[This essay was featured as a ‘featured top pick’ on Medium’s Science page in February 2020 https://medium.com/@emswam/the-bewildering-world-of-bats-c8254acd6e8f ]

Chiropterophily. Source Credit: NWF https://www.nwf.org/Home/Magazines/National-Wildlife/2018/Oct-Nov/Gardening/Native-Bats

With bats, the ‘Umwelt’ is a good place to start. Introduced into ethology, in 1909, by the German Biologist, Jakob von Uexküll, it describes the sensory experience of the world that is unique to every species; animal perceptions of their environment that are vastly different from our own. Each species is imbued with its own distinctive sensory capabilities. They see, hear, taste and feel the world differently from humans. Consequently, their interpretation of the world and their engagement with it is also different. This sensory perception that is special and exclusive to each animal life-form is Umwelt.

Given our tendency to anthropomorphize the world and its creatures, such a word of distinction is both fitting and necessary. Implicit in the word – Umwelt – is the allusion to a level of consciousness that inserts itself above the subjective/ individual and under the umbrella of ‘species’ as a species consciousness.

This is a good place to start because bats differ from us in the two sensory systems that we use the most — vision and hearing. Common knowledge of bats is that they are nocturnal, they use sonar to hunt and navigate and are blind. While the first two are indisputable; the last is untrue. Bats do use ultrasound (high frequency sound that cannot be heard by the human ear) to communicate and for echolocation¹. That they are nocturnal flying mammals is equally well documented.

However, what is less appreciated is that bats, like birds and bees, have the capability of sight with a form of ultraviolet vision. This was first documented in nectar and insect eating bats that use ultraviolet markings on flowers as guides to zero in on their food source². There are many fruit species that have chiropterophillic flowers; bananas, mangoes and agave are some of them (‘Chiropteran’ — of or related to bats; from their ‘order’, chiroptera. Chiropterophillic — attracting bats).

                                                                    Nectar feeding bat. Source Credit: http://www.umsl.edu/~muchhalan/Bat_Flower_Pix.html

The bat experiences its Umwelt with ultraviolet vision and ultrasound. Both are at the extremes of the visual and auditory spectra and are starkly different from our own rather restricted sensory capabilities. The world as seen and heard by a bat has little, if any, similarity with our own.

A chiropteran curiosity 

Bats are one of the earth’s more populous creatures (they comprise twenty percent of the mammalian population). Although there isn’t an estimated population number; there are, at a minimum, 1300 documented species of bats³ with a geographic distribution that spans the globe. Within the Class Mammalia, they are distinguished by two characteristics: they are the only mammals with an expansive migrating potential due to the capacity of flight and, they have longevity with a peculiar absence of morbidity or natural biological aging until the very end of life. The average lifespan of a bat is twenty years; some few species are known to live up to and beyond thirty years and there is one that lives up to forty even.

That last feature — the peculiar absence of morbidity — has come under the research spotlight, in recent years, due to the rising incidence of zoonoses⁴ (human infectious diseases that are acquired by transmission from an animal source). Sixty percent of all such recently emerged infections are zoonoses and almost all have been traced to bats as the source.

Bats are the reservoir hosts of a number of viruses and yet, apart from the rabies and the tacaribe viruses, there is, as yet, no other known virus that is fatal to them. Bats do not fall prey to infectious disease from any of the viruses that live in them; — rhabdoviruses, hantaviruses, paramyxoviruses, flaviviruses, bunyaviruses, filoviruses and others. But when any of these viruses exit bats and enter another species (this transmission event is called ‘spillover’ or ‘jump’) they cause serious disease with high fatality rates. Beyond these viruses that are related to known disease, they house many others that are unlinked to documented disease.

