Zoonotic spillovers: How climate change, habitat destruction, and bushmeat trade might amplify bat-driven viral disease risks

Bats can be the reservoir host of different pathogens, particularly some viruses including various species of the genus Lyssavirus, Influenzavirus A, Henipavirus (e.g. Hendra virus, Nipah virus), Flavivirus (e.g. Japanese Encephalitis Virus, St Louis Encephalitis Virus, West Nile virus, Dengue virus), Alphavirus (e.g. Venezuelan equine encephalitis virus, Chikungunya, Sindbis virus), Rhabdovirus (e.g. Australian bat lyssavirus), Coronaviruses (e.g. SARS-CoV, SARS-CoV-2, MERS-CoV), Filoviruses (e.g. Marburg virus), and Sosuga virus (Amman et al. 2014; Mackenzie et al. 2016; Liu et al. 2024). Bats have been identified to play an important role in the evolution of coronaviruses (CoV) and are known to host at least 30 different CoVs (Platto et al. 2021). According to the WHO (2022) guidelines, and Weinberg and Yovel (2022), bat-borne diseases such as Ebola, Hendra virus infection, Influenza, Marburg disease, MERS-CoV (Middle East respiratory syndrome coronavirus), Nipah virus infection, Coronavirus disease 2019 (COVID-19), and SARS (severe acute respiratory syndrome) have the potential for future epidemics or pandemics.

Interestingly, possible zoonotic transmission of these outbreaks, mostly as epidemics or pandemics, is suspected through different wildlife reservoirs, bats being one of them (Tabish and Nabil 2022). The majority of these diseases are driven by human activities such as habitat fragmentation, agricultural development, land use, and uncontrolled urbanization, which influence the transmission of infectious diseases from animals to humans (Olivero et al. 2020; Platto et al. 2020) (Fig. 1). Apart from this, hunting, wet markets, and the consumption of bat meat play a major role in transmitting bat-borne diseases (Epstein and Field 2015; Platto et al. 2020) (Fig. 1). The main reason for cross-species disease transmission stems from new and unintended interactions between various species (Galindo-González 2024). Valitutto et al. (2020) discovered three new alphacoronaviruses, three novel betacoronaviruses, and one previously identified alphacoronavirus in bats for the first time. It is highlighted that continuous changes in land use are a major contributor to the increase in zoonotic diseases, as they result in more frequent human-wildlife interactions, thus elevating the risk of zoonoses (Galindo-González 2022). Furthermore, Ye et al. (2020) investigate how interactions between CoVs and their animal hosts could offer valuable insights into CoV pathogenesis in humans. Researchers analyze various HCoVs from the perspectives of virus evolution and genome recombination, emphasizing the need to understand the conditions that facilitate successful host transitions and the influence of viral evolution on the severity of diseases.

This study was undertaken with the hypothesis that bats have immune systems similar to other mammals and bat-human interaction has not increased. The following questions were considered during the study: If the bat’s immune system differs from other mammals, does it help to adapt as a carrier of microorganisms? If the bat-human interactions have increased, what are the reasons for it?

The three most commonly used science-based databases, Google Scholar, ScienceDirect, and PubMed were used to search pertinent literature using the terms or combination of terms like “adaptation; bats; bush meat; climate change; conservation; disease reservoirs; emerging diseases; evolution; habitat destruction; immunity; interactions; pathogens; viruses; and zoonoses”. The authors rigorously filtered the original articles from the databases, websites, and organizations published till March 2024. Based on the same title, the duplicate results were quickly removed.

The relevant papers were later selected by reading the title, abstract, and keywords. For the methodical synthesis of the current study, all pertinent articles’ full texts were accessed after an initial screening. Inclusion criteria: articles covering the antiviral, host defense, and immune properties of bats; the ability of the immune system of the bats to suppress the virulence response of pathogens; anthropogenic factors responsible for increased human-bat interactions; and probable steps that can be taken to avoid unwanted disease outbreaks that may originate when an increase in human-bats interaction occurs—exclusion criteria: abstracts from seminars or conferences, viewpoints, opinions, letters, and encyclopedias. All the selected articles were further screened independently by the two authors and were discussed thoroughly for the inclusion of the relevant pieces of information. The reporting of this review is based on the directions of the systematic reviews (PRISMA) guidelines (Haddaway et al. 2022). In Fig. 2, the screening procedure is schematically illustrated. Many mammals, like rodents, pangolins, primates, bats, and pigs, can transmit zoonotic diseases to humans. However, bats are the only mammals among them which is capable of flight, found in a large area of the globe, and have vital roles in the ecosystem, making them one of the most important mammals capable of acting as a reservoir for microbes. Bats exhibit several critical characteristics that facilitate the accumulation of pathogenic organisms: (1) They are highly social animals, often forming colonies that can consist of hundreds of thousands or even millions of individuals; (2) they have a relatively long lifespan, typically ranging from 15 to 20 years or more; (3) they possess the ability to fly, with some species exhibiting migratory behavior; (4) they have a highly developed immune system (Li et al. 2005; Calisher et al. 2006; Han et al. 2015). Thus, the study was focused first on finding the specific characteristics of the bat’s behavior, anatomical adaptations, and immune system adaptations that might help suppress the effect of the micro-organisms’ virulence in their body. This was followed by searching for the anthropogenic factors that increase the chances of frequent human-bat contact and might increase the probability of disease outbreaks. To concisely present the information in an understandable and simpler form, some examples included in this study have been explained through diagrammatic and data representations of the Nipah and rabies virus epidemiology.

