Introduction 2239.2 Bartonella 2269.2.1 Bartonella in bats from Asia 2269.2.2 Bartonella in bats from Africa 2269.2.3 Bartonella in bats from Europe 2289.2.4 Bartonella in bats from the Americas 2289.3 Borrelia 2299.4 Rickettsia 2309.4.1 Rickettsia and human disease 2309.4.2 Rickesttsia and bats 2319.5 Bat Ectoparasites As Bacterial Vectors 2319.5.1 Bacteria from bat flies 2319.5.2 Bacteria from bat ticks 2329.6 Conclusions 234References 23510 OTHER BACTERIA AND BATS 23910.1 Introduction 23910.2 Leptospira 24510.2.1 Leptospira in South America 24510.2.2 Leptospira in Africa 24610.2.3 Leptospira in islands of the Indian Ocean 24610.2.4 Leptospira in Australia 24710.3 Yersinia 24810.4 Pasteurella 24910.5 Mycoplasma 25010.6 Waddlia 25010.7 Rickettsia and Similar Bacteria 25110.8 Bat Gastrointestinal Tract Bacteria 25110.8.1 Gastrointestinal bacteria in bats of Southeast Asia and Oceania 25110.8.2 Gastrointestinal bacteria in bats of Madagascar 25210.8.3 Gastrointestinal bacteria in bats of the Americas 25310.9 Large‐Scale Studies of Other Bat Bacteria 25410.10 Bacterial Species Beneficial to Bats 25510.11 Conclusions 256References 257IV Protist Infections of Bats 26111 APICOMPLEXANS AND BATS 26311.1 Introduction to Apicomplexa and Coccidea 26311.2 Order Haemosporida 26911.2.1 Invertebrate hosts of Haemosporida 26911.2.2 Bat hosts of Haemosporida 27011.3 Order Piroplasmida 27211.3.1 Babesia species and bats 27211.3.2 Other Piroplasmida in bats 27211.4 Order Eimeriida 27311.4.1 Toxoplasma gondii and bats 27311.4.2 Eimeria species and bats 27611.5 Order Adeleida, Crytoporidium Species, and Bats 27711.6 Conclusions 278References 28012 KINETOPLASTIDS AND BATS 28512.1 Kinetoplastids 28512.2 Trypanosomes 28912.2.1 Life cycles of trypanosomes 28912.2.2 Trypanosomes and disease 29012.2.3 Trypanosomes infecting bats throughout the world 29012.2.4 Trypanosoma cruzi 29312.3 Leishmania 29512.3.1 Leishmania and disease 29512.3.2 Leishmania and bats 29612.4 Conclusions 297References 298V Fungal Infections of Bats 30313 WHITE‐NOSE SYNDROME AND BATS 30513.1 Introduction to Pseudogymnoascus destructans 30513.2 White‐Nose Syndrome 30613.2.1 Arousal, loss of fat reserves, and dehydration 30813.2.2 The role of torpor in WNS disease dynamics 30913.2.3 WNS and wing damage 31013.3 The Geographical Distribution of White‐Nose Syndrome 31113.3.1 WNS in North America 31113.3.2 WNS in Europe 31213.3.3 WNS in Eastern Asia 31313.4 The Effects of White‐Nose Syndrome on Selected North American Bat Populations 31313.4.1 WNS and Myotis lucifugus 31313.4.2 WNS and Myotis sodalis 31413.5 The Bat Immune Response to White‐Nose Syndrome 31513.5.1 Leukocyte counts 31513.5.2 Antifungal activity in the plasma 31513.5.3 T helper cell activity in infected bats 31513.5.4 Inflammatory activity in infected bats 31513.5.5 Differences in the immune response to WNS in European and North American bats 31613.5.6 Immune‐mediated pathology in WNS 31713.6 Antifungal Agents 31713.6.1 Antifungal compounds 31713.6.2 Antifungal agents derived from bacteria 31813.6.3 Antifungal agents derived from fungi 31813.7 The Mycobiome of White‐Nose Syndrome‐Infected Hibernacula 31913.8 Recovery and Recolonization 320References 32114 HISTOPLASMA CAPSULATUM AND OTHER FUNGI AND BATS 32714.1 Fungal Species and Bats 32714.1.1 