Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 110(1): 1-22, February 2015 1 Bats and zoonotic viruses: can we confidently link bats with emerging deadly viruses? Ricardo Moratelli1/+, Charles H Calisher2 1Fiocruz Mata Atlântica, Rio de Janeiro, RJ, Brasil 2Arthropod-borne and Infectious Diseases Laboratory, Department of Microbiology, Immunology and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO, USA An increasingly asked question is ‘can we confidently link bats with emerging viruses?’. No, or not yet, is the quali- fied answer based on the evidence available. Although more than 200 viruses – some of them deadly zoonotic viruses – have been isolated from or otherwise detected in bats, the supposed connections between bats, bat viruses and hu- man diseases have been raised more on speculation than on evidence supporting their direct or indirect roles in the epidemiology of diseases (except for rabies). However, we are convinced that the evidence points in that direction and that at some point it will be proved that bats are competent hosts for at least a few zoonotic viruses. In this review, we cover aspects of bat biology, ecology and evolution that might be relevant in medical investigations and we provide a historical synthesis of some disease outbreaks causally linked to bats. We provide evolutionary-based hypotheses to tentatively explain the viral transmission route through mammalian intermediate hosts and to explain the geographic concentration of most outbreaks, but both are no more than speculations that still require formal assessment. Key words: bat-borne viruses - biosafety - Chiroptera - bat immunology - emerging infectious diseases - zoonosis Taxonomically, bats are grouped in the order Chi- carriers of rabies virus. This has been a disservice to both roptera (Gr. cheir, hand; pteron, wing) and, as the name our understanding of the biology of bats and to the vari- suggests, they have morphological and physiological ous medical and research communities and their patrons. adaptations for powered flight. These characteristics False images of bats engendered by entertaining, but pre- and the ecosystem services they provide set them apart posterous motion pictures, alarmist stories in the popu- from all other mammals. Other aspects of their natural lar press and ancient superstitions have been embedded history, ecology, biology and evolution also distinguish in the minds of the public and have impeded education them from other mammals, but none has been more em- and acceptance of these remarkable, useful and widely phasised recently than their potential link with human diverse animals. Thus, until relatively recently, studies of diseases, particularly those caused by zoonotic viruses the relationships of bats and viruses have lagged far be- (Wibbelt et al. 2010, Kupferschmidt 2013, Luis et al. hind studies of viruses in humans, livestock, birds, other 2013, Plowright et al. 2015). wild vertebrates and arthropods (Calisher et al. 2006). Although many bat viruses have been associated with With human encroachment on natural areas intensi- human, livestock and wild animal diseases, the sudden fying, particularly in those with high biological richness appearance of newly recognised viruses causing dread- (Myers et al. 2000, Ceballos & Ehrlich 2006) and bats rec- ful diseases has been surprising, sometimes shocking to ognised as important reservoirs of zoonotic viruses (Luis the scientific and medical communities. Humans have re- et al. 2013), considerable concern and interest have been sponded to these diseases in rapid and often unprepared expended on them. In addition, bats of some species adapt and disorganised ways. In part, this has occurred because well to disturbed habitats (Jones et al. 2009), so that these bat biologists have been in denial regarding their favou- vertebrates have quickly become a focus of epidemiologic rite mammals due to the fear of further damage to the studies. However, most epidemiologists know bats only illogical and false reputation of bats as vampires and as from outdated information or know very little or noth- ing about their biology, ecology and evolution. A similar situation occurs regarding bat biologists, many of whom know little or nothing about diseases ostensibly associ- ated with bats. In an attempt to fill the gaps in knowledge about bats in general, bats as virus hosts and bat diseases, we review many aspects of bat biology, ecology and evo- lution, which we expect will enlighten medical investi- doi: 10.1590/0074-02760150048 gations. In addition, we provide a historical synthesis of Financial support: PAPES, FIOCRUZ, CNPq (407623/2012-4), disease outbreaks causally linked to bats and which have CNPq/CsF (202612/2012), FAPERJ (E-26/111.288/2014), caused isolated deaths or severe outbreaks of diseases. Smithsonian Institution (USA) By linking these aspects, we then attempt to fit together RM current address: Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington DC, USA some pieces of this puzzle. We anticipate that this review + Corresponding author: [email protected] will stimulate collaborations between bat biologists and Received 3 February 2015 medical researchers in field and laboratory investigations Accepted 9 February 2015 concerning both basic and applied research. online | memorias.ioc.fiocruz.br 2 Bats and zoonotic viruses • Ricardo Moratelli, Charles H Calisher TABLE I Synthesis of the distribution and diet of bats by family Family (number of species)a Common namesb Distribution Feeding items Cistugidae (2) Winged-gland bats Southern Africa Insects Craseonycteridae (1) Bumblebee bats Thailand, Burma Insects, spiders Emballonuridae (54) Sheath-tailed bats Pantropical Insects, occasionally fruits Furipteridae (2) Smoky bats Neotropics Insects Hipposideridae (9) Old World leaf-nosed bats Old World tropics Insects and subtropics Megadermatidae (5) False vampire bats Old World tropics Arthropods, small vertebrates Miniopteridae (29) Bent-winged bats Old World tropics Insects and subtropics Molossidae (113) Free-tailed bats Pantropical Insects Mormoopidae (10) Moustached bats Neotropics Insects Mystacinidae (2) New Zealand short-tailed bats New Zealand Insects and other arthropods; also feeding on nectar and fruits Myzopodidae (2) Old World disk-winged bats Madagascar Insects Natalidae (12) Funnel-eared bats Neotropics Insects Noctilionidae (2) Bulldog bats Neotropics Insects; 1 specie feeds on fishes Nycteridae (16) Slit-faced bats Old World tropics Insects, spiders, scorpions; 1 specie feeds on small vertebrates Phyllostomidae (204) New World leaf-nosed bats Neotropics Animals and plants Pteropodidae (198) Old World fruit bats Old World tropics Fruits, nectar, pollen and subtropics Rhinolophidae (97) Horseshoe bats Old World tropics Insects and subtropics Rhinopomatidae (6) Mouse-tailed bats Old World tropics Insects Thyropteridae (5) New World disk-winged bats Neotropics Insects Vespertilionidae (455) Vesper bats Cosmopolitan Most species feed exclusively on insects, but a few also feed on other arthropods (like scorpions), fishes and small birds a, b: scientific and vernacular family group names and numbers of species follow Fenton and Simmons (2015). Biology, diversity and evolution of bats lossidae and Vespertilionidae occur in both the New and Old World, Cistugidae, Craseonycteridae, Hipposi- Diversity, distribution and biology - Bats vary widely deridae, Megadermatidae, Miniopteridae, Mystacinidae, in size and form. Their body masses range from 2 g in the Myzopodidae, Nycteridae, Pteropodidae, Rhinolophidae bumblebee bat [Craseonycteris thonglongyai (Craseo- and Rhinopomatidae occur only in the Old World, and nycteridae), the second smallest mammal known] to 1 Furipteridae, Mormoopidae, Natalidae, Noctilionidae, kg in some flying-foxes [Pteropus spp (Pteropodidae)], Phyllostomidae and Thyropteridae occur only in the New whose wingspans can reach 2 m (Wilson 1997). Among World. Table I provides information on distribution and mammals, bats are second only to rodents in species diet of bats by family. The evolution of flight – the most richness, with more than 1,300 species recognised cur- peculiar characteristic of bats and one of the most impor- rently (Fenton & Simmons 2015). This total comprises tant for their wide distribution – may have had effects on almost one fifth of the world’s mammal species, with some aspects of the evolution of the immune system and more than 175 genera (Simmons 2005, Wilson & Reeder the metabolism of bats, allowing them to host so many 2005) arranged in 20 families. viruses (O’Shea et al. 2014, Brook & Dobson 2015). Bats are distributed widely in the world, occurring Bats are nocturnal mammals (Rydell & Speakman on all continents, except Antarctica. They are the sec- 1995), with most of them spending the day in roosts and ond most widespread order of mammals, surpassed only foraging from dusk to dawn. In general, they have one by Primates due to the wide distribution of humans. Due or two peaks of activity throughout the night (Fenton to their ability to fly, they have colonised many oceanic 1983). Tropical bats are active year-round and those that islands and on some they are the only native mammals live in temperate zones either migrate or hibernate to (Koopman 1994). Among the families recognised cur- avoid unfavourable environmental conditions (Fenton rently (Fenton & Simmons 2015), Emballonuridae, Mo- 1983, Wilson 1997).