Captive Bats Research Articles

Thirty years of conservation breeding: Assessing the genetic diversity of captive Livingstone's fruit bats.

Fruit bats (genus Pteropus) are typically island-endemic species important in seed dispersal and reforestation that are vulnerable to increased extinction risk. An effective method of reducing extinction risk in vulnerable species that cannot be conserved in their native habitat is establishing an ex-situ captive breeding programme. Due to anthropogenic threats and low population numbers, in the early 1990s, a captive breeding programme was established at Jersey Zoo, British Isles, for Critically Endangered Livingstone's fruit bats (Pteropus livingstonii). Here we use six polymorphic microsatellite loci to assess genetic diversity in the captive breeding population of Livingstone's fruit bats (P. livingstonii), 30 years after the programme's establishment, investigating change over generations and comparing our findings with published data from the wild population. We found no significant difference between the genetic diversity in the captive and wild populations of Livingstone's fruit bats (P. livingstonii), in both expected heterozygosity and allelic richness. The captive population has retained a comparable level of genetic diversity to that documented in the wild, and there has been no significant decline in genetic diversity over the last 30 years. We advise that a full pedigree of the paternal lineage is created to improve the management of the captive breeding programme and further reduce the possibility of inbreeding. However, it appears that the captive breeding programme is currently effective at maintaining genetic diversity at levels comparable to those seen in the wild population, which suggests reintroductions could be viable if genetic diversity remains stable in captivity.

Tiger beetles produce anti-bat ultrasound and are probable Batesian moth mimics.

Echolocating bats and their eared insect prey are in an acoustic evolutionary war. Moths produce anti-bat sounds that startle bat predators, signal noxiousness, mimic unpalatable models and jam bat sonar. Tiger beetles (Cicindelidae) also purportedly produce ultrasound in response to bat attacks. Here we tested 19 tiger beetle species from seven genera and showed that they produce anti-bat signals to playback of authentic bat echolocation. The dominant frequency of beetle sounds substantially overlaps the sonar calls of sympatric bats. As tiger beetles are known to produce defensive chemicals such as benzaldehyde and hydrogen cyanide, we hypothesized that tiger beetle sounds are acoustically advertising their unpalatability. We presented captive big brown bats (Eptesicus fuscus) with seven different tiger beetle species and found that 90 out of 94 beetles were completely consumed, indicating that these tiger beetle species are not aposematically signalling. Instead, we show that the primary temporal and spectral characteristics of beetle warning sounds overlap with sympatric unpalatable tiger moth (Arctinae) sounds and that tiger beetles are probably Batesian mimics of noxious moth models. We predict that many insect taxa produce anti-bat sounds and that the acoustic mimicry rings of the night sky are hyperdiverse.

Scanning efficacy of p-Chips implanted in the wing and leg of the Big Brown Bat (Eptesicus fuscus).

Individual marking techniques are critical for studying animals, especially in the wild. Current marking methods for bats (Order Chiroptera) have practical limitations and some can cause morbidity. We tested the p-Chip (p-Chip Corp.)-a miniaturized, laser light-activated microtransponder-as a prospective marking technique in a captive research colony of Big Brown Bats (Eptesicus fuscus). We assessed long-term readability and postimplantation effects of p-Chips injected subcutaneously above the second metacarpal (wing; n = 30) and the tibia (leg; n = 13 in both locations). Following implantation (Day 0), p-Chips were scanned with a hand-held ID reader (wand) on postimplantation days (PIDs) 1, 8, 15, 22, 32, 60, 74, 81, 88, 95, and over 1 year later (PID 464). For each trial, we recorded: (1) animal handling time; (2) scan time; (3) number of wand flashes; (4) p-Chip visibility; and (5) overall condition of the bat. Average scan times for p-Chips implanted in both the wing and leg increased over the duration of the study; however, the number of wand flashes decreased, suggesting that efficacy of p-Chip recording increased with user experience. Importantly, over 464 days both the visibility and readability of p-Chips in the wing remained high and superior to tags in the leg, establishing the second metacarpal as the preferred implantation site. Observed morbidity and mortality in captive bats with p-Chips was similar to baseline values for bats without these tags. Because scan efficiency on PID 464 was comparable with earlier days, this indicates that p-Chips implanted in the wing may be suitable as a long-term marking method. Our provisional results suggest that p-Chips are viable for extended field testing to see if they are suitable as an effective alternative to traditional methods to mark bats.

