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Monitoring the health of wildlife populations is essential in the face of increased agricultural expansion and forest fragmentation. Loss of habitat and habitat degradation can negatively affect an animal’s physiological state, possibly resulting in immunosuppression and increased morbidity or mortality. We sought to determine how fragmentation may differentially impact cellular immunity and infection risk in Neotropical bats species regularly infected with bloodborne pathogens, and to evaluate how effects may vary over time and by dietary habit. We studied common vampire bats (Desmodus rotundus), northern yellow-shouldered bats (Sturnira parvidens), and Mesoamerican mustached bats (Pteronotus mesoamericanus), representing the dietary habits of sanguinivory, frugivory, and insectivory respectively, in northern Belize. We compared estimated total white blood cell counts, leukocyte differentials, and infection status with two blood-borne bacterial pathogens (Bartonellaspp. and hemoplasmas) of 118 bats captured in a broadleaf, secondary forest over a three-year period (2017-2019) of increasing habitat fragmentation. We found evidence for bat species-specific responses of cellular immunity between years, with neutrophil counts increasing inD. rotundus, but decreasing inS. parvidensandP. mesoamericanusfrom 2018 to 2019. However, the odds of infection withBartonellaspp. and hemoplasma spp. between 2017 and 2019 did not differ between bat species, contrary to our prediction that pathogen prevalence may increase with increased fragmentation. We conclude that each bat species invested differently in cellular immunity in ways that changed over years of increasing fragmentation. We recommend further research on the interactions between habitat fragmentation, cellular immunity, and infection across dietary habits of Neotropical bats for informed management and conservation.

The recent pandemic and other environmental concerns have resulted in restrictions on research and surveys involving capture and handling bats. While acoustic surveys have been widely used as an alternative survey method, in this study, we show how photographic surveys can offer an important contribution to study and survey bats. We outline approaches, using high speed flash and automated trip beams to obtain photos of flying bats of sufficient quality for reliable identification of species. We show, through a series of examples of setups and photographs, that photography is effective for surveying bats at a variety of sites, where bats roost, drink, and forage. We note, however, that photographic surveys cannot replace capture in all situations. In addition, although photographing bats is less invasive than capturing them, it can involve disturbance, so we stress the importance of minimizing the impact of such operations on bats.The online version contains supplementary material available at 10.1007/s42991-022-00233-7.

Genetic exchange and hybridization appear common among the western long-eared bats from North America. Multiple sources of evidence indicate that lineages within this group are evolving independently, despite genetic exchange. However, evidence of gene flow raises questions about the species-level status of some lineages. C.L. Lausen et al. (2019. Can. J. Zool. 97(3): 267–279) proposed that Myotis evotis (H. Allen, 1864) (long-eared myotis) and Myotis keenii (Merriam, 1895) (Keen’s myotis) are one species, not two. This conclusion is based on analyses of cytochrome b and microsatellite data suggesting gene flow between these taxa. Microsatellites are not reliable markers for identifying species because homoplasy can be a major confounding factor, which appears to be true in this case. We reanalyzed the dataset of C.L. Lausen et al. (2019) and show that it is not reliable to distinguish between gene flow or homoplasy, and that these data do not support the conclusion that M. evotis and M. keenii represent a single species. Previous morphological and genomic studies indicate that these are separate species despite previous genetic exchange between them. Failing to recognize that gene flow can occur between independently evolving lineages is counterproductive for conservation because it can lead to neglect of important independent lineages, and likewise failing to use proper tools to delimit species is counterproductive to efforts to quantify biodiversity and design conservation strategies.

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Bats are susceptible to rabies. Although bats may appear to be asymptomatic carriers of rabies for a few days, eventually they fall ill to the viral infection and die. Two of at least four bat-specific variants of rabies virus in Canada have killed humans. Rabies is usually transmitted by biting, but bats are small mammals so their bites may go unnoticed. People exposed to rabid animals should receive postexposure prophylaxis (PEP). With 60 known human deaths from 1950 to 2009, rabies is rare in Canada and the United States of America compared with India where it kills over 100 people annually. In Asia and Africa, most human rabies is acquired from dog bites. In Brazil, dog and bat bites together account for >80% of human rabies. In Canada, rabies is a disease primarily confined to wildlife (foxes, racoons, skunks, and bats). The public image of bats is negatively affected by their association with diseases. Too often bats are victimized by allegations of their role in deadly diseases such as rabies, Ebola, severe acute respiratory syndrome (SARS), and Middle East respiratory syndrome (MERS). In general, bats are not dangerous, but humans should seek treatment if they are bitten by one. (Graphical abstract shows a 4-g elegant myotis biting MBF’s finger—photo by Sherri and Brock Fenton.)

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.

Bats are increasingly studied as model systems for longevity and as natural hosts for some virulent viruses. Yet the ability to characterize immune mechanisms of viral tolerance and to quantify infection dynamics in wild bats is often limited by small sample volumes and few species-specific reagents. Here, we demonstrate how proteomics can overcome these limitations by using data-independent acquisition-based shotgun proteomics to survey the serum proteome of 17 vampire bats (Desmodus rotundus) from Belize. Using just 2 μL of sample and relatively short separations of undepleted serum digests, we identified 361 proteins across 5 orders of magnitude. Levels of immunological proteins in vampire bat serum were then compared to human plasma via published databases. Of particular interest were antiviral and antibacterial components, circulating 20S proteasome complex and proteins involved in redox activity. Lastly, we used known virus proteomes to putatively identify Rh186 from Macacine herpesvirus 3 and ORF1a from Middle East respiratory syndrome-related coronavirus, indicating that mass spectrometry-based techniques show promise for pathogen detection. Overall, these results can be used to design targeted mass-spectrometry assays to quantify immunological markers and detect pathogens. More broadly, our findings also highlight the application of proteomics in advancing wildlife immunology and pathogen surveillance.