                                            Source credit: https://doi.org/10.1016/j.coviro.2018.12.007 Science Direct

This chiropteran anomaly raises two obvious questions: 1) why are bats a natural reservoir of viruses and, 2) why do they not fall prey to disease despite the teeming presence of viruses in their body? Both questions have been the focus of intense study in recent years. Of course, the first might be logically answered by the second (they do not contract disease and therefore they become natural reservoirs) but the search for a biological explanation was elusive. Historically, bats have not been studied in detail unlike many other animals — that they are nocturnal and difficult to catch are a couple of reasons why — and our scientific knowledge is riddled with lacunae on the biology, ecology, phylogeny and ethology of these creatures. But that has changed. The old disinterest has been rapidly shed with the rising zoonotic challenge to public health systems across the world.

Batting away the bedeviling

Phylogenetic studies that probe the genetic relatedness of bats and viruses suggest a co-evolution is at play. Host-parasite (bat-virus) relationships are of many kinds; one of which is commensalism. Commensals are benign host microbes — the host neither benefits nor is harmed by them; the parasites, on the other hand, have the benefit of survival in a tolerant host environment. Such relationships are driven by mutual and reciprocal evolution with the host always two steps ahead in a move that ensures their combined survival.

The viral resistance of bats was initially ascribed to a potent antiviral defense. Contrary to popular misconception; bats (in a less traditional form of commensalism) mount a powerful antiviral immune response mediated by the antiviral, Interferon. To prevent being completely wiped out by the bat’s immune response, viruses have co-evolved by increasing the potency of their replication.

As a host response, bat antiviral defense is of a high grade and is always ahead of viral multiplicative power. In the normal course of events, such a potent antiviral defense should provoke an equally strong/ high-grade inflammatory response in the bat. The kind of extreme inflammation that this sort of defense provokes is itself capable of threatening survival. But, in bats, inflammation remains stoically unprovoked and this is the key to the riddle of chiropteran forbearance.

Inflammation is the body’s protective defense response that activates when the body is under assault of any kind; whether metabolic, mechanical or microbial. But it is protective only as long as it is in temporal balance. When the response is imbalanced, severe and exuberant or when it is low grade but over a long drawn out period of time, inflammation can become paradoxically harmful; even to the point of being fatal.

Bats providentially escape the consequences of inflammation due to the anomalous activation of an anti-inflammatory response that is coterminous with their antiviral defense. This is an innate physiological adaptation to cope with the metabolic stress of flight.

                         Source Credit: https://doi.org/10.3390/v11020192 Virises 2019 11(2), 192

Flying is an intensely high metabolic activity; a consequence of which is the production of a vast number of toxic by-products called, free radicals. The resulting oxidative stress provokes a severe and systemic inflammatory response called the cytokine storm which then leads to cellular damage and death. To be capable of flying; a mammalian system must necessarily have adapted to mitigate the near-fatal effects of these compounds. Bats achieved this by suppressing inflammation. They evolved an anti-inflammatory response that prevents the release of powerful mediators of inflammation — the cytokines. Therefore, unlike the expected defense to a viral infection which is — antiviral/ pro-inflammatory; bats have a unique antiviral/ anti-inflammatory response. They, simultaneously, fight off the virus and prevent the damaging effects of inflammation. Suppression of inflammation is also responsible for the longevity and absence of senescence in bats.

The primary explanation for chiropteran viral resistance has thus slowly shifted from ‘potent antiviral defense’ (mediated through Interferon) to a stronger role for ‘anti-inflammatory disease tolerance’ that is, in turn, mediated through a vast expansion and expression of anti-inflammatory gene families⁵.

The viral version of events

While all this is going on with bats; there is a lot happening with their viruses too. Bats are hardly the sole reservoirs of viruses. Viruses can pick and choose reservoir hosts from a wide range of other creatures that include birds, primates, clove footed mammals (camels, goats) and rodents. A study of 300 disease systems⁶ (a disease system comprises pathogen, reservoir, target and geography) reports that rodents are the most common mammalian reservoir hosts for zoonotic pathogens (an infectious agent that causes disease is called a pathogen), while bats and primates host viruses with the most epidemic potential. It also confirmed viruses as the commonest zoonotic pathogen and that bats were over-represented for viral pathogen systems with humans as targets.

