Sick Bats Stay Home Alone: Social distancing during the acute phase response in Egyptian fruit bats (Rousettus aegyptiacus)

Background

Animals are not much different from humans in the ways of responding to illness both at behavioral and immunological levels. The fever response to illness is preserved across different invertebrates and vertebrates (Kluger 1978). In addition to this, there are a set of behaviors such as lethargy, loss of appetite, anxiety, depression and sleepiness exhibited in sick animals (including humans) that are collectively termed as ‘sickness behaviors’ (Hart 2010). For a group living animal, during sickness, these behaviors act as strategies to reduce energy loss at the individual context and decrease disease transmission risks in the social context (Shakhar and Shakhar 2015). However, very few studies have investigated the behavior of sick individuals in free-ranging mammal societies.

Bats are highly gregarious mammals that form colonies up to millions of individuals in the wild. Yet, except for one recent study, there has been no exploration of sickness behaviors in free-ranging bats (Ripperger et al. 2020). Using controlled experiments, GPS telemetry and immunological assays, the current study has demonstrated that sick individuals of the Egyptian fruit bat Rousettus aegyptiacus self-isolated themselves when challenged with a bacterial endotoxin that induced an inflammatory response, simulating a sick-like situation. The authors have used a plethora of approaches to show sickness-related responses in a highly social, long-lived bat and have discussed the implications of their findings in studying the disease transmission patterns among free-ranging bat social groups

Key findings

In this preprint, the authors show how the Egyptian fruit bat Rousettus aegyptiacus responds to bacterial illness. They challenged the bats with lipopolysaccharide (LPS) injection to elicit a sick-like situation for which the bats responded by developing a fever and losing weight. Using a clear experimental design, the authors first provide evidence of a physiological response to sickness in both captive and free-ranging individuals.

Next, they show behavioral responses where the sick bats isolated themselves from the rest of the social groups during the day in the indoor trials. Unlike other animal systems, this was not a case of intra-group aggression where healthy individuals avoided the sick ones (Heinze and Walter 2010; Kazlauskas et al. 2016). Instead, the sick individuals self-isolated themselves and maintained a social distance from the other group members. Their video observations further show that sick bats, after self-isolation, remained less active by reducing their movements which is a typical sickness behavior. In the free-ranging colony, the authors show a clear difference in flight and foraging patterns in sick individuals. Using GPS telemetry, they show sick bats remained in their roost for the first two nights after the LPS injection, and then they flew only for relatively shorter distances compared to the nights before injection.

In addition to these behavioral demonstrations, the authors also show immunological responses to sickness by measuring blood parameters in bats. Compared to the control group, sick bats had a higher neutrophil to lymphocyte ratio (NLR) which is an indicator of physiological stress. The sick bats in the indoor trials also showed a similar increase in haptoglobin – an acute phase protein with immunomodulatory effects, and lysozyme – the antibacterial enzyme that hydrolyses bacterial cell walls compared to the control group (Fig 1).

This study reports self-imposed social isolation as a sickness response in a free-ranging mammal for the first time. The authors also point out that this is the first study to record foraging patterns of sick-like bats in the field. They discuss that self-isolation directly reduces disease transmission for the group.  However, by moving away from the clusters, the sick individuals prevent themselves from raising their temperatures as bats usually get closer to increase their body temperatures. Also, such self-isolation could prevent sick individuals from wasting their energy on intraspecific interactions such as squabbling or pushing to maintain their position in their social groups.

These findings highlight the importance of studying sickness and stress responses on long-lived mammals as it is important to understand pathogen transmission among them. The authors also point out that self-isolation behaviors in bats reduce the transmission of pathogens both within the social group and most importantly reduce the possibilities of inter-specific spillover events. They also emphasize the importance of leaving critical habitats like bat roosts undisturbed as such human disturbances could primarily lead to spill-over events.

Why do I like this preprint?

