**6. Anthropization, human behavior, and dynamic of emergence**

rate between susceptible hosts and infectious individuals. Social organization within the refuges thus plays a major role in virus transmission. Some bat species form a very large and tight monospecific or multispecific colonies of thousands individuals, e.g. the density of a hibernation colony of *Miniopterus schreibersii* near Barcelona was estimated at 1900 bats for square meter [58] (**Figure 4**). *Tadarida brasiliensis Mexicana* forms in Carlsbad Cavern (New Mexico), a colony with 793,838 bats [59]. This gregarious roosting behavior can provide large opportunities for viral exchange in bat colonies. Bat colonies are often composed by more than one species. Large colonies and multispecies associations are frequent among cave-dwelling bats, in particular during the maternity period. This colonial behavior confers thermodynamic and social advantages to reproductive females during pregnancy and lactation [60]. For instance, mixed colonies can be found in Southeastern Europe where *Miniopterus schreibersii*, *Myotis myotis*, and *Myotis capaccinii* are in direct physical contact. This cohabitation can facilitate virus transmission between species. The seroprevalence for EBLV-1 in *Myotis myotis* and *Miniopterus schreibersii* followed the same temporal pattern during 4 years [45], which could be explained by virus transmission between these two species. The size of the colony and species richness were two important ecological factors playing a major role in seroprevalence variability [45]. Virus transmission in colonies may follow different ways depending on the bat and virus species considered, i.e. aerosols, contact with feces, urine, blood, or other body fluids, or by bite. Ectoparasites should also be considered. There are almost no data on vertical transmission from mother to fetus. However, vertical transmission has nevertheless been reported. Transplacental transmission of Hendra virus (HeV) was shown in the fruit bat *Pteropus poliocephalus* [61]. Horizontal transmission is far more documented. Theoretical modeling of disease expansion has assumed large and well-mixed host populations. However, many wildlife systems have small groups with limited contacts among them. The distribution of seropositive bats against European Bat Lyssavirus type 1 (EBLV-1) is not random in bat colonies and follows a gregarious pattern, indicating a non-random transmission of viruses inside the colony. Most of gregarious species of bats have a metapopulation structure (consisting of periodically interacting, spatially discrete subpopulations) with variations in their subpopulations. The total number of individuals in the various subpopulations must be sufficient to maintain virus

122 Bats

**Figure 4.** Colony of *Miniopterus schreibersii* with individuals tightly close to each other.

The main element for the emergence of an infectious disease is the contact. With no contact, there is no possibility for a virus to cross the species barrier. In the case of bat-borne diseases, a direct or indirect contact must occur for the disease to emerge and spread. Synanthropic bats are of course the first ones to be considered as a source of emerging viruses. However, they are far from being the only ones at risk for transmission to humans. It is not only the natural synanthropic behavior that matters but instead the whole complex of biology, ecology, behavior, landscape evolution, and anthropization.

The first interaction considered for transmission of bat-borne viruses to humans is hunting and consumption of bush meat [64]. This is a traditional interaction in which humans are potentially going towards bats and thus viruses. However, there is no documentation of direct origin of virus disease outbreak coming from bat hunting, butchering, and consumption. Bush meat has been for instance regularly considered for the emergence of Ebola [65]. However, there is no evidence of direct contact with bats and bats were not the primary bush meat. Bats might just be a reservoir involved in a sylvatic cycle involving other animals being the actual target of bush hunting. In places where bats are hunted and consumed such as Southeast Asia, there is no report of direct emergence of viral diseases coming from consumption or hunting. A more likely potential process of transfer of viruses from bats to humans might be the attractiveness of degraded environment for bats [41]. Indeed, a highest diversity of bat-borne viruses was demonstrated, as a consequence of a higher diversity of bats, in anthropized, degraded environments. Deforestation and anthropization, instead of leading to the elimination of bats as one would instinctively expect, generate conversely a higher diversity. This might be explained by the complexity of the anthropized environments, which offer opportunities to different groups of ubiquity bat species, whereas natural environments might be more selective and suited for species with stricter ecological requirements. Anthropized environment displaying a higher biodiversity, the risk of virus transmission is therefore increased [41]. The impact of land use change on the emergence of diseases has been modeled to two main processes: (1) the perturbation hypothesis in which "land use change perturbs disease dynamics in multihost disease systems by disrupting the cross-species transmission rate" and (2) the pathogen pool hypothesis in which "land use change allows exposure of novel hosts to a rich pool of pathogen diversity, influencing the cross-species transmission rate" [66]. However, the same authors stated that these hypotheses tend to be vague or case specific with lack of theoretical foundation. This makes sense since the emergence of an infectious disease is an accidental process or in other words a very low probability event resulting from the sum of low probability independent events. According to this accidental process, an emergence cannot be predicted and will always appear as case specific. In the case of bats, numerous viruses have been found in bats but no direct transmission to humans has been formerly described. Emergence of bat-borne viruses is therefore most likely the consequence of the accidental association of a chain of events favored by structural elements from the human society. Although traced as a bat-borne virus, the coronavirus responsible for SARS seems to have been initially transmitted by civet meat to humans [31]. The outbreak itself was most likely triggered by human-to-human transmission through aerosols. The epidemic of SARS in 2003 was limited to hotels, high population density areas, and hospitals. No direct contact with bats was involved in the outbreak. Similarly, the MERS epidemic in the Arabic Peninsula was attributed to a coronavirus probably initially present in bats but transmitted to humans by dromedaries [34]. MERS was also involved, like SARS previously, in major nosocomial outbreaks [67]. In this case, also the trigger for the epidemic was not a direct contact with bats but the human society organization, close proximity with domestic animals, and nosocomial transmission.

