Adv Exp Med Biol - Advances in Microbiology, Infectious Diseases and Public Health (2017) 6: 35–48

DOI 10.1007/5584_2016_131
# Springer International Publishing Switzerland 2016
Published online: 9 October 2016

Bats and Emerging Infections: An

Ecological and Virological Puzzle

Jordi Serra-Cobo and Marc López-Roig

Abstract
More than 200 viruses have been detected in bats. Some unique bat
characteristics can explain the roles played in the maintenance and trans-
mission of viruses: long phylogenetic history can have originated coevo-
lution processes, great number of species are adapted to live in different
environments, big mobility, long lifespan and gregarious behaviour of
many species.
To analyse zoonoses long longitudinal studies are needed with a multi-
disciplinary approximation to obtain the following eco-epidemiological
data: colony size, number of bats per species, population structure,
behaviour of each species, degree of contact between bats, social structure,
remaining time of bats in the colony, colony type, foraging area, turnover
rate of individuals, shelter temperature, relationship with other colonies
and co-infection processes. These data allows assessing the epidemiologi-
cal risk and which preventive measures are necessary to take.
The structure and functionality of ecosystems are changing worldwide
at an unprecedented rate and can modify the interactions between humans
and infected bats. There are more or less local factors that can affect the
emergence and spread of diseases (environmental alterations, changes in
land use, human population growth, changes in human socioeconomic
behavior or social structure, people mobility increase, trade increase,
forest fires, extreme weather events, wars, breakdown in public health
infrastructure, etc.).
Twenty-three percent of all bat species in the world are decreasing.
How does the regression of bat species affect the dynamic of viruses? The

J. Serra-Cobo (*) and M. López-Roig

Departament de Biologia Evolutiva, Ecologia i Ciències
Ambientals, Universitat de Barcelona, Institut de Recerca
de la Biodiversitat, Av Diagonal 643, 08028 Barcelona,
Spain
e-mail: serracobo@areambiental.com

35
36 J. Serra-Cobo and M. López-Roig

dichotomy between health risk and bat preservation is compatible with a

preventive task based on more information and training.

Keywords
Bats • Zoonoses • Emergent viruses • Bat ecology • Public health

1 Introduction weight to the importance of bats as reservoir and

they play a key role in dynamic of viruses
The result of millions years of evolution has given (O’Shea et al. 2014). For example, numerous
rise to an extraordinary biodiversity with com- bat species can be infected by lyssaviruses. Bats
plex inter and intraspecific interrelations of the serve as reservoirs of 13 out of the 15 lyssavirus
species and also with the environment in which species described (the only lyssavirus species
they live. Each host species performs a specific that have not been isolated from bats, to date,
ecological function, followed by a particular are Mokola virus and Ikoma virus). Furthermore,
story and interacts with other species and their recently described lyssavirus species enlarged
environment. The million years of evolution also the genetic diversity of lyssaviruses found in
has given rise to the co-evolution processes bats, suggesting that the lyssaviruses originated
between host and pathogen, very important to in these mammals and progressively diverged
understand the virus dynamic in host populations. from a common ancestor (Badrane and Tordo
All these complex interrelations between host- 2001; Delmas et al. 2008).
pathogen-environment require analysis of multi- The epidemiological studies made about bats
ple biological and environment factors and this is raise different questions. Why are bats good
only possible with a multidisciplinary approach. virus reservoirs? What is the dynamic of viruses
All these factors must be taken into account in in bat populations? Are there processes of
eco-epidemiological studies and are very impor- co-evolution between bats and pathogens? Can
tant in order to find preventive measures that the environmental changes influence the
reduce the risk of transmission to the human dynamic of viruses and the risk of transmission
population, livestock and pets. to humans? What are the main gaps in the study
The evolution of bats is a very successful of bat zoonosis? Which are the risk factors and
singular history amongst the mammals that has the prevention tasks? These questions have no
produced an enormous diversity of species simple answers because it requires a multidis-
adapted to a great spectrum of environments. ciplinary approach that should take into account
In recent years, bats have been implicated in a diverse range of abiotic and biotic factors.
numerous emerging infectious disease events The world in which we live is extremely com-
and have been recognized as important reservoir plex, with a multitude of relationships between
hosts for viruses that can cross the species barrier living organisms and the environment where
to infect humans and other domestic and wild they live. For example, the emergence of a
mammals (Calisher et al. 2006; Hayman viral epidemic will depend on the dynamics of
et al. 2013; Moratelli and Calisher 2015). More the virus, which in turn will be influenced by
than 200 viruses of 28 families have been external environmental factors. The dynamics
isolated or detected in bats, distributed in the of the reservoir species influence the virus
two suborders, 11 families and 37 genera of dynamics. But the reservoir depends on factors
bats (Table 1). These viruses apparently cause such as temperature, rainfall, state of conserva-
little or no pathology in bats. A comparative tion of the habitat, the situation of stress affect-
analysis (Luis et al. 2013) showed bats to be ing the species, etc. The aim of this paper is to
more likely to be infected with more zoonotic contribute to elucidate this ecological and viro-
viruses per host species than rodents, thus adding logical puzzle.
Bats and Emerging Infections: An Ecological and Virological Puzzle 37