Many wild animals have the natural tendency to harbor different types of pathogens, bats are just one among them. In population, bats are the second-most abundant group of mammals after rodents. About 1462 living bats comprise approximately 22% of all known living mammal species (Burgin et al. 2018; Simmons and Cirranello 2022). The diversity of bat species (species richness) can be favorable for the emergence of new viruses that infect humans and other domestic and wild mammals (Cohn 2020; Mollentze and Streicker 2020). Compared to other mammals, bat’s unique physiological and life-history traits, such as long life span (Wilkinson and South 2002), flight ability and echolocation (Norberg and Rayner 1987), hibernation, geographical distribution, and daily torpor could influence the noticeable high viral richness for bats (Calisher et al. 2006). These factors may underlie or contribute to the immune mechanisms that help bats mount their hardy innate immune response against pathogens.

Some bat species also undergo hibernation. For such bats, emerging from hibernation is a difficult experience (Lee and McCracken 2002). Gamma herpes viruses are latently present in many big brown bats (Subudhi et al. 2018). According to Gerow et al. (2019), when large brown bats emerge from hibernation, the virus reactivates from latency, which results in the virus being found in the blood. Low levels of antiviral antibodies were also linked to this reactivation. However, after some time of the bats’ hibernation, the virus again enters latency due to rising antibody levels. Eventually, antiviral immunity increases by reducing viral DNA in the blood cells of non-hibernating bats (Gerow et al. 2019).

The sudden resurgence of some specific pathogens of bat origin, like the Nipah virus infection, is suspected to be triggered by a combination of factors such as reduced antibody levels and increased stress levels due to habitat destruction (Sohayati et al. 2011). Plowright et al. (2016) introduced a hypothesis stating that viruses infect vulnerable, naïve bats, resulting in acute illness. This then develops into a latent or chronic infection. After that, the virus periodically reactivates in response to various environmental and physiological cues. This hypothesis is known as the Susceptible–Infectious–Latent–Infectious (SILI) hypothesis (Plowright et al. 2016). The immune system of bats is unique and viral infection is likely to occur in many bats (Fig. 3).

The antiviral and immune defense response in bats

Bats are an ancient species, dating back 64 million years. The long evolutionary history has contributed to various viruses co-evolving with bats to become their natural reservoir (Teeling et al. 2005). When challenged with the virus, Jamaican fruit bats (Artibeus jamaicensis) show no or minimal signs of disease, even when high viral loads are detected in tissues (Munster et al. 2016). Interferons (IFNs) are cytokines that induce an antiviral state in host cells and are especially responsible for resisting viral infection. Bats exhibit a distinctive IFN, which may illustrate their efficiency in coexisting with pathogens (Ahn et al. 2016). Generally, mammals carry a large IFN locus comprising a family of IFN-α genes expressing themselves only during a viral infection. In contrast, bats have only three IFN-α genes continuously and constitutively expressed (Ahn et al. 2016). In fact, except for pigs, no other mammal has high expression levels of the IFN-ω subfamily (Schountz et al. 2017; Jennings and Sang 2019). In mice, IFN-ω is lacking. When compared with other mammals, IFNω and IFNδ genes appear expanded in the black flying fox (Baker and Zhou 2015). According to the hypothesis of Pavlovich et al. (2020), the IFN-ω subfamily’s expansion might help to create a more adaptable antiviral response that would benefit bats by preventing excessive pathology. Dysregulation of the IFN response has already been involved in autoimmune diseases and the pathogenesis of various bat-borne viruses, including Ebola virus, SARS-CoV (Liu et al. 2017), and SARS-CoV-2 (Huang et al. 2020). Not all bats constitute IFN all the time (Weinberg and Yovel 2022). Conceivably, bats can manage a distinctive balance between the levels of the two key type I IFNs, assisting in their antiviral abilities (Clayton and Munir 2020). In bats, this may be managed by IRFs (IFN regulatory factors) as differential expression patterns of IRF7 (Zhou et al. 2014) and IRF3-mediated enhanced antiviral responses (Banerjee et al. 2020). This confined induction of type I IFNs would reduce the production of inflammatory cytokines (Hölzer et al. 2019). The kinetics of the IFN response in bats is also different from that of other mammals, with a rapid decline phase for some bat ISGs (Interferon-stimulated genes) (La Cruz-Rivera et al. 2018). Further, various antiviral genes, for example, RNase-L (2–5 A-dependent endoribonuclease) genes, are IFN-inducible in bats (La Cruz-Rivera et al. 2018) but not in other mammals (Hölzer et al. 2019). Additionally, when bats are stimulated by virus infection, they maintain a high basal rate of autophagy that acts as both an anti-viral and pro-survival mechanism (Laing et al. 2019). Brook and Dobson (2015) suggested that bats evolved a secondary anti-viral role for the apoptotic removal of damaged mitochondrial DNA, resulting from increased oxidative stress during flight. Simultaneously, these bat-specific changes in baseline expression, dynamics, functions, or induction of antiviral genes in IFN signaling may help bats effectively control the abundant viruses they host (Irving et al. 2021).