Bats have been the major animal in focus from the start of the COVID-19 pandemic. Highly misunderstood, these animals are portrayed as the main reason for the pandemic. However, studies have clearly shown how bats handle pathogens without getting infected (Wynne and Wang 2013; Moratelli et al. 2015). The current study has focused on the sickness behaviors of Egyptian fruit bats that are highly colonial and known to roost in human-dominated landscapes. I liked the study as the authors have sent out a clear message that sick bats practice social distancing to reduce transmission risks and that could potentially change the public perception of bats, especially in the current situation. In addition to that, studies on sickness responses are lacking in such long-lived social animals that are often associated with zoonotic transmission. The authors have demonstrated how free-ranging bats respond to illness and they show the similarities of sickness-related behaviors that are common among bats and other mammals including humans. This study could potentially pave the way for many follow-up studies in other free-ranging bat species that roost near human habitations. This study demonstrates that free-ranging bats have natural mechanisms to control pathogen transmission within their social groups and hence are less likely to cause an inter-specific spillover event.

Questions and comments to the authors

1. The authors mention that males for the closed colony were caught from a natural roost and then mixed with the females from a captive colony after a two-week acclimation. What is the justification for selecting two weeks for this? Is there any prior standardization in this species showing clearance of pathogens from their system in 14 days?
2. The authors discuss that a higher baseline haptoglobin in the free-ranging colony could be due to their nightly exposure to outdoor bacterial pathogens. Since males in the closed colony were also exposed to outdoor pathogens before two weeks, is it possible that could cause the higher basal level haptoglobin level in the treatment group? How did the authors control for that?
3. There is a mention of an anecdotal female-female interaction in the closed group where a healthy female hung near the sick-like isolated female. Could those two individuals be a mother-daughter pair? As the females were from the same captive colony, were their social interactions monitored earlier?
4. Is there a reason for not comparing male and female sickness responses in the results? Since female bats could modify their flight patterns according to their reproductive status, an inter-gender comparison could have been presented. Can the authors comment on this?
5. In the Mixed ANOVA analysis for the temperature treatment, the authors have chosen 6 hours pre – 8 hours post LPS injection. Why was this time range chosen? A justification statement can be added. Also in the GLMM for sociality/isolation, the authors could provide some more details about the models as their descriptions are not clear.

References

Hart B (2010) Beyond Fever: Comparative Perspectives on Sickness Behavior. In: Encyclopedia of Animal Behavior. pp 205–210

Heinze J, Walter B (2010) Moribund Ants Leave Their Nests to Die in Social Isolation. Curr Biol 20:249–252. https://doi.org/10.1016/j.cub.2009.12.031

Kazlauskas N, Klappenbach M, Depino AM, Locatelli FF (2016) Sickness Behavior in Honey Bees. Front Physiol 7. https://doi.org/10.3389/fphys.2016.00261

Kluger MJ (1978) The Evolution and Adaptive Value of Fever: Long regarded as a harmful by-product of infection, fever may instead be an ancient ally against disease, enhancing resistance and increasing chances of survival. Am Sci 66:38–43

Moratelli R, Calisher CH, Moratelli R, Calisher CH (2015) Bats and zoonotic viruses: can we confidently link bats with emerging deadly viruses? Mem Inst Oswaldo Cruz 110:1–22. https://doi.org/10.1590/0074-02760150048

Ripperger SP, Stockmaier S, Carter GG (2020) Sickness behaviour reduces network centrality in wild vampire bats. bioRxiv 2020.03.30.015545. https://doi.org/10.1101/2020.03.30.015545

Shakhar K, Shakhar G (2015) Why Do We Feel Sick When Infected—Can Altruism Play a Role? PLOS Biol 13:e1002276. https://doi.org/10.1371/journal.pbio.1002276

Wynne JW, Wang L-F (2013) Bats and Viruses: Friend or Foe? PLOS Pathog 9:e1003651. https://doi.org/10.1371/journal.ppat.1003651

Tags: bats, fever response, illness, social distancing

doi: https://doi.org/10.1242/prelights.26350

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