Table 1 Viruses found in bats Table 1 (continued)

Virus Genus Virus Genus
Family Adenoviridae Mastadenovirus Family Poxviridae Molluscipoxvirus
Family Arenaviridae Arenavirus Family Reoviridae Orbivirus
Family Astroviridae Mamastrovirus Orthoreovirus
Family Bornaviridae Unnamed genus Rotavirus
Family Bunyaviridae Orthobunyavirus Family Retroviridae Betaretrovirus
Hantavirus Spumavirus
Phlebovirus Gammaretrovirus
Nairovirus Family Lyssavirus
Family Caliciviridae Sapovirus Rhabdoviridae Vesiculovirus
Family Circoviridae Circovirus Family Togaviridae Alphavirus
Cyclovirus Family Totiviridae Totivirus
Family Alphacoronavirus Unassigned family Hepevirus
Coronaviridae Betacoronavirus (SARS,
MERS)
Family
Dicistroviridae 2 Why the Bats Are Good Virus
Family Filoviridae, Cuevavirus Reservoirs?
Ebolavirus
Marburgvirus The roles played by bats in the maintenance and
Family Flaviviridae Flavivirus transmission of viruses requires consideration of
Hepacivirus the unique characteristics that distinguish bats
Pegivirus from all other mammals.
Pestivirus
Family Orthohepadnavirus
Hepadnaviridae
Family Hepeviridae Unnamed genus 2.1 Evolution and Phylogeny
Family Herpesviridae (Alpha-herpesvirinae) of Bats
Simplexvirus
(Beta-herpesvirinae) unnamed
genus The origin of bats is estimated in about 64 mil-
Cytomegalovirus lion years ago at or following the Cretaceous-
Percavirus Tertiary boundary. The Order Chiroptera is clas-
Rhadinovirus sified in Yinpterochiroptera (Rhinolophoidea
Macavirus and Pteropodidae) and Yangochiroptera (all
Family Nodaviridae Nodavirus other bat families) (Teeling et al. 2005). Hence
Family Influenzavirus A this long period of time can have originated
Orthomyxoviridae coevolution processes between bats and viruses.
Family Omegapapillomavirus
Papillomaviridae
The analysis done by Luis et al. (2013) indicated
Family Morbillivirus that bats host more zoonotic viruses and more
Paramyxoviridae Henipavirus total viruses per species than rodents, despite
Rubulavirus there are a lot more of rodent species in the
Pneumovirus world. Zhang et al. (2013) did an extensive geno-
Family Parvoviridae Dependovirus mic analysis of two distantly related species of
Bocavirus bats and found a concentration of positively
Family Picobirnavirus selected genes in the DNA damage checkpoint
Picobirnaviridae
and nuclear factor kB (protein complex that
Family Kobuvirus
Picornaviridae
controls transcription of DNA) pathways that
Family Unnamed genus may be related to the origin of flight. These
Polyomaviridae authors propose that the flight evolved in tandem
(continued) with concomitant genetic changes to their innate
38 J. Serra-Cobo and M. López-Roig

immune systems. These changes were related to The diversity of bat species and their world-
the need of DNA damage repair because of high wide distribution contribute to the biodiversity of
metabolic rates that are produced during flight. their pathogens.
Baker et al. (2013a, b) suggested the possibility
that bats might be able to control viral replication
through innate immunity. 2.3 Ability to Fly