Interactions between nutrients and fruit secondary metabolites shape bat foraging behavior and protein absorption

AbstractFrugivore foraging behavior is largely influenced by two key groups of chemical traits: nutrients and secondary metabolites. Many secondary metabolites function in plant defense, but their consumption can negatively impact both mutualistic and antagonistic frugivores, often due to toxic properties of the metabolites or through nutrient absorption interference. Frugivores are assumed to maximize nutrient acquisition while avoiding or minimizing toxic metabolite intake, but the relative roles of co‐occurring nutrients and secondary metabolites in foraging behavior are not well understood. Here, we used a neotropical fruit bat to investigate the interactive effects of nutrients and a broadly bioactive fruit secondary metabolite, piperine, on two essential processes in nutrient acquisition, namely foraging behavior and nutrient absorption. Through the manipulation of nutrient and piperine concentrations in artificial diets, we showed that captive fruit bats prioritize nutrient concentrations regardless of the levels of piperine, even though piperine is a strong deterrent on its own. Furthermore, our findings reveal that while piperine has no detectable influence on total sugar absorption, it reduces protein absorption, which is a crucial and limited nutrient in the frugivore diet. Overall, our results demonstrate the importance of considering the interaction between co‐occurring chemical traits in fruit pulp to better understand frugivore foraging and physiology.

Weight as an indicator of enclosure suitability in Livingstone's fruit bats (Pteropus livingstonii).

Obesity is common in zoo animals, and both dietary management and the provision of adequate opportunities for exercise are needed to tackle it. We used 30 years of records from Jersey Zoo to compare the weight and forearm length of wild and captive-born Livingstone's fruit bats (Pteropus livingstonii), and to assess the impact on weight of enclosure space. The mean capture weight of wild-caught male Livingstone's bats was 657 g, significantly higher than that of females (544 g). In both wild and captive-born bats, males had significantly longer forearms than females, but there was no effect of birth location. Males weighed more in the mating season than at other times of year. Both sexes gained more weight during development if born in enclosures that restricted flight rather than a large aviary; this was particularly noticeable in females. After reaching maturity at 3 years, weights of bats born in restricted enclosures continued to increase, reached a peak of over 1000 g at 8-10 years, and then declined in both sexes. The weight of bats born in the aviary remained more stable after the age of three. Like wild bats, adult females born in the aviary weighed less than males. However, females born in restricted enclosures weighed more than males born in the same enclosures. Enclosure designs that maximize opportunities for flight can limit excessive weight gain in captive fruit bats and may therefore improve fitness and health, essential in planning for future reintroduction programs.

Sex differences and individual variability in the captive Jamaican fruit bat (Artibeus jamaicensis) intestinal microbiome and metabolome

The intestinal microbiome plays an important role in mammalian health, disease, and immune function. In light of this function, recent studies have aimed to characterize the microbiomes of various bat species, which are noteworthy for their roles as reservoir hosts for several viruses known to be highly pathogenic in other mammals. Despite ongoing bat microbiome research, its role in immune function and disease, especially the effects of changes in the microbiome on host health, remains nebulous. Here, we describe a novel methodology to investigate the intestinal microbiome of captive Jamaican fruit bats (Artibeus jamaicensis). We observed a high degree of individual variation in addition to sex- and cohort-linked differences. The intestinal microbiome was correlated with intestinal metabolite composition, possibly contributing to differences in immune status. This work provides a basis for future infection and field studies to examine in detail the role of the intestinal microbiome in antiviral immunity.

Artificial light affects foraging behavior of a synanthropic bat.