Histoplasma capsulatum 32714.1.2 Blastomyces dermatitidis 33614.1.3 Pneumocystis 33714.1.4 Coccidioides 33714.1.5 Encephalitozoon 33714.1.6 Other fungi of bats 33814.2 Broad Surveys of Fungi in Bats 33814.2.1 Asia 33814.2.2 Europe 33814.2.3 The Americas 33914.2.4 Fungi inhabiting bat external surfaces 34014.3 Experimental Infection of Bats with Fungi 34114.4 Immune Response to Fungi 34114.5 Yeast in Bats 34214.5.1 Candida 34214.5.2 Malassezia 34214.5.3 Yeasts in Japan 34214.6 Conclusions 343VI Zoonotic Disease Transmission and Bats 34915 ZOONOTIC TRANSMISSION OF DISEASE BY BATS AND OTHER ANIMALS 35115.1 Introduction 35115.2 Zoonotic Transmission of Infection by Bats 35315.2.1 Direct or indirect zoonotic transmission by bats to humans 35415.2.2 Transmission and persistence of viruses within and among bat species over large geographical ranges 35415.2.3 Seasonal changes contributing to zoonotic transmission from bats 35515.3 Zoonotic Transmission of Infection by other Animal Species 35615.3.1 Zoonotic transmission by rodents 35715.3.2 Zoonotic transmission by companion animals 35915.3.3 Zoonotic transmission by selected agricultural animals 36015.4 Factors that Increase the Risk of Zoonotic Infection by Bats 36215.4.1 Increasing urbanization of bats 36215.4.2 Human activities that increase contact with bats, including the bushmeat trade 36215.5 Strategies to Prevent Zoonotic Transmission from Bats to Humans or other Animals 36315.6 Conclusions 364References 366Index 371

About the AuthorLisa A. Beltz is an Associate Professor of Natural Sciences at Malone University in Canton, Ohio, USA.

• Foreword xvA Brief Introduction to Unique Features of Bats in Relation to Infectious Diseases xvAbout the companion website xixI Introduction 11 BAT IMMUNOLOGY 31.1 Introduction to the Immune System of Bats 31.1.1 White blood cell count and other serological parameters 31.1.2 Innate versus adaptive immunity 41.1.3 MicroRNA 51.2 Viral Pattern‐Recognition Receptors and the Bat Immune Response to Microbes 51.3 Introduction to the Interferons 71.3.1 Regulation of interferon production 71.3.2 The JAK‐STAT pathway and interferon‐stimulated genes 81.3.3 Type I interferons 101.3.4 Type II interferon 121.3.5 Type III interferons 121.3.6 Viral avoidance of the host IFN response 141.4 Antibodies and B Lymphocytes 151.5 Macrophages, Dendritic Cells, and Proinflammatory Cytokines 161.6 T Lymphocytes 171.7 Other Parameters of the Immune Response 181.8 Conclusions 19References 21II Viral Infections of Bats 252 RABIES VIRUS AND OTHER BAT RHABDOVIRUSES 272.1 Introduction to the Family Rhabdoviridae 272.2 Lyssaviruses 272.2.1 Rabies virus 322.2.2 Other lyssaviruses of bats 362.2.3 Lyssavirus transmission 402.2.4 Lyssavirus sites of infection 412.2.5 Lyssavirus entry into cells 422.2.6 Prevention of lyssavirus infection 432.2.7 Immune response to lyssaviruses 442.2.8 Lyssavirus surveillance 452.3 Other Rhabdoviruses 452.3.1 The Kern Canyon serogroup of genus Vesiculovirus 462.3.2 Kumasi rhabdovirus 472.3.3 Unclassified rhabdoviruses 472.4 Conclusions 48References 493 HENIPAVIRUSES AND OTHER PARAMYXOVIRUSES OF BATS 533.1 Introduction to Paramyxoviridae 533.2 Diseases Associated with Paramyxoviridae 593.2.1 Henipaviruses and disease 593.2.2 Morbilliviruses and disease 593.2.3 Rubulaviruses