Bats have a high mobility and have the potential

2.2 Species Richness to spread rapidly and widely the viruses. The
flight provides them more mobility than the
The bat evolution has led to a great number of greatest part of terrestrial mammals have, includ-
species adapted to fly, to consume a wide range ing rodents. Some species can do long seasonal
of food resources and live in very different movements, behaviour that can enable the virus
environments, characteristics that allowed them spread into regions that are more or less far away.
to colonize much of the terrestrial ecosystems. The migration is an important component in the
We find bats in deserts oasis, tropical and subtrop- life cycle of numerous animals, especially in a
ical rainforests, plains near the sea, mountains changing world in space and time. The seasonal
relatively high, islands far from continents, tem- movements not only allow to escape from the
perate regions, boreal regions, etc. There are insec- adverse conditions, but also possibilities the
tivorous, frugivorous, carnivorous, piscivorous, exploitation of news habitats and contribute to
haemtophagous, nectarivorous, and scavengers the gen flow between colonies. Cross
bat species, and there are also bats that eat et al. (2005) showed that the probability of a
scorpions. Bats are the second largest order of pandemic event depended on the interaction
mammals and currently, there are ~1200 world- between colony size and movement of hosts
wide recognized bat species, accounting for amongst groups during their infectious lifetime.
approximately 21 % of all mammalian species. They suggested that the gregarious hosts that
Every year new bat species from around the form large groups and frequent movements are
world are described, found not only in tropical more heavily impacted by acute diseases than
and subtropical regions but also in temperate hosts with small groups and infrequent move-
regions. The species richness increases towards ment. It is possible to find examples of long bat
the tropics and in most tropical areas bat diversity migrations in all continents. Some African spe-
is higher than in any other group of mammals cies perform seasonal migrations between rain
(Moratelli and Calisher 2015). forest areas, where they remain during the dry
They are the only mammals that can fly and season, and savannah areas where they frequent
they play a major ecological role as insect during the rainy season (Ossa et al. 2012). Eido-
predators, seed dispersers and pollinators. lon helvum is an African bat species on which it’s
Approximately 75 % of microchiroptera species found neutralizing antibodies against Zaire
are insectivorous and make an important control ebolavirus. This species forms big colonies and
about the insect populations. In a longitudinal does seasonal migrations that can exceed the
study done in Natural Park of Sant Llorenç del 2500 km (Sørensen et al. 2001; Richter and
Munt i l’Obac (Barcelona, Spain), we estimate Cumming 2008; Hayman et al. 2013).
that Miniopterus schreibersii population in about E. helvum can play a role in the spread of
17,000 individuals that could annually consume filoviruses. In this sense, Ogawa et al. (2015)
between 15 and 30 tonnes of insects. McCraken suggest in their work on E. helvum the introduc-
estimated in about 10 tonnes of insects the daily tion of multiple species of filoviruses in the
consume of a big breeding colony constitute by a migratory bat population and point to the need
million of Tadarida brasiliensis that lived in for continued surveillance of filovirus infection
Texas (McCracken and Wilkinson 2000). of wild animals in sub-Saharan Africa, including
Bats and Emerging Infections: An Ecological and Virological Puzzle 39

hitherto nonendemic countries. Pons-Salort could be expelled from the nostrils of

et al. (2014) show the importance that can have echolocating bats (Constantine et al. 1972;
Miniopterus schreibersii in the dynamic of Winkler 1968).
European Bat lyssavirus on the bat populations
of Balearic Islands. They found that EBLV-1
could not be sustained if transmission between 2.4 Long Lifespan and Bat Ecology
M. schreibersii and other bat species was
eliminated. This species can do seasonal The existence of a trade-off between lifespan and
movements of some 100 km and can move reproduction is central to the concept of life
between Mallorca and Menorca islands history strategy (Partridge and Harvey 1988;
(Amengual et al 2007a, b). Stearns 1992). Organisms cannot simultaneously
Bats, except for most species of maximize both of these traits in the nature
megachiroptera, emit ultrasounds to orient them- (resources are limited) but must balance invest-
selves during the flight, to communicate between ment in survival versus offspring to maximize its
them and also to locate and capture their prey. lifetime reproductive fitness. Moreover, in stable
Lazzaro Spallanzani, considered one of the populations, survival and birth rates must be
fathers of experimental biology, observed in inversely related (Sibly and Calow 1987). The
1793 that bats that were bereft of vision were evolution of life history therefore is constrained
able to orient themselves without any problem. along a slow–fast continuum strategies, in which
Later, Spallanzani and Jurine found that bats species with slow life histories generally have
need the sense of hearing to navigate and orient higher survival rates, live longer maximum
themselves during flight. It was not until 1941 lifespans, mature at older ages and produce
that Griffin and Galambos showed that bats use fewer young per year compared with species
ultrasound for orientation. Griffin proposed the with fast life histories. The bats belong to this
term echolocation to define the process by which type of life history and they have a long lifespan
bats locate objects that can not see or touch greater than most of mammal species of the same
thanks to the emission of acoustic signals and size (for example mice and shrews). The greater
its echo analysis. We can distinguish two groups longevity observed in a bat is 41 years in a
according to the type of bats that emit ultrasonic Myotis brandtii (Wilkinson and South 2002).
signals: the species that emit ultrasonic signals of However, the longevity of most species is much
constant frequency and narrow frequency band lower. The greater lifespan observed in our stud-
(these bats use as a nasal cavity as a resonator ies ranged from 8 years in Pipistrellus khulii to
organ); species that emit FM ultrasonic signals 17 years in R. ferrumequinum. The extreme lon-
with a frequency of wideband (these bats use gevity of bats, together with the possibility that
buccal cavity as a resonator organ), where the they might develop persistent infections with
frequency is modulated by the position of the certain viruses, may help to maintain the viruses
tongue and lips. and transmit them to other vertebrates.
Production of such loud sounds could gener- Lifespan is generally longer in heterothermic
ate droplets or small-particle aerosols of oropha- mammals (such as bats) than in related
ryngeal fluids, mucus, or saliva, enabling homeotherms. Heterotherms can employ several
transmission of viruses between individuals in strategies (as hibernation) to withstand adverse
close proximity. Airborne rabies virus transmis- periods and then repopulate when circumstances
sion was documented in a large colony of Mexi- improve. Hibernation is associated with high
can free-tailed bats constituted by several million rates of overwinter and annual survival and an
of individuals (Constantine 1967). Furthermore, increase in survival in hibernating species is
the isolation of rabies virus from mucus obtained linked to the coevolution of indicative traits of
from naturally infected same species of bats relatively slow life histories (Turbill et al. 2011).
could support the hypothesis that rabies virus Endothermic mammals have the ability to
40 J. Serra-Cobo and M. López-Roig