In addition to the innate immune responses, some bats express very high levels of heat-shock proteins (HSPs), which enable bat cells to survive high temperatures and high oxidative stress in vitro (Phillips et al. 2017). By tolerating some viral mutations and modulating viral proteins, HSPs contribute to the rapid acceleration of viral evolution (Phillips et al. 2017). It also acts as a viral receptor (Reyes-del Valle et al. 2005), regulates or blocks apoptosis (Beere et al. 2000), inflammation (Srivastava 2002), and affects aging (Singh et al. 2006). A recent study has demonstrated that bats express ABCB1 (ATP binding cassette subfamily B member 1 gene) comparatively more than humans (Koh et al. 2019). The broad expression of the ABCB1 gene uniquely promotes resistance to DNA damage induced by the chemotherapeutic drugs doxorubicin and etoposide, providing resistance to genotoxic compounds, regulating cellular homeostasis, and probably lowering the occurrence of cancer (Koh et al. 2019). Another feature is their close association with viruses (Barton et al. 2007). The pool of viruses present in the guts of bats can help the microbiome boost immunity (Kapp et al. 2010). This has also led to the survival of diverse pools of CoV quasi-species in bat populations (Seronello et al. 2011).

Unique immune properties and suppression of strong pathological effects of virus-induced inflammation

Although bats are well-equipped to control viral infection, they also have mechanisms to reduce the induction of inflammatory genes (Subudhi et al. 2019). Excessive inflammation can be harmful and is associated with unwanted pathological changes in other species of vertebrates, such as humans (Channappanavar and Perlman 2017). Bats have evolved mechanisms for controlling excessive inflammation. Studies on cell culture have revealed that the promoter region of tumor necrosis factor-alpha (TNFα), a crucial inflammatory cytokine, contains a binding site for the inhibitor molecule (cRel) in the cells of many species of bats. In Eptesicus fuscus (Big brown bat) cells, a synthetic double-stranded viral RNA (dsRNA), poly I: C (Polyinosinic: polycytidylic acid), stimulated with cRel actively suppressed TNFα expression (Banerjee et al. 2017). Genome analysis of David’s myotis and black flying foxes has also exhibited the presence of positive selection pressure on the cRel gene (Zhang et al. 2013). This indicates that many bats can maintain a balanced response to viral infection by suppressing the expression of TNFα (Subudhi et al. 2019).

STING or stimulator of interferon genes, the most adapted protein, senses damaged DNA or dsRNA from viruses and enhances an interferon response (Xie et al. 2018). Several bat species showed immune tolerance by reducing STING-dependent type I IFN activation. This adaptation has been caused by replacing the functionally important and extremely conserved serine residue at position 358 (S358) (Xie et al. 2018). The replacement of S358 by other amino acids in bat STING dampened but did not completely reduce the function of STING (Mandl et al. 2018). A weakened but not completely lost function of STING may have profound implications for bats in maintaining a balanced state of “effective response” but not “over-response” against viruses (Xie et al. 2018). The PHYIN (Pyrin and HIN domain) genes, responsible for the formation of the inflammasome and microbial DNA sensing, are not present in bats (Ahn et al. 2016). The complete loss of PYHIN in bats suggests a vital adaptation for flight (Dempsey and Bowie 2015). Therefore, its removal may enable some bats to limit excessive inflammation activation and regulate the type I IFN response to normally recognized DNA damage by PYHIN proteins. There is the possibility that the increased exposure of bats to many zoonotic RNA and DNA viruses compared to other mammals (that do not cover large distances), may have been an evolutionary driver of PYHIN loss or, conversely, that PYHIN loss may have allowed for this bat-viral co-evolution (Ahn et al. 2016). It is hypothesized that the reason for bat longevity is the loss of the PYHIN gene (Clayton and Munir 2020). These regulations suggest that bats may experience some reduction in inflammation at the time of viral infection (Subudhi et al. 2019). For the mitigation of the deleterious effects of flight, mechanisms to regulate inflammation may have evolved. Cytosolic DNA is abundantly produced in bat cells during flight, which may create a strong natural selection pressure to reduce the activation of bat DNA sensors (Subudhi et al. 2019). Similarly, a study discovered a suppressed NLRP3 (NLR-family pyrin domain-containing 3) inflammasome activity in the immune cells of MERS-CoV-infected black flying fox, which can recognize various cellular stresses and pathogen invasions and results in lower production of the proinflammatory cytokine IL-1β (Interleukin-1β) (Ahn et al. 2019). Ahn et al. (2019) showed an overall dampened activation of NLRP3 in bat immune cells compared to humans in their study (Fig. 4). Consequently, reducing immunopathology during viral infections and diminished STING and NLRP3 inflammasome activity in black flying foxes potentially evolved to decrease the pathological consequences of oxidative DNA damage during flight (Baid et al. 2024). Flights increase the metabolic rate and result in the formation of higher levels of oxygen-free radicals (Maina 2000). This makes bats more susceptible to producing damaged DNA (Cadet and Wagner 2013). Since mounting an immune response is energetically costly (Sheldon and Verhulst 1996) and harmful, bats have likely evolved mechanisms to suppress the activation of the immune system caused by damaged DNA generated during flight, thereby reducing the overall inflammation (Jebb et al. 2018). During hibernation, bats conserve energy by lowering their body temperature and metabolic rate, which can suppress the immune system and delay viral clearance (George et al. 2011).