and disease 603.3 Henipaviruses in Bats 603.3.1 Henipaviruses in bats from Oceania and Southeast Asia 603.3.2 Henipaviruses and bats from Africa 613.3.3 Henipaviruses in bats from Madagascar 623.3.4 Henipavirus proteins and infection of bats 623.4 Hendra Virus 643.4.1 Hendra virus in Australian bats, horses, and humans 643.4.2 Factors affecting levels of Hendra viruses in bats and the potential for zoonotic transmission 653.5 Nipah Virus 663.5.1 Nipah virus in humans and pigs 663.5.2 Nipah virus in bats from Malaysia and Indonesia 673.5.3 Nipah virus in bats from India and Bangladesh 683.5.4 Interspecies Nipah virus transmission via date palm sap and bat urine 683.6 Cedar Virus 703.7 Protective Bat Responses to Henipavirus Infection 703.7.1 The interferon/STAT pathway and henipaviruses 703.7.2 Antibodies and henipaviruses 723.7.3 Apoptosis 723.8 Methods of Preventing Henipavirus Infection 733.9 Rubulaviruses 743.9.1 Bat parainfluenza virus 743.9.2 Menangle virus in bats and domestic animals 743.9.3 Tioman virus in bats and humans 753.9.4 Tuhoko viruses in bats 753.9.5 Achimota viruses in bats 753.9.6 Sosuga virus in bats and humans 763.9.7 Jeilongvirus in bats 763.9.8 Mumps‐like bat virus 763.9.9 Mapuera virus in bats 763.10 Morbilliviruses in Bats 773.11 Belinga bat Virus 773.12 Large, Multiviral Studies of Paramyxoviruses in Bats 783.12.1 Multiviral paramyxoviruses studies in Asia 783.12.2 Multiviral paramyxoviruses studies in Africa 783.12.3 Multiviral paramyxoviruses studies in Madagascar and islands of the Southwest Indian Ocean 793.12.4 Multiviral paramyxoviruses studies in Oceania 793.13 Conclusions 80References 824 FILOVIRUSES AND BATS 894.1 Filoviruses 894.1.1 History of filovirus infection 904.1.2 Filovirus disease 914.1.3 The roles of viral proteins 914.2 Marburg Virus 964.2.1 Marburg virus in humans and bats 964.2.2 Experimental infection of bats with Marburg virus 984.3 Ebola Virus 994.3.1 Ebola virus in humans and bats 994.3.2 Ebola virus and bats prior to the 2014 outbreak 994.3.3 EBOV incidence in bats during and after the 2014 outbreak 1004.4 Lloviu and Related Filoviruses in Bats 1014.5 Seasonality of Filovirus Infection in Bats 1014.6 Factors Affecting Zoonotic Infection by Filoviruses 1024.7 Filoviruses in Animals Other Than Bats 1034.8 Conclusions 104References 1065 BATS AND CORONAVIRUSES 1115.1 Introduction 1115.2 SARS Coronavirus 1145.2.1 The history of SARS 1145.2.2 SARS pathology 1155.2.3 Viral and cellular proteins and their role in entry into the host cells 1165.2.4 SARS in civits and raccoon dogs 1185.2.5 Relatedness of bat SARS‐like CoV to SARS‐CoV 1195.3 MERS Coronavirus 1225.3.1 MERS pathology 1225.3.2 Viral and cellular proteins and their role in entry into the host cells 1235.3.3 MERS‐CoV and spillover from domestic livestock 1245.3.4 Relatedness of bat‐CoV to MERS‐CoV 1265.3.5 Transmission of MERS‐CoV 1305.4 Other Coronaviruses of Bats 1315.5 Conclusions 133References 1346 OTHER RNA VIRUSES AND BATS 1396.1 Introduction 1396.2 Baltimore Class III Viruses and Bats 1396.2.1 Orbiviruses 1406.2.2 Rotaviruses 1406.2.3 Pteropine orthomyxovirus group 1406.2.4 Mammalian orthoreoviruses 1546.3 Baltimore Class IV Viruses 1566.3.1 Astroviruses 1566.3.2 Flaviviruses 1586.3.3 Hepeviruses 1646.3.4 Picornaviruses 1646.4 