maintain a constant high body temperature et al. 2003). In this sense, bats exhibit selection
(Tb) over a wide range of ambient temperatures in roost choice, showing preferences linked to
(Ta). However, keep a constant high Tb can have their ecological requirements, which differ
a high energetic cost. This is especially critical among species, different seasons (Kunz 1982;
for small mammals because heat loss increases Kunz and Lumsden 2003) and geographical
with decreasing size as a result of increasing areas (Rodrigues et al. 2003). Bats spend a con-
relative surface area. Small size also limits the siderable part of their life roosting, and thus roost
relative amounts of fat that can be stored. As heat characteristics have important implications for
loss is a function of the Tb-Ta differential, ther- survival and reproductive success (Kunz 1982).
moregulatory costs at low Ta may become Roost location, structure and aspect determine
prohibitively expensive in small endotherms, microclimatic conditions, which may influence
especially when energy availability is low the energetic costs of key stages of life cycle
(Kronfeld-Schor and Dayan 2013; Geiser 2004). such as hibernation (Humphries et al. 2002),
For this reason, bats use two common patterns pregnancy and lactation (Sedgeley 2001; Kerth
of torpor as physiological and behavioral adapta- et al. 2001). Consequently, summer and winter
tion that permits survival during seasonal periods shelters often differ in microclimates conditions
of low resources: daily torpor and hibernation or and bat populations move seasonally between
multiday torpor. them, thereby connecting seemingly isolated
Daily torpor is widely used in bats and it is an populations. The metapopulation structure,
important strategy for coping with fluctuating social organization within the refuges (intra-
environments, involves significant plasticity, and interspecific interactions), where multiple
and may constitute an important part of how bat species usually cohabit, can play important
endotherms cope with environmental challenges. roles in the dynamics of virus persistence. Per-
The daily torpor is not as deep as hibernation, sistent viral infections occurring among long-
lasts only for hours rather than days or weeks, lived bats together with their often gregarious
and is usually interrupted by daily foraging and roosting behaviour, could greatly increase the
feeding. Bats used daily torpor in response to potential for intra- and inter-species transmission
adverse conditions such as low food availability of viruses (Halloran 1998). Some bat species
and low ambient temperature, mainly when their form a very large monospecific or multispecific
mass and fat stores are low (Geiser 2004; Geiser colonies of thousands individuals tight against
and Stawsky 2011). each other (Fig. 1). For example, we estimated
Hibernation is often seasonal and usually lasts the density of the hibernation colony of
from late autumn to late winter/spring. However, M. schreibersii that lives near Barcelona in
hibernating bats do not remain torpid throughout 1900 bats for square meter. This dense clustering
the hibernation season. Bouts of torpor, during of individuals can provide large opportunities for
which body temperature (Tb) is low and bodily viral exchange in bat colonies. However, apart
functions are reduced to a minimum, last for from the colony size, bat species richness appear
several days or weeks, but are interrupted by to be another ecological factor strongly
periodic rewarming and brief (usually less than associated with European bat lyssavirus type 1
1 day) normothermic resting periods with high seroprevalence in bat colonies (Serra-Cobo
Tb and high energy turnover. Over-winter sur- et al. 2013). The bat colonies are often composed
vival of hibernating bats should depend primarily by more than one species, which may facilitate
on the size of their energy reserves at the onset of the virus transmission between species. For
hibernation, the rate at which the energy store is example, in South of Europe there are mixed
depleted during winter, and the length of the colonies where M. schreibersii, M. myotis and
winter. If the size of the reserve is less than the M. capaccinii have direct physical contact
rate of depletion times the length of winter, the amongst them and also their urine and guano.
hibernator will not survive (Humphries This suggests that interspecies virus transmission
Bats and Emerging Infections: An Ecological and Virological Puzzle 41