Global warming and climate change

Climate change may contribute to the risk of pathogen spillover. Environmental changes can alter species ranges and densities, leading to novel interactions between species and increasing the risk of zoonotic introduction (Carlson et al. 2022; Guth et al. 2020; Galindo-González 2024). The El Niño-Southern Oscillation (ENSO) is an important source of annual global climate variability, characterized by three phases: El Niño (warming), La Niña (cooling), and the Neutral phase (Hanley et al. 2003). ENSO is one of the most important climate events due to the global atmospheric circulation and its ability to change global temperature and precipitation patterns (Hanley et al. 2003). It directly supports outbreaks or the spread of various public health concerns (Anyamba et al. 2019). According to the WHO (2023a), El Niño occurrences have increased in South and Southeast Asia due to less rainfall. ENSO-related drought conditions and anthropogenic forest fires may have resulted in fruit bat infection with the Nipah virus while they were migrating from Sumatra to Malaysia in mid-1997 in search of food (Chua et al. 2002). The populations of black flying foxes in Australia, a main reservoir of the Hendra virus, have shifted 100 km south over the past 100 years due to climate change. This shifting range likely contributed to the spread of the Hendra virus in southern horse populations, and these horses subsequently infected humans (Yuen et al. 2021). Latinne and Morand (2022) showed in their experiment that the cool phase or La Niña event directly influenced the five emerging outbreaks including, the Nipah virus in Malaysia and India, the Melaka virus in Malaysia, SADS-CoV (Swine acute diarrhea syndrome coronavirus) in China, and MERS-CoV in Saudi Arabia, while four of them, i.e., Hendra virus in Australia, SARS-CoV-1 and − 2 in China, Menangle virus in Australia occurred at the time of warm phase or El Niño event (Table 1). The other three bat-related events, including the Australian bat lyssavirus in Australia, the Nipah virus in the Philippines, and the Kampur virus in Malaysia, occurred during the neutral phase (Table 1). Fruit bats could respond to severe weather events and climate change by shifting their distribution to more favorable areas since they are highly proactive and often travel great distances in search of resources (Roberts et al. 2012). Bats can colonize previously uninhabited areas (Boardman et al. 2020). It is predicted that in Australia, fruit bats may migrate as far south as Tasmania in the next 10 to 20 years due to the climate crisis, possibly leading to human-wildlife conflict (Diengdoh et al. 2022).

In the Americas, bat-borne rabies virus spillover from wildlife to domesticated species is substantial (Pan American Health Organization 2024). In Latin America, Desmodus rotundus, the common vampire bat, one of three sanguivorous species in the family Phyllostomidae, is one of the wildlife species responsible for the transmission of the rabies virus to other domestic animals and humans (Meske et al. 2021). Being a homeothermic species, D. rotundus exhibits a varied response to extreme temperatures in laboratory settings (Lyman and Wimsatt 1966). Canine rabies has been effectively controlled in Brazil, yet bovine rabies is still endemic because of the presence of vampire bats. This zoonotic viral disease causes an annual loss of 17 million US dollars (Ferreira et al. 2012). Climate conditions can affect bat population dynamics and rabies cases, especially in domestic animals and humans. Several studies have shown that factors such as temperature, climate, rainfall, and the ENSO affect the prevalence of rabies in specific areas, seasonally and throughout the years (Santos et al. 2019). Under climate change conditions, bat species may expand their range in response to rising temperatures (Ancillotto et al. 2016), and the mechanisms by which bat range shifts in response to climate change may include dependence on water, roost quality, bat physiology, and phenology (Cappelli et al. 2021). Modeling future conditions for the sanguivorous bats along the US border with Mexico, the authors showed areas in South Texas could become suitable for this species’ habitation by 2070 (Hayes and Piaggio 2018).