Baltimore Class V Viruses 1656.4.1 Bunyaviridae 1656.4.2 Orthomyxoviruses 1686.4.3 Arenaviridae 1706.5 Large, Multi‐Virus Studies 1716.6 Conclusions 171References 1747 BALTIMORE CLASS I AND CLASS II DNA VIRUSES OF BATS 1817.1 Introduction to Double‐ and Single‐ Stranded DNA Viruses 1817.2 Baltimore Class I Viruses 1817.2.1 Poxviruses 1907.2.2 Adenoviruses 1917.2.3 Herpesviruses 1927.2.4 Papillomaviruses 1947.2.5 Polyomaviruses 1947.3 Baltimore Class II Viruses 1967.3.1 Parvoviruses 1967.3.2 Dependoviruses 1977.3.3 Circular replication‐associated protein encoding single‐stranded DNA viruses 1977.4 Conclusions 199References 2018 REVERSE‐TRANSCRIBING BAT VIRUSES AND LARGE‐SCALE BAT VIROME STUDIES 2058.1 Baltimore Class VI Retroviruses 2058.1.1 Exogenous and endogenous retroviruses and their life‐cycles 2058.1.2 Viral polyproteins 2088.1.3 Retroviral genera 2098.1.4 Endogenous gammaretroviruses of bats and other mammals 2098.1.5 Betaretroviruses of bats and other mammals 2108.2 Evidence of Ancient Endogenous Virus Genomic Elements in Bat Chromosomes 2118.2.1 Endogenous bornavirus genomic elements in bat chromosomes 2128.2.2 Endogenous Ebola and Marburg virus genomic elements in bat chromosomes 2128.3 Hepadnaviruses – Baltimore Class VII Reverse‐Transcribing DNA Viruses 2138.3.1 Human hepatitis B virus 2138.3.2 Orthohepadnaviruses and bats 2148.4 Large‐Scale Bat Virome Studies 2158.4.1 Bat virome studies in North America 2158.4.2 Bat virome studies in Europe 2158.4.3 Bat virome studies in Asia and Southeast Asia 2168.4.4 Bat virome studies in Oceania 2178.5 Conclusions 217References 218III Bacterial Infections of Bats 2219 ARTHROPOD‐BORNE BACTERIAL INFECTIONS OF BATS 2239.1 Introduction 2239.2 Bartonella 2269.2.1 Bartonella in bats from Asia 2269.2.2 Bartonella in bats from Africa 2269.2.3 Bartonella in bats from Europe 2289.2.4 Bartonella in bats from the Americas 2289.3 Borrelia 2299.4 Rickettsia 2309.4.1 Rickettsia and human disease 2309.4.2 Rickesttsia and bats 2319.5 Bat Ectoparasites As Bacterial Vectors 2319.5.1 Bacteria from bat flies 2319.5.2 Bacteria from bat ticks 2329.6 Conclusions 234References 23510 OTHER BACTERIA AND BATS 23910.1 Introduction 23910.2 Leptospira 24510.2.1 Leptospira in South America 24510.2.2 Leptospira in Africa 24610.2.3 Leptospira in islands of the Indian Ocean 24610.2.4 Leptospira in Australia 24710.3 Yersinia 24810.4 Pasteurella 24910.5 Mycoplasma 25010.6 Waddlia 25010.7 Rickettsia and Similar Bacteria 25110.8 Bat Gastrointestinal Tract Bacteria 25110.8.1 Gastrointestinal bacteria in bats of Southeast Asia and Oceania 25110.8.2 Gastrointestinal bacteria in bats of Madagascar 25210.8.3 Gastrointestinal bacteria in bats of the Americas 25310.9 Large‐Scale Studies of Other Bat Bacteria 25410.10 Bacterial Species Beneficial to Bats 25510.11 Conclusions 256References 257IV Protist Infections of Bats 26111 APICOMPLEXANS AND BATS 26311.1 Introduction to Apicomplexa and Coccidea 26311.2 Order Haemosporida 26911.2.1 Invertebrate hosts of Haemosporida 26911.2.2 Bat hosts of Haemosporida 27011.3 Order Piroplasmida 27211.3.1 Babesia species and bats 27211.3.2 Other Piroplasmida in bats 27211.4 Order Eimeriida 27311.4.1 Toxoplasma gondii and bats 27311.4.2 Eimeria species and bats 27611.5 Order Adeleida, Crytoporidium Species, and Bats 