Artificial light at night has been considered an emerging threat to global biodiversity. However, the impacts of artificial light on foraging behavior in most wild animals remain largely unclear. Here, we aimed to assess whether artificial light affects foraging behavior in Asian parti-colored bats (Vespertilio sinensis). We manipulated the spectra of light-emitting diode (LED) lighting in a laboratory. Using video and audio recording, we monitored foraging onset, total foraging time, food consumption, freezing behavior (temporary cessation of body movement), and echolocation vocalizations in triads of bats under each lighting condition. Analyses showed that the foraging activities of experimental bats were reduced under LED light. Green, yellow, and red light had greater negative effects on bats' foraging onset, total foraging time, and food consumption than white and blue light. LED light of different spectra induced increased freezing time and echolocation vocalizations in captive bats, except for the white light. The peak wavelength of light emission correlated positively with freezing time, estimated echolocation pulse rate (the number of echolocation pulses per minute), and foraging onset, but negatively with total foraging time and food consumption. These results demonstrate that artificial light disturbs foraging behavior in Asian parti-colored bats. Our findings have implications for understanding the influencing mechanism of light pollution on bat foraging.

Patterns of post-hibernation wing damage healing in little brown bats (Myotis lucifugus) impacted by white-nose syndrome

Abstract The patterns of recovery from injury or infection are not well studied in free-ranging animals. Bats that survive the fungal disease white-nose syndrome (WNS) often emerge from hibernation suffering from skin infections and wing damage. The extent of wing damage reflects physiological and immunological responses to WNS and may impact the ability of bats to fly, forage, and reproduce. Here, we built on previous studies of wing damage in both captive and free-ranging bats to better understand the patterns and extent of wing damage healing in little brown bats (Myotis lucifugus) post-hibernation. We quantified two main types of wing damage, black necrotic dots and white spots, and used the extent of damage to assign bats 1 of 6 wing damage scores. We found that the patterns of black dots and white spots on wing membranes of free-ranging bats aligned with the patterns observed in captive bats soon after emergence from hibernation. Black dot extent was highest at the beginning of the active season in May, while white spot extent peaked 3–4 weeks later. Our study also extends our knowledge of wing damage healing throughout the active season. Wing scores of bats recaptured within the summer decreased or stayed the same and >95% had negligible signs of wing damage by August. We found that black dots were more indicative of disease status than other types of wing damage and could be consistently quantified in the field and from photographs by multiple observers. These results suggest that black dots and our wing damage scoring system can be used to better understand the patterns of post-hibernation healing in little brown bats impacted by WNS.

Contrasting torpor use by reproductive male common noctule bats in the laboratory and in the field.

Metabolic processes of animals are often studied in controlled laboratory settings. However, these laboratory settings often do not reflect the animals' natural environment. Thus, results of metabolic measurements from laboratory studies must be cautiously applied to free-ranging animals. Recent technological advances in animal tracking allow detailed eco-physiological studies that reveal when, where and how physiological measurements from the field differ from those from the laboratory. We investigated torpor behavior of male common noctule bats (Nyctalus noctula) across different life history stages using two approaches: in controlled laboratory experiments and in the field using calibrated heart rate telemetry. We predicted that non-reproductive males would extensively use torpor to conserve energy, whereas reproductive males would reduce torpor use to promote spermatogenesis. We did not expect differences in torpor use between captive and wild animals as we simulated natural temperature conditions in the laboratory. We found that during the non-reproductive phase, both captive and free-ranging bats used torpor extensively. During reproduction, bats in captivity unexpectedly also used torpor throughout the day, while only free-ranging bats showed the expected reduction in torpor use. Thus, depending on life history stage, torpor behavior in the laboratory was markedly different from the wild. By implementing both approaches and at different life history stages, we were able to better explore the limitations of eco-physiological laboratory studies and make recommendations for when they are an appropriate proxy for natural behavior.

Genomic Characterization of a Relative of Mumps Virus in Lesser Dawn Bats of Southeast Asia.

The importance of genomic surveillance on emerging diseases continues to be highlighted with the ongoing SARS-CoV-2 pandemic. Here, we present an analysis of a new bat-borne mumps virus (MuV) in a captive colony of lesser dawn bats (Eonycteris spelaea). This report describes an investigation of MuV-specific data originally collected as part of a longitudinal virome study of apparently healthy, captive lesser dawn bats in Southeast Asia (BioProject ID PRJNA561193) which was the first report of a MuV-like virus, named dawn bat paramyxovirus (DbPV), in bats outside of Africa. More in-depth analysis of these original RNA sequences in the current report reveals that the new DbPV genome shares only 86% amino acid identity with the RNA-dependent RNA polymerase of its closest relative, the African bat-borne mumps virus (AbMuV). While there is no obvious immediate cause for concern, it is important to continue investigating and monitoring bat-borne MuVs to determine the risk of human infection.