Climate change is a great concern for bat survival. In addition to spreading diseases among humans, climate change also affects bats themselves. Grey long-eared bats are among the UK’s rarest mammals, numbering fewer than 1000, and have migrated to the UK from Spain and Portugal as they struggle in the increasingly hot climates of these two countries. The effects of heat waves have been quite dramatic in Australia, resulting in the death of flying foxes yearly (Groc 2021). As climate change progresses and these events become more common, bat populations may face further reduction. Numerous bats dying in heat waves can lead to ecological imbalances and the spread of zoonotic diseases (Nitnaware 2023). Large numbers of sick or dead bats lying on the ground can increase the risk of infection due to increased human-animal-bat interactions, especially if members of the public try to rescue ill bats or remove the remains of dead bats. Bat mass mortality events threaten public health because of the increased risk of disease transmission from bats to humans (Paterson et al. 2014).

Damage to the natural habitat

Destruction of natural habitats due to natural disasters and changes in human social structures can lead to higher disease outbreaks in wildlife, posing a significant risk to humans through zoonotic spillover (Faust et al. 2018). In tropical Asia, 65% of the main forest habitat has been lost, with specifically high rates of destruction recorded for Bangladesh (96%), Sri Lanka (86%), India (78%), and Vietnam (76%) (Primack and Morrison 2013). Loss of natural habitats of bats may lead to outbreaks of bat-associated viral infections in humans and animals (Chattu et al. 2018). As humans encroach on the environment, many bats are dislocated from natural foraging grounds, which can reduce their numbers. Bats, in turn, adjust themselves in human-made rural or urban constructions. However, as the bats adapt to human habitation, it becomes more likely that bats will have increased chances of human contact. Pteropus sp., the fruit bat, has been identified as a natural host of the Nipah virus. Sixty-five Pteropus species are distributed from Madagascar island of Africa through the Indian subcontinent to Southeast Asia and Australia and as far east as the Cook Islands. Some Pteropus species are the largest of all bats, exhibiting a weight of 1.2 kg and a wingspan of up to 1.7 m. (Neuweiler 2000). Since bats are known to be migratory or travel long distances (e.g.>200 km during migration, Krauel and McCracken 2013), they have the potential to transfer zoonotic viruses between countries through their movements (Breed et al. 2010). In Australia, all bat-related viruses, such as Hendra, Menangle, and Australian bat lyssavirus that have emerged are hypothesized to be linked to habitat loss caused by deforestation and agricultural reinforcement (Jones et al. 2013). Nipah virus (NiV) outbreaks will likely continue in affected countries due to the large distribution of native fruit bats in South and Southeast Asia. Flying foxes become stressed and starved as their habitat is uprooted by human activity and their immune system weakens. Because of the weakened immune system, their viral load increases, and they shed more viruses in their urine and saliva (Halpin et al. 2000). Similar fluctuations in virus shedding may be associated with physiological states of stress or seasonality. Among all other South Asian countries, Bangladesh is considered an important global hotspot for zoonotic spillover to humans (Allen et al. 2017). The government of Bangladesh has selected six diseases through a one-health zoonotic disease priority workshop, including three bat-borne diseases, which were Nipah virus, rabies, and zoonotic influenza (CDC 2017). Bangladesh alone contributes about 42% of the global Nipah disease burden and recorded 325 human cases from 2001 to 2022, with a case fatality rate of 71% (Pillai et al. 2020). A total of six outbreaks of NiV have been reported in India. The disease first broke out in the West Bengal state bordering Bangladesh in 2001 and 2007, during which seventy-one cases were reported, with 50 deaths between the outbreaks. Four other outbreaks have occurred in the country’s southern district of Kerala in recent years. The virus found in Kerala has been identified as the Indian genotype or I-genotype by the National Institute of Virology, Pune, identified to be identical to the NiV strain found in Bangladesh (World Health Organization 2023b). According to the World Health Organization (2023b), the Kerala outbreak strain originated in Bangladesh in 2001. It often causes small outbreaks with high mortality. To reach Kerala, the virus must have spread undetected from Bangladesh or the neighboring Indian state of West Bengal over more than 2,000 km. Many Indian states and some countries like Sri Lanka, southern China, Nepal, Bhutan, Myanmar, Thailand, and Laos are within the same range of distance from Bangladesh and have significant populations of fruit bats (Jayanth 2023). In Malaysia and Singapore, the infection was initially detected among workers involved in pig slaughter in 1998–1999 (Fig. 5). The virus spread in Malaysia due to the mismanagement of large piggeries and unplanned pulpwood deforestation, the natural habitat of NiV-carrying bats (Halder and Chakravarty 2006). Also, Malaysia lost 14.4% of its forest cover from 2000 to 2012, at the rate of one football pitch every 1.5 min; it lost 4.5 million hectares of its dense forest (Rana and Singh 2015) (Fig. 5). Similarly, the mode of transmission was observed during the outbreak on the island of Mindanao, Philippines, in persons involved in the slaughter of infected horses and consumption of infected meat (Paton et al. 1999). First in Bangladesh and then in India, NiV spillover occurred during the consumption of raw or fermented palm fruit juice contaminated with saliva, urine, and feces of bats (Hughes et al. 2009). Date palm juice consumption is popular in several Southeast Asian countries, including India, Bangladesh, Indonesia, Malaysia, Thailand, and the Philippines. Due to urbanization and increasing habitat destruction, bats progressively find homes in human habitats, leading to human-bat disputes (Hassan et al. 2020). Pteropus bats roost on trees in hundreds at the time of day and forage for fruits, pollen, and nectar at night. The roosting trees are usually located on the side of water bodies (Dey et al. 2013). Mature mangrove forests could offer distinctive roosting opportunities for bats because they support a high density of habitat trees, a stable microclimate, and a possibly low abundance of competitors and predators (McConville et al. 2013). About 46% of the world’s mangroves are present in South Asia, Southeast Asia, and the Asia-Pacific sub-region (Giri et al. 2011). However, the deforestation rate in Indonesia due to land conversion for shrimp farming and settlement ranges from 182,091 to 2,000,000 hectares annually (Arifanti et al. 2021). Similar trends are noticed in Southeast Asian countries such as Myanmar, Vietnam, and Thailand (Luo and Chui 2022). The Philippines lost 10.5% of mangroves between 1990 and 2010 (Long et al. 2014), while Cambodia experienced a 42% reduction from 1989 to 2017 (Veettil and Quang 2019). Although there has been no evidence of NiV infection in Cambodia, Cappelle et al. (2020) confirmed that NiV is prevalent in Cambodian fruit bats. Deforestation is not only caused by shrimp farming but also by the extension of palm tree plantations on forest lands, especially in Indonesia and Malaysia (Richards and Friess 2016). The Sundarbans, the world’s largest mangrove ecosystem in the sub-region, covers about 1,000,000 hectares of area at the India-Bangladesh interface (Quader et al. 2017). The most significant loss of mangroves has occurred in Bangladesh, where the initial loss rate was 80% from 2010 to 2016 (Goldberg et al. 2020). Across the sub-region, mangrove loss is caused by land-cover conversion, over-harvesting, and pollution (Giri et al. 2008). Chattu et al. (2018) mention that in Bangladesh urbanization and deforestation have contributed to immense overlap between human and bat habitats in some areas. Even in India, a large part of the mangrove forest has been destroyed due to increased aquaculture. In India, about 40% of the mangrove habitat along the western coastline has been converted for aquaculture (Kathiresan 2022). Bat populations in many Indian states have serological evidence of exposure to NiV. Many places in South and Southeast Asia have NiV reservoirs which may cause disease outbreaks in different regions in the future (Jayanth 2023). An overview of the yearly distribution of Nipah cases in humans worldwide is shown in Table 2, along with the case fatality rates.