If little is/was known about bats; a little more is known about their viruses. Of all microbes, — (infectious agents with the potential to cause disease are called microbes; when they actually cause disease they are called pathogens. Every pathogen is a microbe; every microbe need not become a pathogen) — viruses cross (jump) the species barrier with relative ease. In just the past decade; four viruses — Handra, Nipah, Menengle and Lyssa — have jumped from Pteropid bats alone (Pteropus is a genus) and caused severe & fatal disease in both animals and humans.

A common classification of viruses is based on the nucleic acid in their core — DNA viruses and RNA viruses. All the viruses that have jumped from bats are RNA single stranded viruses⁷. RNA viruses thrive in the new host better than DNA viruses. They have innately higher mutation rates and so, adapt better to new environments.

The extreme replication ability of chiropteran viruses, which co-evolved within bats, is a matter of indifference to the bat because it has a host-parasitic relationship akin to commensalism with them. But when such viruses jump from the bat to an intermediate host and from there to other end-targets; the result is disastrous. This ability to root and multiply, overwhelms unprepared immune systems of new hosts resulting in severe sickness and death.

Viruses cross the species barrier only upon contact. With bats; the opportunities for direct contact with humans are few and far between and transmission happens in two ways: 1. Direct — from direct contact with a bat either through a bite or through contact with its secretions. This is a relative rare route and was first documented in the rabies outbreak, of the early twentieth century, in cattle in Brazil where rabid bats became diurnal and were spotted biting cattle. A century later, another virus — a Henipavirus called Nipah — has been identified as the cause of outbreaks of human encephalitis in Malaysia, India and Bangladesh. In Malaysia, pigs are an intermediate host; but in South Asia, this virus transmits through direct contact. Not with the bat itself but with fruit-bat saliva and excretions in date palm sap. 2. Indirect — through an intermediate animal host which, in its turn, has contact with both bats and humans. Horses, pigs, civet cats, camels and gorillas have been implicated in Lassa fever, Nipah encephalitis, SARS, MERS and Ebola respectively.

A recent paper, published early this month in e-Life, tracks the impact of bat immunity on viral dynamics⁸. Using both in vitro experimentation and within-host modeling, it evidences the enhanced replication of viruses as a co-evolutionary tactic. It also establishes this as the reason for their devastating virulence and demonstrates the presence of an enhanced interferon-mediated immune response.

The spillover schema

‘Spillover’ is the term used to identify the specific event in which disease in a focal population has been transmitted from an animal reservoir source and depends upon it for its perpetuation. In other words, this is the event wherein a microbe in an animal source exits the animal, crosses the species barrier into another animal where it adopts a new avatar as a disease-causing pathogen.

For all the ease with which we commonly use the word; it is important to remember that spillovers are rare events and that the transition from microbe to pathogen is neither easy nor common. We live in a world that is teeming with microbes. Our own bodies are infested with them to the point where we now know that our bodies have actually been shaped and molded by them in what is called the microbiome. More than a third of human genes have their origin in bacteria⁹.

Microbes and pathogens are two ends of a continuum; inside every microbe is a potential pathogen and every pathogen is a microbe. Under certain circumstances, a commensal can turn pathogenic in its own host. A spillover event is however concerned with a microbe in one animal that crosses the species barrier and becomes pathogenic in another animal. That invariably happens because of the foreign, unrecognizable nature of the infecting organism which can be both directly toxic to the new host and can secondarily produce a strong defense response.

For zoonotic transmission to occur; a complex cocktail of circumstances needs to come together at the same time in what we might call a ‘Spillover Schema’. Since bats very rarely bite their targets; they must first shed the virus in question. Simultaneously, a susceptible intermediate host or target must be available close at hand. If this second animal is an intermediate host; the final human or animal target must then be in contact with this secondarily infected animal. Once seeded in a human, the virus must then set up an infection where it is expelled in body excretions in significant quantities in order for it to become a contagion. That is four steps in the schema already and four steps that must align simultaneously. Numbers are critical at every step — significant numbers of both the reservoir hosts, pathogens and targets are required to establish a sustainable contagion. This, as expected, requires highly fortuitous circumstances which is why spillover events are decidedly rare despite the many thousand trillion microbes that live with and around us.