27711.6 Conclusions 278References 28012 KINETOPLASTIDS AND BATS 28512.1 Kinetoplastids 28512.2 Trypanosomes 28912.2.1 Life cycles of trypanosomes 28912.2.2 Trypanosomes and disease 29012.2.3 Trypanosomes infecting bats throughout the world 29012.2.4 Trypanosoma cruzi 29312.3 Leishmania 29512.3.1 Leishmania and disease 29512.3.2 Leishmania and bats 29612.4 Conclusions 297References 298V Fungal Infections of Bats 30313 WHITE‐NOSE SYNDROME AND BATS 30513.1 Introduction to Pseudogymnoascus destructans 30513.2 White‐Nose Syndrome 30613.2.1 Arousal, loss of fat reserves, and dehydration 30813.2.2 The role of torpor in WNS disease dynamics 30913.2.3 WNS and wing damage 31013.3 The Geographical Distribution of White‐Nose Syndrome 31113.3.1 WNS in North America 31113.3.2 WNS in Europe 31213.3.3 WNS in Eastern Asia 31313.4 The Effects of White‐Nose Syndrome on Selected North American Bat Populations 31313.4.1 WNS and Myotis lucifugus 31313.4.2 WNS and Myotis sodalis 31413.5 The Bat Immune Response to White‐Nose Syndrome 31513.5.1 Leukocyte counts 31513.5.2 Antifungal activity in the plasma 31513.5.3 T helper cell activity in infected bats 31513.5.4 Inflammatory activity in infected bats 31513.5.5 Differences in the immune response to WNS in European and North American bats 31613.5.6 Immune‐mediated pathology in WNS 31713.6 Antifungal Agents 31713.6.1 Antifungal compounds 31713.6.2 Antifungal agents derived from bacteria 31813.6.3 Antifungal agents derived from fungi 31813.7 The Mycobiome of White‐Nose Syndrome‐Infected Hibernacula 31913.8 Recovery and Recolonization 320References 32114 HISTOPLASMA CAPSULATUM AND OTHER FUNGI AND BATS 32714.1 Fungal Species and Bats 32714.1.1 Histoplasma capsulatum 32714.1.2 Blastomyces dermatitidis 33614.1.3 Pneumocystis 33714.1.4 Coccidioides 33714.1.5 Encephalitozoon 33714.1.6 Other fungi of bats 33814.2 Broad Surveys of Fungi in Bats 33814.2.1 Asia 33814.2.2 Europe 33814.2.3 The Americas 33914.2.4 Fungi inhabiting bat external surfaces 34014.3 Experimental Infection of Bats with Fungi 34114.4 Immune Response to Fungi 34114.5 Yeast in Bats 34214.5.1 Candida 34214.5.2 Malassezia 34214.5.3 Yeasts in Japan 34214.6 Conclusions 343VI Zoonotic Disease Transmission and Bats 34915 ZOONOTIC TRANSMISSION OF DISEASE BY BATS AND OTHER ANIMALS 35115.1 Introduction 35115.2 Zoonotic Transmission of Infection by Bats 35315.2.1 Direct or indirect zoonotic transmission by bats to humans 35415.2.2 Transmission and persistence of viruses within and among bat species over large geographical ranges 35415.2.3 Seasonal changes contributing to zoonotic transmission from bats 35515.3 Zoonotic Transmission of Infection by other Animal Species 35615.3.1 Zoonotic transmission by rodents 35715.3.2 Zoonotic transmission by companion animals 35915.3.3 Zoonotic transmission by selected agricultural animals 36015.4 Factors that Increase the Risk of Zoonotic Infection by Bats 36215.4.1 Increasing urbanization of bats 36215.4.2 Human activities that increase contact with bats, including the bushmeat trade 36215.5 Strategies to Prevent Zoonotic Transmission from Bats to Humans or other Animals 36315.6 Conclusions 364References 366Index 371

About the AuthorLisa A. Beltz is an Associate Professor of Natural Sciences at Malone University in Canton, Ohio, USA.