Fig. 1 Multispecies bat

colony of Myotis punicus
and Miniopterus
schreibersii shelter in a
Moroccan cave. The two
bat species are tight against
each other

plays an important role in EBLV-1 dynamics. A bat lyssavirus dynamics exhibit a strong seasonal
high number of species might not only increase pattern and that the breeding period could favor bat
the rates of contact between bat groups and spe- infection (George et al. 2011; Serra-Cobo
cies, but also could facilitate virus entry or spread et al. 2013). We analyzed ecological and epidemi-
through the higher mobility of individuals among ological factors that might be associated with the
colonies, especially if these bats exhibit a migra- infection dynamics of EBLV-1 observed in Span-
tory behaviour. ish bat colonies. The analyses revealed that the
colony size and species richness were two impor-
tant ecological factors and showed their relevant
3 Virus Dynamic in Bat roles in seroprevalence variability. Higher sero-
Populations prevalence was observed in multispecies colonies
compared to monospecific colonies, suggesting
The dynamic of viruses is the result of the inter- that interspecific virus transmission plays an
action between the characteristic of pathogen, the important role in EBLV-1 dynamics. The results
life history traits of host population and the envi- suggested that EBLV-1 seroprevalence was
ronmental factors. The seasonality existing in strongly affected by the colony size and species
great part of the world (winter, spring, summer, richness, and indicated that multispecies, large
autumn, dry and rainy seasons) determines the colonies, especially those with three or more dif-
birthing periods, migration, gregarious behavior ferent bat species, had a higher probability of
and the torpor of bat species. Each of these EBLV-1 infection (Serra-Cobo et al. 2013).
aspects of the bat life may affect population Large colonies and multispecies associations
density, rates of contact between individuals occurred frequently among cave-dwelling bats,
and immune response, thus leading to spatiotem- principally during the maternity period. This colo-
poral variation in infection dynamics (George nial behaviour confers thermodynamic and social
et al. 2011; Hayman et al. 2013). advantages to reproductive females during preg-
Some authors suggest that the pathogen repli- nancy and lactation (Willis and Brigham 2007).
cation in the host is generally very temperature- In order to know the virus dynamic is neces-
dependent (Sadler and Enright 1959; Sulkin sary to carry long longitudinal studies with a
et al. 1960; Luis and Hudson 2006; Bouma multidisciplinary approximation. The long active
et al. 2010). Different studies demonstrated that surveys can provide information about the
42 J. Serra-Cobo and M. López-Roig

dynamic of the host population and the cycles and the lifespan of immunity in front of a virus
followed by virus infection. The work of moni- infection can differ between bat species. So, it is
toring the bat colonies usually is not easy. Their more likely to find seropositive bats in the spe-
shelters have often difficult access, it’s necessary cies with long lifespan immunity. This is a factor
to work during night and are animals with a great to consider in the serological active survey. For
mobility, factor that difficult their recapture. The example, EBLV-1–seroprevalence differences
long longitudinal studies of bat colonies using were found between bat Vespertilionidae and
capture-mark-recapture techniques can provide Rhinolophidae families. This variability might
the infection history at individual level in species be explained by different immunological
with long lifespan. These studies also allow responses of the bat species to EBLV-1 virus.
obtaining demographic and epidemiological These differences might rather suggest different
parameters (mortality, survival and turnover seroconversion rates in these two families (Serra-
rates, colony size, immune lifespan, period of Cobo et al. 2013). Despite his interest, there is
infections cycles, distribution of individuals very few information about the lifespan of immu-
infected in the colony, basic reproductive rate nity of bat species in front of viruses infection.
of virus, threshold population for infection). The threshold levels of host abundance for inva-
The basic reproductive number (R0) is an sion or persistence of infectious diseases are an
important parameter in the diseases dynamic and important epidemiological parameter. The notion
is the average number of new infections that would of a threshold population for invasion is a founding
arise from a single infectious host introduced into a principle of epidemiological theory (Lloyd-Smith
population of susceptible hosts. The immunity et al. 2005). This parameter is important in the
induced by many viral infections reduces the num- gregarious bat species. But in order to be applicable
ber of susceptible individuals, which reduces R0, is necessary to know the spatial structure and
which therefore tends to lead to a decline in the dynamic of the population. Most of gregarious
incidence of the infection itself in the colony. species of bats have a metapopulation structure
However and before the infection disappears (consisting of periodically interacting, spatially dis-
from the population, it is likely there is an influx crete subpopulations) with variations in their
(births, immigration and loss of immunity) of new subpopulations. The total number of individuals
susceptible into the population that will produce a in the various subpopulations must be sufficient to
subsequent increase in susceptible and R0, and so maintain virus circulation in the metapopulation
on. Theoretical works about disease invasion have over time, while immunity or death due to viral
assumed large and well-mixed host populations. infection extinguishes transmission chains within
However, many wildlife systems have small individual subpopulations. We observed this phe-
groups with limited contacts amongst them. In nomenon of local virus extinctions in bat colonies
these situations, the R0 is likely to be a poor pre- from Spain that follow a metapopulation structure.
dictor of a disease pandemic because it typically All efforts to eradicate wildlife diseases by reduc-
does not account for group structure and contacts ing the numbers of susceptible hosts through con-
of individuals amongst groups. For example, Kerth troversial methods such as culling, sterilization, or
et al. (2011) detected two stable subunits in a larger vaccination are based in the threshold concept.
colony of Myotis bechsteinii and each of them However, the general applicability of standard
comprised bats from several family lineages. threshold concepts in wildlife disease systems is
These authors showed that the links between very difficult and often forgets many factors rele-
these subunits were mainly maintained by older vant to natural populations (turnover rate of popu-
bats and persisted over all years. lation, migrations, immunity loss).
The immunity lifespan is a parameter that A long longitudinal study done from 1995 to
should be taken into consideration in epidemio- 2006 demonstrates cyclic EBLV-1 infection in
logical studies because influences the disease spatial discrete subpopulations of M. myotis in
dynamic in a bat colony. The immunity response Spain, without any significant increase in
Bats and Emerging Infections: An Ecological and Virological Puzzle 43