A spillover event requires: the presence of density (of both the viral infecting agent and of overcrowding in the target population) and the absence of — a) distance (it thrives on intimate contact between virus and target), b) diversity (a diversity of susceptible species denies the virus the ease of locating and spreading in a captive host. This aspect played a major role in the potato blight which caused the Irish Famine and in the zoonoses of Lyme disease and West Nile virus disease) and, c) defense (weak or unprepared immune systems make for susceptible targets). Density needs the absence of distance and diversity for defense. That is, regions with high human population densities must defend themselves by maintaining an ecological barrier- distance from reservoir species and by preserving bio-diversity.

Ecology and conservation

Significant viral shedding in bats happens only when they are under stress. That stress could be an internal driver when the bat is combating illness or infection. More commonly, the stress factors are extraneous and related to human activity.

Although the last few instances of viral spillover have all involved bats as the source; it is not they that are to be blamed. Contrarily, it is unchecked human migration and expansion into bat territory that has created facilitatory circumstances for contact. In almost every zoonosis, regardless of the source, it is humans who have forced a point of contact either by causing the fragmentation of bat habitats by farming and urban expansion (windmills are a new challenge for bat conservation) or by hunting them for culinary or medicinal use. It is human predatory behavior that has, unknowingly or unthinkingly, caused the jump.

When under threat from an epidemic or pandemic, the almost knee jerk response to elimination of source raises important questions of conservation. Bats are critical hubs in ecosystems. They are both pollinators and predators. Their dwindling numbers disrupt both these crucial roles. Already bats are under threat because of take-over of their natural habitats and some of their species are listed as critically endangered.

Aside from human predation and in a reversal of circumstance that shatters, once more, our belief in our exceptionalism, humans have themselves served as an intermediate host for a chiropteran fungal disease — ‘white nose syndrome’ — that has afflicted North American landmass where the fungus, Psueduogymnoascus destructans has been ravaging sympatric bat populations for the past decade. Well known in Europe, it was alien to the North American geography until this century, and is now believed to have been transmitted to bats from an anthropogenic source. Humans transported the fungus on clothing, shoes and other fomites across the oceans from Europe to America and gifted it to bats across the pond.

Just like humans have cultivated-habitats that suit their purposes, just like we encounter the world through our own sensory experience; so too are the qualia-suited habitats of every other species. By our callous indifference to the environment of every species other than our own, we have put a great number of living creatures under stress from habitat takeover and pushed some of them to the brink of extinction. Whether through factory farms, wet markets or the outlawed hunting trade of wild animals, we have put ourselves in close contact with animals by illicit means that have now started to threaten our own health. Time and time again, in their every avatar, zoonoses reiterate the importance of respect for boundaries and urge us to rethink our eroded and deeply manipulative relationship with other animals.

The Umgebung

Biology’s discovery of echolocation first in bats and then in whales, led to Uexküll’s elaboration of the uniqueness of animal perception. It did not take long, from there, for philosophy to ponder the Umwelt. In 1974, one year after its description, Thomas Nagel authored a landmark essay in The Philosophical Review on the nature of consciousness titled, ‘What is it like to be a bat’¹⁰. He used the by then well documented uniqueness of chiropteran sensory perception to illustrate his argument that the subjective experience of consciousness eludes deterministic efforts. The unique and individual experience of human consciousness which varies not only from human to human but also between human and animal cannot be explained by psychophysical identification. The core argument of his essay was that the mind cannot be sited in brain matter nor can phenomenology in the physical.

“In so far as I can imagine this (which is not very far), it tells me only what it would be like for me to behave as a bat behaves. But that is not the question. I want to know what it is like for a bat to be a bat. Yet if I try to imagine this, I am restricted to the resources of my own mind, and those resources are inadequate to the task.” Further down he says, “The fact that we cannot expect ever to accommodate in our language a detailed description of Martian or bat phenomenology should not lead us to dismiss as meaningless the claim that bats and Martians have experiences fully comparable in richness of detail to our own”.