The common vampire bat (D. rotundus), a hematophagous bat, is one of the main sylvatic rabies reservoirs and source of human and livestock infection in Latin America (Bergner et al. 2020). Common vampire bats range throughout South America (except south of the Patagonia region) to northern Mexico (Bergner et al. 2020). Human activities have contributed to increasing the density and distribution of the common vampire bat through an abundant food supply (cattle ranching) and deforestation of large areas. The deforestation of large areas, which represents an increasing problem in many South American countries, promotes the dispersal of vampire bats in search of a new location to colonize and may favor the contact between humans, livestock, and bats (Gupta 2005; Botto Nuñez et al. 2020). It has been proposed that bats’ tolerance of fragmentation and habitat loss may be connected to their ability to cross open areas to reach other vegetation or forest fragments and use resources within the matrix (Schulze et al. 2000). Brazil is the fifth largest country by territorial expansion and has the largest cattle stock in Latin America (OECD/FAO 2019), with livestock production important for national and international trade. Deforestation has occurred in some biomes in Brazil, particularly in the Amazon, where extensive cattle ranching has increased pressure on large forests, significantly altering the landscape (Dos Santos et al. 2022). The abysmal lack of strategic planning for expanding areas earmarked for agriculture and livestock alters the landscape and exacerbates the risk of outbreaks of infectious diseases among animals and humans (Fig. 6). Though in recent times incidences of rabies in humans and animals have reduced, still rabies is a potential disease for the emergence of outbreaks because vampire bats have a great capacity to adapt to anthropogenic environmental changes (Gomes et al. 2010). Coupled with this, the ability of vampire bats to travel great distances, greater than 10 km, and use all types of forest to traverse large agricultural expansions (Medina et al. 2007) makes rabies a disease capable of crossing states and countries. Botto Nuñez et al. (2020) noted that the Uruguay-Brazil border is most likely the source of the rabies epidemics in cattle that began in 2007. During the last decade in Brazil, rabies has been transmitted to humans through bites by D. rotundus bats (52.60%), dogs (23.70%), non-human primates (10.50%), and felines (10.50%) (Ministry of Health 2024) and there have been an increasing number of reports of D. rotundus bites on humans, posing a potential threat to public health in this country (Benavides et al. 2020). D. rotundus is the main transmitter of rabies in livestock animals in Brazil (100.00%, n = 50 and 99.20%, n = 650) (Kobayashi et al. 2008; Pimentel et al. 2022). Cases of rabies in livestock animals are frequently reported, with cattle being the most affected among the livestock animals (Mello et al. 2019). Vampire bats probably prefer cattle because cattle populations are constantly present and exist in higher densities than native prey mammals (Becker et al. 2018). Furthermore, the incidence of this disease has recently been on the rise in equines in Brazil (Oliveira et al. 2022).