• Foreword xvA Brief Introduction to Unique Features of Bats in Relation to Infectious Diseases xvAbout the companion website xixI Introduction 11 BAT IMMUNOLOGY 31.1 Introduction to the Immune System of Bats 31.1.1 White blood cell count and other serological parameters 31.1.2 Innate versus adaptive immunity 41.1.3 MicroRNA 51.2 Viral Pattern‐Recognition Receptors and the Bat Immune Response to Microbes 51.3 Introduction to the Interferons 71.3.1 Regulation of interferon production 71.3.2 The JAK‐STAT pathway and interferon‐stimulated genes 81.3.3 Type I interferons 101.3.4 Type II interferon 121.3.5 Type III interferons 121.3.6 Viral avoidance of the host IFN response 141.4 Antibodies and B Lymphocytes 151.5 Macrophages, Dendritic Cells, and Proinflammatory Cytokines 161.6 T Lymphocytes 171.7 Other Parameters of the Immune Response 181.8 Conclusions 19References 21II Viral Infections of Bats 252 RABIES VIRUS AND OTHER BAT RHABDOVIRUSES 272.1 Introduction to the Family Rhabdoviridae 272.2 Lyssaviruses 272.2.1 Rabies virus 322.2.2 Other lyssaviruses of bats 362.2.3 Lyssavirus transmission 402.2.4 Lyssavirus sites of infection 412.2.5 Lyssavirus entry into cells 422.2.6 Prevention of lyssavirus infection 432.2.7 Immune response to lyssaviruses 442.2.8 Lyssavirus surveillance 452.3 Other Rhabdoviruses 452.3.1 The Kern Canyon serogroup of genus Vesiculovirus 462.3.2 Kumasi rhabdovirus 472.3.3 Unclassified rhabdoviruses 472.4 Conclusions 48References 493 HENIPAVIRUSES AND OTHER PARAMYXOVIRUSES OF BATS 533.1 Introduction to Paramyxoviridae 533.2 Diseases Associated with Paramyxoviridae 593.2.1 Henipaviruses and disease 593.2.2 Morbilliviruses and disease 593.2.3 Rubulaviruses and disease 603.3 Henipaviruses in Bats 603.3.1 Henipaviruses in bats from Oceania and Southeast Asia 603.3.2 Henipaviruses and bats from Africa 613.3.3 Henipaviruses in bats from Madagascar 623.3.4 Henipavirus proteins and infection of bats 623.4 Hendra Virus 643.4.1 Hendra virus in Australian bats, horses, and humans 643.4.2 Factors affecting levels of Hendra viruses in bats and the potential for zoonotic transmission 653.5 Nipah Virus 663.5.1 Nipah virus in humans and pigs 663.5.2 Nipah virus in bats from Malaysia and Indonesia 673.5.3 Nipah virus in bats from India and Bangladesh 683.5.4 Interspecies Nipah virus transmission via date palm sap and bat urine 683.6 Cedar Virus 703.7 Protective Bat Responses to Henipavirus Infection 703.7.1 The interferon/STAT pathway and henipaviruses 703.7.2 Antibodies and henipaviruses 723.7.3 Apoptosis 723.8 Methods of Preventing Henipavirus Infection 733.9 Rubulaviruses 743.9.1 Bat parainfluenza virus 743.9.2 Menangle virus in bats and domestic animals 743.9.3 Tioman virus in bats and humans 753.9.4 Tuhoko viruses in bats 753.9.5 Achimota viruses in bats 753.9.6 Sosuga virus in bats and humans 763.9.7 Jeilongvirus in bats 763.9.8 Mumps‐like bat virus 763.9.9 Mapuera virus in bats 763.10 Morbilliviruses in Bats 773.11 Belinga bat Virus 773.12 Large, Multiviral Studies of Paramyxoviruses in Bats 783.12.1 Multiviral paramyxoviruses studies in Asia 783.12.2 Multiviral paramyxoviruses studies in Africa 783.12.3 Multiviral paramyxoviruses studies in Madagascar and islands of the Southwest Indian Ocean 793.12.4 Multiviral paramyxoviruses studies in Oceania 793.13 Conclusions 80References 824 FILOVIRUSES AND BATS 894.1 Filoviruses 894.1.1 History of filovirus infection 904.1.2 Filovirus disease 914.1.3 The roles of viral proteins 914.2 Marburg Virus 964.2.1 Marburg virus in humans and bats 964.2.2 Experimental infection of bats with Marburg virus 984.3 Ebola Virus 994.3.1 Ebola virus in humans and bats 994.3.2 Ebola virus and bats prior to the 2014 outbreak 994.3.3 EBOV incidence in bats during and after the 2014 outbreak 1004.4 Lloviu and Related Filoviruses in