Fig. 2 Interannual
variations of seropositive
bats observed in a Myotis
myotis colony from
Mallorca (Spain). Results
obtained together with
H. Bourhy team from
Institut Pasteur (Paris)

associated mortality. The data provided by this facilitate information about the virus transmis-
longitudinal study was the first evidence that sion between species. The longitudinal study of a
mortality of M. myotis in their natural environ- T. teniotis and Plecotus austriacus colony
ment does not increase significantly after showed significant inter-annual fluctuations in
episodes of EBLV-1 infection (Amengual percentage of seropositive bats. However, signif-
et al. 2007a, b). The monitoring of these colonies icant differences were observed in the temporal
until 2015 showed that the M. myotis immunity patterns of the seroprevalence modelling of
could persist for 2 years (Fig 2). During the T. teniotis and P. austriacus. The behavioural
20 years of survey we observed periodic ecology of the species involved could explain
oscillations in the number of susceptible, the different annual fluctuations in EBLV-1 sero-
immune and infected bats. The delay between prevalence (López-Roig et al. 2014).
the waves was dependent on the rate of inflow Works that consider co-infection processes in
of susceptible bats into the colonies as a conse- hosts that are produced by more than one parasite
quence of new births, immigration of naive and their interactions are not abundant. The epi-
animals from neighbouring colonies, and expira- demiological studies usually analyse a single
tion of EBLV-1specific immunity in previously pathogen. The results obtained by Munson
infected animals. When a sufficient fraction of et al. (2009) in a study done in two lion
susceptible individuals in the bat population was populations from Serengeti and Ngorongoro Cra-
reached, the virus spreads again if infected ter shows the importance that might have the
individuals joined the colony. Here we showed processes of co-infections in wildlife. These
the cycles observed in M. myotis seroprevalence authors observed a high mortality in lion
for EBLV-1, but the characteristics of these populations affected by a canine distemper
cycles can change according to the zoonotic virus epidemic. They show that lions were
diseases and the host species. infected by unusually high numbers of Babesia,
Only a few studies have addressed the inter- infections that were magnified by the immuno-
annual dynamics of lyssavirus amongst bat mul- suppressive effects of coincident canine distem-
tispecies that are roosting in the same refuge per virus epidemic. Complex interplay between
despite these studies are giving a better under- epidemic and endemic pathogens that are nor-
standing of the dynamics of bat lyssaviruses and mally tolerated in isolation, but with
44 J. Serra-Cobo and M. López-Roig