Predictors of dominance rank and agonistic interactions in captive Livingstone's fruit bats.

Male dominance hierarchies have been studied in many animals but rarely in bats (Chiroptera). The dominance rank of social animals may dictate access to resources and mates; therefore, it has important implications for an individual's fitness and is crucial for successful captive management. Between January and December 2018, at both Bristol Zoo Gardens (Bristol, UK) and Jersey Zoo (Jersey, British Isles), we observed 19 male Livingstone's fruit bats Pteropus livingstonii using focal follows for 345 h overall, noting the outcome of all agonistic interactions. We recorded instigators of interactions, along with winners and losers, and analyzed these data using the R-package "EloRating" to create Elo-rating temporal plots of dominance ranks. We used generalized linear mixed models and multiple linear regression to analyze interaction data and test hypotheses regarding predictors of dominance rank, frequency of agonistic interaction, and choice of interaction partner. Age was positively correlated with dominance rank up to around year 9, when an asymptote was attained. Highly ranked bats instigated the most agonistic interactions, and largely directed these interactions at bats with much lower rankings than themselves. Hierarchies were extremely stable throughout the data collection period at both sites. We conclude that Livingstone's fruit bats have a stable linear dominance hierarchy, with high-ranking, typically older males instigating the most interactions with lowest ranking males to secure dominance rank. This study adds to the limited discourse on Pteropus social behaviors, indicating that some bat species may have social systems similar in complexity to some nonhuman primates.

Social effects of rabies infection in male vampire bats (Desmodus rotundus).

Rabies virus (RABV) transmitted by the common vampire bat (Desmodus rotundus) poses a threat to agricultural development and public health throughout the Neotropics. The ecology and evolution of rabies host-pathogen dynamics are influenced by two infection-induced behavioural changes. RABV-infected hosts often exhibit increased aggression which facilitates transmission, and rabies also leads to reduced activity and paralysis prior to death. Although several studies document rabies-induced behavioural changes in rodents and other dead-end hosts, surprisingly few studies have measured these changes in vampire bats, the key natural reservoir throughout Latin America. Taking advantage of an experiment designed to test an oral rabies vaccine in captive male vampire bats, we quantify for the first time, to our knowledge, how rabies affects allogrooming and aggressive behaviours in this species. Compared to non-rabid vampire bats, rabid individuals reduced their allogrooming prior to death, but we did not detect increases in aggression among bats. To put our results in context, we review what is known and what remains unclear about behavioural changes of rabid vampire bats (resumen en español, electronic supplementary material, S1).

Ethogram of Ghost Bat (Macroderma gigas) Behaviours and Associated Social Vocalisations

The ghost bat (Macroderma gigas) is a carnivorous species of bat endemic to northern Australia that roosts in colonies of up to 1,500 individuals. The ghost bat produces a number of social vocalisations, but little is known about the species' behaviour and what role social vocalisations play in interactions between conspecifics. The aim of this study was to construct an ethogram of ghost bat behaviours and to determine the associations between behaviours and social vocalisations. To achieve our aims, we filmed the behaviour of a captive ghost bat colony (one male, five females) using four trail cameras installed within the enclosure over a six-week period, coinciding with the estimated mating season. Video recordings were examined by eye, and solitary and social behaviours were catalogued into distinct behavioural units (e.g. hang-alert, chew, wing-groom, etc.) along with social context and associated social vocalisations, if applicable. To assess the associations between behavioural interactions and social vocalisation types, we combined each of the catalogued social behavioural units into six behavioural classes (eating, grooming, mating, huddling, flying, and fighting) and used generalised linear models to determine which social behavioural classes significantly predicted the production of each vocalisation. There was a strong association between flight behaviour by a member of the colony and the production of the ‘Chirp-trill’ vocalisation by the male member of the colony, suggesting a territorial or mate attraction function. There was also a strong association between fighting behaviour and the production of the ‘Squabble’, ‘Rasp’ and ‘Grumble’ vocalisations, with the Squabble and Rasp likely representing levels of agonistic vocalisations produced by aggressive bats during altercations. The Grumble, on the other hand, was produced by the target of the aggressor and so may function as an appeasement call. The ethogram with its associated social vocalisations provides a formal basis for future behavioural studies in this species and can serve as a template for such studies in other echolocating bats. Our study revealed an unexpected degree of complexity in the behaviour and associated vocalisations in this species and highlights the need for studies of this kind in other bats.