Consumption of bushmeat and the role of wet markets

Tanalgo et al. (2023) found that 19% (N = 254 spp.) of 1320 bats on the IUCN red list were hunted. Bat hunting is widespread, especially for large and colony-bound species, which are easy targets for hunting. In addition to habitat loss, hunting is a major threat to many bat species (Fritz et al. 2009). Bat hunting often involves various socioeconomic and cultural motivations, but food security is a major factor in rural areas (Oedin et al. 2021). In tropical regions of Africa and Asia, bats are hunted and consumed, especially fruit bats (Ghosh 2020). Between 2014 and 2016, about 28,616 people were infected, and 11,310 died in several West African countries during the Ebola virus outbreak, where bushmeat consumption was a transmission route (Wirsiy et al. 2021). Baudel et al. (2019) conducted a study of 135 people in southern Cameroon, where direct human contact with bats was found to be substantial, with 40% of respondents reporting consuming bats, 28% hunting them, 22% informed that children catch them, and 17% responded being previously bitten by bats. Hunting and consumption of bushmeat by humans carry considerable risk for cross-species disease transmission (Santos et al. 2019), particularly where bats are included. More recently, an outbreak of Sudan ebolavirus in Uganda infected 160 people between September 2022 and January 2023 and killed 77 people before it was brought under control (Okamoto et al. 2022). Uganda has several areas with high bat densities, some of which have experienced outbreaks of hemorrhagic fevers due to unknown pathogens that have been most probably transmitted by bats (MacNeil et al. 2010). A study identified that hunting and consuming bats was the top activity during an outbreak (Ninsiima et al. 2024). Respondents who hunted were ten times more likely (as a risk factor) than farmers to be exposed to bats (Vora et al. 2020). Bats are hunted for food in many parts of the world and can pose a risk to human health by spreading zoonotic pathogens from bats to humans (Vora et al. 2020). Bat hunters have domestic animals at home, where they slaughter and prepare bushmeat in front of them. Sometimes, they keep the bats alive and throw away the bat remains or feed them to pets, increasing the risk of disease transmission from bats to animals and humans. A human NiV outbreak occurred in Malaysia when bats infected pigs and the pigs infected humans (Nahar et al. 2020). Hunting, consuming, and trading bats put humans in direct contact with zoonotic pathogens that the animals may harbor, thus increasing the potential for spillover. Those involved in hunting, butchering, and consuming wildlife are at risk of infection by close contact, such as through mucosal and transcutaneous routes with live and dead animals or via contaminated sources, for example, fomites and feces (Cantlay et al. 2017). Lyssaviruses should be considered a greater infection risk for hunters because cases of fatal encephalitis from bat bites and scratches have occurred in Australia (ProMED-mail 2014). Openshaw et al. (2017) found that bat hunting occurred in 49% of the villages surveyed in Bangladesh and that bat hunting may increase the risk of NiV infection.