Bats 1014.5 Seasonality of Filovirus Infection in Bats 1014.6 Factors Affecting Zoonotic Infection by Filoviruses 1024.7 Filoviruses in Animals Other Than Bats 1034.8 Conclusions 104References 1065 BATS AND CORONAVIRUSES 1115.1 Introduction 1115.2 SARS Coronavirus 1145.2.1 The history of SARS 1145.2.2 SARS pathology 1155.2.3 Viral and cellular proteins and their role in entry into the host cells 1165.2.4 SARS in civits and raccoon dogs 1185.2.5 Relatedness of bat SARS‐like CoV to SARS‐CoV 1195.3 MERS Coronavirus 1225.3.1 MERS pathology 1225.3.2 Viral and cellular proteins and their role in entry into the host cells 1235.3.3 MERS‐CoV and spillover from domestic livestock 1245.3.4 Relatedness of bat‐CoV to MERS‐CoV 1265.3.5 Transmission of MERS‐CoV 1305.4 Other Coronaviruses of Bats 1315.5 Conclusions 133References 1346 OTHER RNA VIRUSES AND BATS 1396.1 Introduction 1396.2 Baltimore Class III Viruses and Bats 1396.2.1 Orbiviruses 1406.2.2 Rotaviruses 1406.2.3 Pteropine orthomyxovirus group 1406.2.4 Mammalian orthoreoviruses 1546.3 Baltimore Class IV Viruses 1566.3.1 Astroviruses 1566.3.2 Flaviviruses 1586.3.3 Hepeviruses 1646.3.4 Picornaviruses 1646.4 Baltimore Class V Viruses 1656.4.1 Bunyaviridae 1656.4.2 Orthomyxoviruses 1686.4.3 Arenaviridae 1706.5 Large, Multi‐Virus Studies 1716.6 Conclusions 171References 1747 BALTIMORE CLASS I AND CLASS II DNA VIRUSES OF BATS 1817.1 Introduction to Double‐ and Single‐ Stranded DNA Viruses 1817.2 Baltimore Class I Viruses 1817.2.1 Poxviruses 1907.2.2 Adenoviruses 1917.2.3 Herpesviruses 1927.2.4 Papillomaviruses 1947.2.5 Polyomaviruses 1947.3 Baltimore Class II Viruses 1967.3.1 Parvoviruses 1967.3.2 Dependoviruses 1977.3.3 Circular replication‐associated protein encoding single‐stranded DNA viruses 1977.4 Conclusions 199References 2018 REVERSE‐TRANSCRIBING BAT VIRUSES AND LARGE‐SCALE BAT VIROME STUDIES 2058.1 Baltimore Class VI Retroviruses 2058.1.1 Exogenous and endogenous retroviruses and their life‐cycles 2058.1.2 Viral polyproteins 2088.1.3 Retroviral genera 2098.1.4 Endogenous gammaretroviruses of bats and other mammals 2098.1.5 Betaretroviruses of bats and other mammals 2108.2 Evidence of Ancient Endogenous Virus Genomic Elements in Bat Chromosomes 2118.2.1 Endogenous bornavirus genomic elements in bat chromosomes 2128.2.2 Endogenous Ebola and Marburg virus genomic elements in bat chromosomes 2128.3 Hepadnaviruses – Baltimore Class VII Reverse‐Transcribing DNA Viruses 2138.3.1 Human hepatitis B virus 2138.3.2 Orthohepadnaviruses and bats 2148.4 Large‐Scale Bat Virome Studies 2158.4.1 Bat virome studies in North America 2158.4.2 Bat virome studies in Europe 2158.4.3 Bat virome studies in Asia and Southeast Asia 2168.4.4 Bat virome studies in Oceania 2178.5 Conclusions 217References 218III Bacterial Infections of Bats 2219 ARTHROPOD‐BORNE BACTERIAL INFECTIONS OF BATS 2239.1 Introduction 2239.2 Bartonella 2269.2.1 Bartonella in bats from Asia 2269.2.2 Bartonella in bats from Africa 2269.2.3 Bartonella in bats from Europe 2289.2.4 Bartonella in bats from the Americas 2289.3 Borrelia 2299.4 Rickettsia 2309.4.1 Rickettsia and human disease 2309.4.2 Rickesttsia and bats 2319.5 Bat Ectoparasites As Bacterial Vectors 2319.5.1 Bacteria from bat flies 2319.5.2 Bacteria from bat ticks 2329.6 Conclusions 234References 23510 OTHER BACTERIA AND BATS 23910.1 Introduction 23910.2 Leptospira 24510.2.1 Leptospira in South America 24510.2.2 Leptospira in Africa 24610.2.3 Leptospira in islands of the Indian Ocean 24610.2.4 Leptospira in Australia 24710.3 Yersinia 24810.4 Pasteurella 24910.5 Mycoplasma 25010.6 Waddlia 25010.7 Rickettsia and Similar Bacteria 25110.8 Bat Gastrointestinal Tract Bacteria 25110.8.1 Gastrointestinal bacteria in bats of Southeast Asia and Oceania 25110.8.2 Gastrointestinal bacteria in bats of Madagascar 25210.8.3 