Staphylococcus aureus lineages associated with a free-ranging population of the fruit bat Pteropus livingstonii retained over 25 years in captivity

Conservation of endangered species has become increasingly complex, and costly interventions to protect wildlife require a robust scientific evidence base. This includes consideration of the role of the microbiome in preserving animal health. Captivity introduces stressors not encountered in the wild including environmental factors and exposure to exotic species, humans and antimicrobial drugs. These stressors may perturb the microbiomes of wild animals, with negative consequences for their health and welfare and hence the success of the conservation project, and ultimately the risk of release of non-native organisms into native ecosystems. We compared the genomes of Staphylococcus aureus colonising critically endangered Livingstone’s fruit bats (Pteropus livingstonii) which have been in a captive breeding programme for 25 years, with those from bats in the endemic founder population free ranging in the Comoros Republic. Using whole genome sequencing, we compared 47 isolates from captive bats with 37 isolates from those free ranging in the Comoros Republic. Our findings demonstrate unexpected resilience in the bacteria carried, with the captive bats largely retaining the same two distinctive lineages carried at the time of capture. In addition, we found evidence of genomic changes which suggest specific adaptations to the bat host.

Establishment of a Captive Cave Nectar Bat (Eonycteris spelaea) Breeding Colony in Singapore.

Bats are known natural reservoirs of several highly pathogenic zoonotic viruses, including Hendra virus, Nipah virus, rabies virus, SARS-like coronaviruses, and suspected ancestral reservoirs of SARS-CoV-2 responsible for the ongoing COVID-19 pandemic. The capacity to survive infections of highly pathogenic agents without severe disease, together with many other unique features, makes bats an ideal animal model for studying the regulation of infection, cancer, and longevity, which is likely to translate into human health outcomes. A key factor that limits bat research is lack of breeding bat colonies. To address this need, a captive bat colony was established in Singapore from 19 wild-caught local cave nectar bats. The bats were screened for specific pathogens before the start of captive breeding. Custom-made cages and an optimized diet inclusive of Wombaroo dietary formula, liquid diet, and supplement of fruits enabled the bats to breed prolifically in our facility. Cages are washed daily and disinfected once every fortnight. Bats are observed daily to detect any sick bat or abnormal behavior. In addition, bats undergo a thorough health check once every 3 to 4 mo to check on their overall wellbeing, perform sampling, and document any potential pregnancy. The current colony houses over 80 bats that are successfully breeding, providing a valuable resource for research in Singapore and overseas.

Two Novel Iflaviruses Discovered in Bat Samples in Washington State.

Arthropods are integral to ecosystem equilibrium, serving as both a food source for insectivores and supporting plant reproduction. Members of the Iflaviridae family in the order Picornavirales are frequently found in RNA sequenced from arthropods, who serve as their hosts. Here we implement a metagenomic deep sequencing approach followed by rapid amplification of cDNA ends (RACE) on viral RNA isolated from wild and captured bat guano in Washington State at two separate time points. From these samples we report the complete genomes of two novel viruses in the family Iflaviridae. The first virus, which we call King virus, is 46% identical by nucleotide to the lethal honeybee virus, deformed wing virus, while the second virus which we call Rolda virus, shares 39% nucleotide identity to deformed wing virus. King and Rolda virus genomes are 10,183 and 8934 nucleotides in length, respectively. Given these iflaviruses were detected in guano from captive bats whose sole food source was the Tenebrio spp. mealworm, we anticipate this invertebrate may be a likely host. Using the NCBI Sequence Read Archive, we found that these two viruses are located in six continents and have been isolated from a variety of arthropod and mammalian specimens.