Live and wet markets are dense concentrations of large numbers of species that may never encounter each other in natural conditions and that may have never interacted in their evolutionary history because they do not share the same ecosystem (Lynteris 2016; Naguib et al. 2021; Galindo-González 2022). Various wild species are available in wholesale markets in Africa and Asia, either dead, frozen, or alive. In most cases, bats, rats, snakes, insects, sea urchins, turtles, sea cucumbers, civets, hedgehogs, and groundhogs are poached and sold illegally (Lynteris 2016; Zhang and Holmes 2020; Zheng 2020; Naguib et al. 2021). The study showed that bat-related diseases could spread through livestock markets (Naguib et al. 2021; Galindo-González 2022). For example, the Ebola virus in West and Central Africa, the Marburg virus in sub-Saharan Africa, and the Nipah virus in South and Southeast Asia can spread through live exotic animals or bush meat consumption (Marí Saéz et al. 2015; Judson and Munster 2023). Emerging infectious disease risks arise from interactions between humans, food products, live domestic animals for sale, and wild and scavenging animals (Naguib et al. 2021; Galindo-González 2024). Moreover, these animals interact with domestic species like pigs, rabbits, ducks, cats, chickens, dogs, etc., and humans, leading to cross-species transmission (Tian et al. 2022; Salinas-Ramos et al. 2021). Southeast Asia and China are global hotspots of emerging zoonotic diseases (Allen et al. 2017). In these regions, wildlife is generally sold in open markets, and such markets have been in the spotlight as a source of zoonotic viruses. For example, it is believed that China’s wet market in Wuhan played a crucial role in the initial spread of COVID-19 (Xiao et al. 2021). At that time, China immediately shut these markets over fears of coronavirus propagation (Xiao et al. 2021). Even Siamese Crocodiles, Indian Peafowls, Common Pheasants, raccoon dogs, Foxes, and Amur hedgehogs are used in the market as food and kept in cramped, dirty conditions like market cages. According to the World Economic Forum (Beech 2020), “it was not a wet market for China strictly, but a wildlife market”. The disease can spread easily through body fluids to handlers and customers. Indonesia’s wildlife markets are like a cafeteria for animal pathogens (Paddock and Sijabat 2020), Morcatty et al. (2022) reported that short-nosed fruit bats and large flying foxes are also sold in large quantities in ten out of fourteen markets.

The chances of the emergence of infectious disease increase in high-biodiversity areas experiencing changes in land use (Allen et al. 2017) and in degraded landscapes (Bloomfield et al. 2020). Well-implemented area-based management can reduce land-use change (Bruner et al. 2001). Unprotected areas with high biodiversity or important habitat features at risk of land use change must be identified and protected, particularly where bat habitats exist. To prevent range expansion into urban and semi-urban areas, natural bat habitats must be better protected to allow adequate space for bat populations, where the risk of spillover may increase through contact with humans and livestock (Schneeberger and Voigt 2016) (Fig. 6).

To avoid future epidemics of zoonotic diseases, governments must rigorously execute bans on the sale and trade of wildlife for food, and they must adhere to food safety and hygienic conditions ( https://www.bbc.com/news/world-australia-52391783 ). National policies to protect or control bat hunting are either absent or lack enforcement in many countries (Oedin et al. 2021 ). More measures may be needed to address illegal hunting (Geldmann et al. 2019 ). Regardless of the public’s negative perception of bats, they are important components of all terrestrial biological communities (Del Vaglio et al. 2011 ). They help control insects, harvest forest seeds or aid in seed dispersal, enhance soil fertility and nutrient distribution, recycle and pollinate plants that provide food for humans and other species, and act as predators of insects (Russo et al. 2018; Enríquez-Acevedo et al. 2020 ). In pest control, they provide at least $3.7 billion in services each year in North America alone (Boyles et al. 2011 ). Ramírez-Fráncel et al. ( 2022 ) identified 409 bat species that provide ecosystem services, 549 plant species are pollinated or dispersed by bats, and bats eat 752 insect species. Resolving the bat-human conflict requires rigorous approaches to underpin human behavior and develop effective interventions to promote behavioral change (Kingston 2016 ). Integrating local hunter/collector communities (e.g. vendors and customers) and Indigenous peoples into early warning systems for disease outbreaks that link to national and international public health reporting systems. Community engagement activities should co-design interventions and conduct them to strengthen the perceived fairness and legitimacy of new laws or standards. Public awareness should be created about the risks of contact with wildlife and the increased chances of transmission of diseases associated with wildlife hunting. The importance of the beneficial ecosystem services bats provide should also be highlighted in public awareness programs. Social acknowledgment campaigns can help influence public behavior for the benefit of biodiversity and society (Salazar et al. 2019 ). It should be noted that appropriate conservation measures can even reduce the risk of viral spread from bat populations to human populations (Schneeberger and Voigt 2016; Weber et al. 2023 ).

Through millions of years of evolution, the bat population on earth has adapted their immune system so that they do not suffer from the deadly outcomes of different microbes, especially viruses. However, they can still act as a carrier for several viral diseases. Bats have adjusted to various niches and habitats, and confrontation with humans is generally avoided. This has also limited the potential of outbreaks of deadly diseases from bats to humans. However, with global warming, changing climate, bat habitat destruction, and bushmeat consumption, the frequency of bat-human contact has increased by multiple folds. The anthropogenic factors have also influenced the change and shift of the bat population. This has further increased the chances of frequent bat-human contact. This increase in contact between bats and humans has also increased the chances of an outbreak and the consecutive spread of zoonotic diseases, which were suppressed in nature. Governments of the world and people, in general, should consider the necessary steps that can be taken to conserve the bat population in their natural habitats and to minimize frequent contact of humans with this vital fauna. If serious efforts are not implemented soon to prevent global warming, climate change, and bush meat consumption, it might be too late to control newer microbial outbreaks.