The extra-ordinariness of the bat’s experience of the world captivated the attention of not just scientists and philosophers; but of poets too. And the poets had, as is their wont, a startling prescience. Here is how Emily Dickinson described the bat¹¹: “Elate philosopher! Deputed from what firmament/ Of what astute abode/ Empowered with what malevolence/ Auspiciously withheld”. The new appreciation that reality is a spectrum sparked a growing awareness of species-consciousness across science and the humanities. Long unregarded doors opened again to new frontiers of animal behavior and cognition.

Umwelt is where we started and Umgebung is a good place to close. It stands in opposition to the parochial and limited world that the Umwelt affords us through our own restricted sensory capabilities. The Umgebung, instead, is the great undiscovered reality of the vast spectrum of sound, smell, taste and vision that exists outside human confines. By appreciating its unfathomable scope of experience, we recognize our presence as one amongst many on this planet and the attendant need, therefore, to re-calibrate our relationships with the myriad forms of life. The Umgebung’s explosive expanse exists in our very own territorial world as a reminder that infinitude is not always extraterrestrial. It is that same infinitude on earth.

Bat in moon. Biko Takahashi; Color woodblock print on paper. Source Credit: Brooklyn Museum https://www.brooklynmuseum.org/opencollection/objects/173752

References and footnotes:

1. Echolocation uses sound to create a visual representation of the environment making navigation easier under low vision or absent vision conditions. On the anatomy that produces echolocation in bats. Alain van Rickegham: ‘ How do bats echolocate and how are they adapted to this activity’https://www.scientificamerican.com/article/how-do-bats-echolocate-an/ Scientific American, Dec 14 1998. Karl Gruber: ‘Humans have the ability to echolocate too and click-based echolocation has been used by the blind for navigation’: https://phys.org/news/2018-04-humans-echolocation.html Phys Org April 3 2018.

2. B Muller at al: ‘More to Bats’ vision than meets the eye’ www.sciencedaily.com/releases/2009/07/090727203745.htm ScienceDaily, 29 July 2009

3. Taxonomy: https://animaldiversity.org/accounts/Chiroptera/classification/

4. Zoonoses (Greek: zoon — animal; nosos — disease) are infections contracted by humans from organisms that have jumped from their animal hosts to humans. Sometimes the transmission is direct; often it is indirect where there is an intermediate animal that serves as the bridge between the source and the end-target. For example, in SARS — the infecting agent was a virus, the SARS coronavirus which jumped from bats (the natural source) to civet cats (the intermediate host) to humans (the end target). Intermediate hosts come into play since bats have little point of contact with humans unlike the intermediate host which has contact with both source and target.

5. SS Pavlovitch et al: ‘The Egyptian Rousette Genome reveals unexpected features of bat antiviral immunity’ Cell. Volume 173. Issue 5, P1098–1110. E19, May 17 2018 https://www.cell.com/cell/fulltext/S0092-8674(18)30402-1?_returnURL=https%3A%2F%2Flinkinghub.elsevier.com%2Fretrieve%2Fpii%2FS0092867418304021%3Fshowall%3Dtrue#secsectitle0070

6. Plourde BT et al: ‘Are disease reservoirs special? Taxonomic and life history characteristics’ PLoS ONE 12(7): e0180716 https://doi.org/10.1371/journal.pone.0180716

7. The exception is the Hepadnavirus which is a DNA virus but uses an RNA intermediate for transcription

8. Brook CE et al: ‘Accelerated viral dynamics in bat cell lines, with implications for zoonotic emergence’ eLife 2020;9: e48401

9. Kat McGowan ‘Where animals come from’: https://www.quantamagazine.org/did-bacteria-drive-the-origins-of-animals-20140729/ Quanta Magazine 2014

10. Nagel Thomas “What is it like to be a bat”: https://warwick.ac.uk/fac/cross_fac/iatl/study/ugmodules/humananimalstudies/lectures/32/nagel_bat.pdf The Philosophical Review, 1974

11. Emily Dickinson ‘The Bat’ https://www.infoplease.com/primary-sources/poetry/emily-dickinson/poems-548 Collected Poems, Digireads, Sept 2016