Diseases and histopathological findings from lesional pinnae of 10 bats

AbstractPinnae are vital structures for echolocation and survival in many species of bats. Pinnal lesions have been described as common in captive bats, but information on specific diseases affecting the pinnae is scarce. A collection of histological sections of lesional pinnae from 10 bats, archived by bat conservation centers worldwide, was examined to identify potential aetiologies of disease. No neoplastic changes were seen but all pinnae showed inflammation, most commonly intraepidermal pustular dermatitis, deep perivascular dermatitis, nodular and/or diffuse dermatitis, and panniculitis. All bats with deep inflammation had concurrent pinnal perichondritis and cartilage necrosis. Microbial overgrowth was frequent, and pyoderma was confirmed in two bats based on histopathological and culture findings. Although no single aetiological agent was identified, deep inflammation was common and severe, highlighting the potential detriment to affected bats and the need for future study of these delicate structures.

Temperature alone is insufficient to understand hibernation energetics.

Energy conservation has long been a focal point in hibernation research. A long-standing assumption is that ambient temperature (Ta) largely defines the rate of energy expenditure because of well-known relationships between Ta, metabolic rate and frequency of arousal from torpor. Body condition and humidity also affect energy expenditure but are usually considered secondary factors. We held tricolored bats (Perimyotis subflavus) in captivity under multiple environmental conditions to directly compare the importance of Ta, fat mass and humidity for hibernation energy expenditure. Fat mass was the best predictor of female mass loss, followed by Ta and humidity. However, males had less fat and adopted a more energetically conservative hibernation strategy. Our results demonstrate that understanding the evolution of behavior, physiology and ecology of hibernation requires disentangling the relative contributions of multiple drivers of hibernation energetics, and that Ta is not always the most important factor driving energy expenditure.

Body size affects immune cell proportions in birds and non-volant mammals, but not bats.

Powered flight has evolved several times in vertebrates and constrains morphology and physiology in ways that likely have shaped how organisms cope with infections. Some of these constraints probably have impacts on aspects of immunology, such that larger fliers might prioritize risk reduction and safety. Addressing how the evolution of flight may have driven relationships between body size and immunity could be particularly informative for understanding the propensity of some taxa to harbor many virulent and sometimes zoonotic pathogens without showing clinical disease. Here, we used a comparative framework to quantify scaling relationships between body mass and the proportions of two types of white blood cells - lymphocytes and granulocytes (neutrophils/heterophils) - across 63 bat species, 400 bird species and 251 non-volant mammal species. By using phylogenetically informed statistical models on field-collected data from wild Neotropical bats and from captive bats, non-volant mammals and birds, we show that lymphocyte and neutrophil proportions do not vary systematically with body mass among bats. In contrast, larger birds and non-volant mammals have disproportionately higher granulocyte proportions than expected for their body size. Our inability to distinguish bat lymphocyte scaling from birds and bat granulocyte scaling from all other taxa suggests there may be other ecological explanations (i.e. not flight related) for the cell proportion scaling patterns. Future comparative studies of wild bats, birds and non-volant mammals of similar body mass should aim to further differentiate evolutionary effects and other aspects of life history on immune defense and its role in the tolerance of (zoonotic) infections.

COVID-19: Vaccine Delivery System, Drug Repurposing and Application of Molecular Modeling Approach.

The acute respiratory syndrome coronavirus (SARS-CoV-2) has spread across the world, resulting in a pandemic COVID-19 which is a human zoonotic disease that is caused by a novel coronavirus (CoV) strain thought to have originated in wild or captive bats in the initial COVID outbreak region. The global COVID-19 outbreak started in Guangdong Province, China’s southernmost province. The global response to the COVID-19 pandemic has been hampered by the sheer number of infected people, many of whom need intensive care before succumbing to the disease. The epidemic is being handled by a combination of disease control by public health interventions and compassionate treatment for those who have been impacted. There is no clear anti-COVID-19 medication available at this time. However, the need to find medications that can turn the tide has led to the development of a number of investigational drugs as potential candidates for improving outcomes, especially in the severely and critically ill. Although many of these adjunctive medications are still being studied in clinical trials, professional organizations have attempted to define the circumstances in which their use is deemed off-label or compassionate. It is important to remind readers that new information about COVID-19’s clinical features, treatment options, and outcomes is released on a regular basis. The mainstay of treatment remains optimized supportive care, and the therapeutic effectiveness of the subsequent agents is still being studied.