co-infection, result in unusually mortality. pathogens in wild populations; and (3) the fre-
Bats have been recognized as important reservoir quency of human contact and pets with wild
hosts for emerging viruses and despite this, there animals potentially zoonotic reservoirs (includ-
is a big lack of knowledge about co-infection ing not only direct contact with the animals but
processes. Studies about co-infection processes also with their droppings, saliva or urine). More-
might contribute to understand the viruses over, the structure and functionality of
dynamic in the colonies and possible outbreaks. ecosystems are changing worldwide at an
On the other hand, the studies of a single parasite unprecedented rate (Jones et al. 2009) and affect
may drive incorrect or incomplete epidemiologi- the three factors exposed. These changes can
cal conclusions. modify the interactions between humans and
In summary, the knowledge of virus and host infected animals, in our case bats. The emer-
dynamics is relevant in terms of public health gence of a disease is often the result in changes
because it allows assessing the epidemiological from ecology of the host or the pathogen, or in
risk and also to take preventive measures. both. In this sense, various authors assert that
Analysing the virus dynamic in bat colonies is environmental changes and ecological
important to obtain the following eco- disturbances, due to natural phenomena and
epidemiological data: the number of species that human activities, have a strong influence on
form the colony, how many bats there are of each emerging diseases (Patz and Wolfe 2002;
species, the structure of the population, the McMichael 2004). Interest has grown in knowing
behaviour of each species (for example, is impor- how and to what extent environmental changes,
tant to know if there are one or more migratory especially global climate change, affect the
species that might spread the virus), the degree of dynamics of infectious diseases. Much attention
contact between them, the social structure, how has been accorded to the role and potential
much time the individuals of the colony rest impact of global environmental changes on the
together, colony type (reproduction, mating, hiber- dynamics of infectious diseases. But there are
nation), the foraging area of species, the turnover other more or less local factors that can affect
rate of individuals, the shelter temperature and the the emergence and spread of diseases. For exam-
relationship with other colonies, the co-infection ple, environmental alterations, changes in land
processes. use of a region, human population growth,
changes in human socioeconomic behavior or
social structure, people mobility increase, trade
4 Changes in Ecology increase, forest fires, extreme weather events,
and Management of Bat wars, breakdown in public health infrastructure,
Populations etc. Understanding infectious diseases beyond
the scale of individual clinical cases requires
Wildlife plays a key role in emerging infectious assessment of ecological and evolutionary
diseases by providing a “zoonotic pool” from perspectives. Changes in abundance of reservoir
which the pathogens may emerge (Daszak hosts can increase transmission risk of zoonotic
et al. 2000). Zoonotic pathogens represent virus for humans, livestock and pets. Land modi-
approximately 60 % of all known pathogens fication, changes vegetation paterns,
able to infect humans. Many emerging viral disturbances in vector and host species dynamics
zoonoses arise from greater contact between and microclimates changes can increase the con-
human populations, livestock and pets with wild- tact between human or livestock and wildlife
life reservoirs of pathogens. The risk of zoonotic (Karesh et al. 2012). For example, local episodes
viruses in a given region depends largely on three of Ebola diseases have taken place regularly for
factors: (1) the prevalence of the virus in wild years in Africa. Studies based on analysis of
species that inhabit the region; (2) the effects of poleovirus estimate the age of the divergence
environmental changes on the prevalence of between Marburgvirus and Ebolavirus at early
Bats and Emerging Infections: An Ecological and Virological Puzzle 45

Miocene (Taylor et al. 2014). It is therefore new inhabitants of the area. Some of the animals
likely that the Ebola virus has been present in that hardly had contact with humans now can
Africa for many years. Also is likely that the have it. The contacts may be important if any of
virus were in bats for many years. However, the animal species is the reservoir of zoonotic
unlike the epidemic that occurred in viruses and can infect locals, their livestock or
2014–2015, in previous outbreaks the number pets. Therefore, it is possible the contact between
of cases was relatively small. Why an epidemic the human species and certain pathogens that
of colossal proportions not comparable with ear- remained more or less isolated in their animal
lier outbreaks occurred in 2014? What has reservoirs. An example is the Nipah virus out-
changed? Probably there has been more human break occurred in 1998–1999 in Malaysia. The
contact with bat species or contact with others outbreak has been linked to intensification of pig
infected mammals and higher mobility of people, farming. More than 100 people died during this
factors that may have contributed to this epi- outbreak and more than one million pigs were
demic. In this regard, in March 2014 Ebola killed to control the disease (Chua et al. 1999;
infections had already spread outside the village Karesh et al. 2012; Hayman et al. 2013). The
where there was the initial case and had arrived infections were produced by the direct or indirect
to Guinea capital, Conakry, a city with over a (urine, guano) interaction between fruit bats
million and half inhabitants. The current people and pigs.
mobility has no precedent and is a very important The deforestation rate can be very high in
epidemiological factor to take into account, certain African regions, such as in Cameroon
because it increases the risk of diseases spread. where tree cover loss is estimated at
Hence to determine which are the causes of epi- 800–1000 km2 annually for road construction
demic Ebola whose origin seem to be the bats, it and expansion of human settlements. According
is necessary to conduct a multidisciplinary to Wolfe et al. (2005), deforestation promotes
approach. This study needs to provide informa- bushmeat trade in Cameroon and increases the
tion on the dynamics of pathogens in wildlife, contact between hunters and wildlife. The open-
interactions between humans and wildlife, ing of roads for logging also provides at hunters
anthropogenic pressures on wildlife populations better access to hunting areas that until today
and socio-economic changes that have occurred were hardly accessible. Exposure to new
in human societies that live in the region where pathogens is not always the result of a more or
the epidemic originated (Serra-Cobo 2016). The less important exploitation of forest areas, pov-
deforestation of areas to perform human erty also leads people to expand their range of
activities, either to find new resources, install activities to survive into the rainforest in search
farms, crops, houses, roads,. . . is generally of new resources.
analysed in terms of loss or alteration of The overall trend of the populations of bats is
biological diversity (loss or reduction of species). evident in the data presented by the IUCN under
However, the consequences of deforestation can which 23 % of the all bat species that live in the
be much more important and unpredictable than world are considered to be decreasing (The
it might seem at first glance. Some of the animals IUCN Red List of Threatened Species 2015-3
leave the area deforested toward new areas while http://www.iucnredlist.org/search). How does
others remain in the area where they lived before the regression of bat species affect the dynamic
the alteration. The species that continue to of viruses? We have little information about this
develop its activity in the deforested area, unlike question and it represents an important
what happened previously, are much more likely eco-epidemiological point for analysis. The
to come into contact with the human population, shelters are usually vulnerable to a wide range
either directly or indirectly through livestock or of threats, which in recent years have led to the
pets. So, they continue searching for food and loss and fragmentation of habitats. Our
shelter, and may enter farms and houses of the observations, over the past 32 years in Spain,
46 J. Serra-Cobo and M. López-Roig