Gastrointestinal bacteria in bats of the Americas 25310.9 Large‐Scale Studies of Other Bat Bacteria 25410.10 Bacterial Species Beneficial to Bats 25510.11 Conclusions 256References 257IV Protist Infections of Bats 26111 APICOMPLEXANS AND BATS 26311.1 Introduction to Apicomplexa and Coccidea 26311.2 Order Haemosporida 26911.2.1 Invertebrate hosts of Haemosporida 26911.2.2 Bat hosts of Haemosporida 27011.3 Order Piroplasmida 27211.3.1 Babesia species and bats 27211.3.2 Other Piroplasmida in bats 27211.4 Order Eimeriida 27311.4.1 Toxoplasma gondii and bats 27311.4.2 Eimeria species and bats 27611.5 Order Adeleida, Crytoporidium Species, and Bats 27711.6 Conclusions 278References 28012 KINETOPLASTIDS AND BATS 28512.1 Kinetoplastids 28512.2 Trypanosomes 28912.2.1 Life cycles of trypanosomes 28912.2.2 Trypanosomes and disease 29012.2.3 Trypanosomes infecting bats throughout the world 29012.2.4 Trypanosoma cruzi 29312.3 Leishmania 29512.3.1 Leishmania and disease 29512.3.2 Leishmania and bats 29612.4 Conclusions 297References 298V Fungal Infections of Bats 30313 WHITE‐NOSE SYNDROME AND BATS 30513.1 Introduction to Pseudogymnoascus destructans 30513.2 White‐Nose Syndrome 30613.2.1 Arousal, loss of fat reserves, and dehydration 30813.2.2 The role of torpor in WNS disease dynamics 30913.2.3 WNS and wing damage 31013.3 The Geographical Distribution of White‐Nose Syndrome 31113.3.1 WNS in North America 31113.3.2 WNS in Europe 31213.3.3 WNS in Eastern Asia 31313.4 The Effects of White‐Nose Syndrome on Selected North American Bat Populations 31313.4.1 WNS and Myotis lucifugus 31313.4.2 WNS and Myotis sodalis 31413.5 The Bat Immune Response to White‐Nose Syndrome 31513.5.1 Leukocyte counts 31513.5.2 Antifungal activity in the plasma 31513.5.3 T helper cell activity in infected bats 31513.5.4 Inflammatory activity in infected bats 31513.5.5 Differences in the immune response to WNS in European and North American bats 31613.5.6 Immune‐mediated pathology in WNS 31713.6 Antifungal Agents 31713.6.1 Antifungal compounds 31713.6.2 Antifungal agents derived from bacteria 31813.6.3 Antifungal agents derived from fungi 31813.7 The Mycobiome of White‐Nose Syndrome‐Infected Hibernacula 31913.8 Recovery and Recolonization 320References 32114 HISTOPLASMA CAPSULATUM AND OTHER FUNGI AND BATS 32714.1 Fungal Species and Bats 32714.1.1 Histoplasma capsulatum 32714.1.2 Blastomyces dermatitidis 33614.1.3 Pneumocystis 33714.1.4 Coccidioides 33714.1.5 Encephalitozoon 33714.1.6 Other fungi of bats 33814.2 Broad Surveys of Fungi in Bats 33814.2.1 Asia 33814.2.2 Europe 33814.2.3 The Americas 33914.2.4 Fungi inhabiting bat external surfaces 34014.3 Experimental Infection of Bats with Fungi 34114.4 Immune Response to Fungi 34114.5 Yeast in Bats 34214.5.1 Candida 34214.5.2 Malassezia 34214.5.3 Yeasts in Japan 34214.6 Conclusions 343VI Zoonotic Disease Transmission and Bats 34915 ZOONOTIC TRANSMISSION OF DISEASE BY BATS AND OTHER ANIMALS 35115.1 Introduction 35115.2 Zoonotic Transmission of Infection by Bats 35315.2.1 Direct or indirect zoonotic transmission by bats to humans 35415.2.2 Transmission and persistence of viruses within and among bat species over large geographical ranges 35415.2.3 Seasonal changes contributing to zoonotic transmission from bats 35515.3 Zoonotic Transmission of Infection by other Animal Species 35615.3.1 Zoonotic transmission by rodents 35715.3.2 Zoonotic transmission by companion animals 35915.3.3 Zoonotic transmission by selected agricultural animals 36015.4 Factors that Increase the Risk of Zoonotic Infection by Bats 36215.4.1 Increasing urbanization of bats 36215.4.2 Human activities that increase contact with bats, including the bushmeat trade 36215.5 Strategies to Prevent Zoonotic Transmission from Bats to Humans or other Animals 36315.6 Conclusions 364References 366Index 371