and domestic animals. Another recent example is the first report of the presence of human and chicken blood in the diet of *Diphylla ecaudata* vampire bats living in the highly anthropized Caatinga dry forests of northeastern Brazil [68]. This attractive effect of anthropized environments on bats and the consequent promiscuity of bats, domestic animals, and humans are most likely to increase the risk of direct transmission of viruses and to the probability to trig-

Bats, Bat-Borne Viruses, and Environmental Changes http://dx.doi.org/10.5772/intechopen.74377 125

Bats have long rendered great services to mankind by acting positively on its environment and without living in a too close vicinity of human populations. However, by increasing the surface of cultivated areas and through the rapid growth of cities in the recent decades, men have drastically modified ecosystems which had remained in equilibrium for millennia. This evolution of ecosystems is even faster in Asia than in the rest of the world. Southeast Asia (SEA) is the region in the world that suffered the largest deforestation with a loss of 30% of forest surface over the last 40 years. In Thailand, agricultural lands represented 23% in 1960 and 40% since 1985 [69]. Similar trends were observed in other Southeast Asian countries [69]. In Cambodia, agricultural surfaces doubled from 15% in the 1980s to 30% in 2000. A similar trend was observed in Vietnam with an increase from 20% in 1990 to 35% today. In Indonesia, the growth was from 21% in the 1980s to 31.5% today. Deforestation is today linked to increased agricultural surfaces and to poorly managed urban growth. Owing to evolving land use, bat populations are setting in area closer to human dwellings [70]. Anthropized rural environments are characterized by a wide diversity of landscapes comprising houses, barns, fields, orchards, and woods of differing density. Human dwellings are also established close to water which along with the presence of animals is favorable for insects and insectivorous bats. Unlike natural environment which are highly selective, these altered landscapes are acceptable by a wide range of bat species, usually not encountered together, which establish close to human dwellings. This results in a higher density of bat-borne CoVs in the close vicinity of human dwellings [70–72], and thus a higher risk of human infection through direct contact or contamination by urine or feces. An aggravating factor is that the human population growth is higher in suburban and rural areas generating thus a higher pressure on land use, agricultural land, and deforestation with the most common activities being farming, logging, and hunting. The recent acceleration of deforestation in Southeast Asia and all predictions based on demographic burden on land use clearly indicate that the risk of contact and of transmission of new microorganisms which could turn pathogenic for humans will increase. It is thus just a matter of time, chance to encounter appropriated targets (human or animal in close contact with humans) and viral mutations to adapt to new hosts. Similar trends of deforestation are occurring in South America, but landscape organization is different, and the human population density is far lower than in SEA making thus the risk perhaps lower. If the exact time and nature of the emergence cannot be predicted, the increased probability of encounter and occurrence of emergence-leading chain of events yielded by anthropized

**7. Deforestation trends and increased risk of emergence**

ger the accidental process of emergence.

environment must be considered seriously.

The main risk for emergence of bat-borne diseases is directly linked to the development of anthropized environment and reduction of natural environments. It is often understood that deforestation and anthropization will lead to the disappearance of species. This is not always true and anthropized environments can provide an acceptable habitat for a large range of bat species, generating thus a higher diversity of bats and in turn of bat-borne viruses next to human dwellings. Anthropization generates a highly diverse environment in the vicinity of human, characterized by differing forest densities. Bats of differing ecology can find in anthropized environments niches compatible with their roosting and hunting needs. Natural environments are highly selective and compatible only with adapted species over a large surface, usually away from human settlements. In the exact contrary, anthropized environments provide a mosaic of ecosystems, very close to each other, each one corresponding to the needs of a given group of bat host. Insectivorous bats will find large populations of insects due to the presence of water, animals, and humans. Furthermore, house lights attract large number of insects at night. Houses and barns offer shelter for cave-dwelling bats while orchard and field can attract frugivorous bats. This environment is favorable to the occurrence of key parameters identified for virus transmission in large colonies of cave bats, i.e. shared roosting areas, close contact of different species, and regular introduction of infected individuals [45, 58]. However, in this specific environment, there is an additional aspect, the proximity of humans and domestic animals. Another recent example is the first report of the presence of human and chicken blood in the diet of *Diphylla ecaudata* vampire bats living in the highly anthropized Caatinga dry forests of northeastern Brazil [68]. This attractive effect of anthropized environments on bats and the consequent promiscuity of bats, domestic animals, and humans are most likely to increase the risk of direct transmission of viruses and to the probability to trigger the accidental process of emergence.