indicate that bat-shelter alterations are frequent We reckon five different ways: by bite, by
and cause the disappearance or a partial reduc- inhalation of viral particles, by scratches done
tion of the bat colonies. Such latter phenomena due to direct contact with bats, by eating bats
promote the between-colony exchange of (probably this has been the beginning of Ebola
individuals and big changes in metapopulation epidemic in Africa) or by being in contact with
structures of bat species. The environmental something that had previously been in contact
disturbances that affect shelters of large bat with bats or their urine or guano (fruits, water,
colonies have a big impact on the species. etc.). Another factor that should be considered
These changes have incidence on the ethology is the synanthropic character of some bat spe-
and ecology of species, which has resulted in cies. Due to important loss of habitat, some bat
demographic changes in populations of different species have found shelter in human
species and changes in land use. In some species, environments (houses, underground, farms,
there is the tendency of bats being concentrated churches, mosques, etc.), increasing exposition
in a smaller number of shelters with largest of humans to pathogens. Synanthropic species
colonies. In this sense, the formation of relatively are possible to be found in all continents. In this
large colonies, distributed in fewer shelters, sense, we should always avoid direct contact
presents a higher risk for species conservation with bats or with their urine or guano.
than the distribution of relatively smaller In order to decrease the risk of viral transmis-
colonies in more numerous shelters. Also, the sion is important to take the following
formation of large colonies may increase the recommendations: do not touch the bats, if you
probability of virus presence. need to handle bats do protect the hands and
wash them often with soap, avoid any contact
with bats guano (in a lot of shelters there is big
5 Risk Factors and Prevention amount of guano in which numerous infectious
Tasks agents for humans live, ie, viruses, bacteria,
fungi), develop training about the risks and
Are bats dangerous? On one hand bats play benefits that involve bats with the objective to
ecological important roles and place high learn good practices and preserve the bat
levels in the ecosystems where their live and populations from disturbances that can change
this is the reason why is necessary to preserve the colony dynamic and the viruses
them. But on the other hand, they are host of transmission risk.
emergent zoonosis. Apparently, we are in the The bat preservation, especially insectivo-
dichotomy between the health risk and the bat rous species, is very important in a time where
preservation. What shall we do? The answer is vector species and zoonotic viruses spread in
not easy and a lot of factors have to be consid- large regions over the world. In the last years
ered. It is important to take into account that different mosquitoes of Aedes species have
bats can have some zoonotic viruses without colonized large areas of Europe. These species
having signs of diseases, which can reduce the can be potentially vectors of zoonotic viruses
perception of risk and difficult the prevention (flavivirus and alphavirus). In this sense, the bat
tasks. Most bat species are not aggressive if insectivorous species can play a major role in
they are not disturbed, which is helpful to the vector control and in the reduction of
reduce the risk of viruses transmission. transmission risk.
Another factor to be taken into account is that
the health risk of bats for humans is different Acknowledgments This paper was written thank to the
depending on the region of the world and the European project No. 278433 PREDEMICS (“Prepared-
ness, Prediction and Prevention of Emerging Zoonotic
species considered. Which are the ways that
Viruses with Pandemic Potential using Multidisciplinary
bats can transmit viruses? The ways can be Approaches”). We wish to acknowledge Marta Bordas her
different depending on the viruses considered. cooperation.