Neotropical bat communities are among the most diverse mammal communities in the world, and a better understanding of these assemblages may permit inferences about how so many species coexist. While broad trophic guilds (e.g., frugivore, insectivore) of bats are recognized, details of diet and similarities among species remain largely unknown. We used stable isotope ratios of carbon (δ¹³C) and nitrogen (δ¹⁵N) to characterize the community structure of a diverse Neotropical bat fauna from Belize to test predictions of niche theory and the competitive exclusion principle. We predicted that (1) interspecific variation in isotopic overlap would be greater within guilds than between guilds, and (2) no two sympatric populations would have isotopic niches that overlap completely, unless there is variation along some other axis (e.g., temporal, spatial). We additionally tested body size as an explanatory metric of potential overlap and predicted that larger‐bodied animals would have greater niche breadths. Results suggest that while guild‐level characterizations of communities are at least somewhat informative, there are multiple examples of intra‐ and inter‐guild species pairs with significantly overlapping isotopic niches, suggesting that, counter to predictions, they may compete for resources. Understanding the trophic structure of animal communities is fundamental to conservation and management of endangered species and ecosystems and important for evolutionary studies, and stable isotope analyses can provide key insights as well as informing hypotheses of the diet of species that are not well known. Abstract in Spanish is available with online material.

Cimicid insects, bed bugs and their allies, include about 100 species of blood-feeding ectoparasites. Among them, a few have become widespread and abundant pests of humans. Cimicids vary in their degree of specialization to hosts. Whereas most species specialize on insectivorous birds or bats, the common bed bug can feed on a range of distantly related host species, such as bats, humans, and chickens. We suggest that association with humans and generalism in bed bugs led to fundamentally different living conditions that fostered rapid growth and expansion of their populations. We propose that the evolutionary and ecological success of common bed bugs reflected exploitation of large homeothermic hosts (humans) that sheltered in buildings. This was a departure from congeners whose hosts are much smaller and often heterothermic. We argue that interesting insights into the biology of pest species may be obtained using an integrated view of their ecology and evolution.

As molecular tools for assessing trophic interactions become common, research is increasingly focused on the construction of interaction networks. Here, we demonstrate three key methods for incorporating DNA data into network ecology and discuss analytical considerations using a model consisting of plants, insects, bats and their parasites from the Costa Rica dry forest. The simplest method involves the use of Sanger sequencing to acquire long sequences to validate or refine field identifications, for example of bats and their parasites, where one specimen yields one sequence and one identification. This method can be fully quantified and resolved and these data resemble traditional ecological networks. For more complex taxonomic identifications, we target multiple DNA loci, for example from a seed or fruit pulp sample in faeces. These networks are also well resolved but gene targets vary in resolution and quantification is difficult. Finally, for mixed templates such as faecal contents of insectivorous bats, we use DNA metabarcoding targeting two sequence lengths (157 and 407 bp) of one gene region and a MOTU, BLAST and BIN association approach to resolve nodes. This network type is complex to generate and analyse, and we discuss the implications of this type of resolution on network analysis. Using these data, we construct the first molecular-based network of networks containing 3,304 interactions between 762 nodes of eight trophic functions and involving parasitic, mutualistic and predatory interactions. We provide a comparison of the relative strengths and weaknesses of these data types in network ecology.

Contaminants such as mercury are pervasive and can have immunosuppressive effects on wildlife. Impaired immunity could be important for forecasting pathogen spillover risks, as many land-use changes that generate mercury contamination also bring wildlife into close contact with humans and domestic animals. However, the interactions among contaminants, immunity, and infection are difficult to study in natural systems, and empirical tests of possible directional relationships remain rare.We capitalized on extreme mercury variation in a diverse bat community in Belize to test association among contaminants, immunity, and infection. By comparing a previous dataset of bats sampled in 2014 with new data from 2017, representing a period of rapid agricultural land conversion, we first confirmed bat species more reliant on aquatic prey had higher fur mercury. Bats in the agricultural habitat also had higher mercury in recent years. We then tested covariation between mercury and cellular immunity and determined if such relationships mediated associations between mercury and common bacterial pathogens. As bat ecology can dictate exposure to mercury and pathogens, we also assessed species-specific patterns in mercury–infection relationships.Across the bat community, individuals with higher mercury had fewer neutrophils but not lymphocytes, suggesting stronger associations with innate immunity. However, the odds of infection for hemoplasmas and Bartonella spp. were generally lowest in bats with high mercury, and relationships between mercury and immunity did not mediate infection patterns. Mercury also showed species- and clade-specific relationships with infection, being associated with especially low odds for hemoplasmas in Pteronotus mesoamericanus and Dermanura phaeotis. For Bartonella spp., mercury was associated with particularly low odds in the genus Pteronotus but high odds in the Stenodermatinae.Synthesis and application: Lower general infection risk in bats with high mercury despite weaker innate defense suggests contaminant-driven loss of pathogen habitat (i.e., anemia) or vector mortality as possible causes. Greater attention to these potential pathways could help disentangle relationships among contaminants, immunity, and infection in anthropogenic habitats and help forecast disease risks. Our results also suggest contaminants may increase infection risk in some taxa but not others, emphasizing the importance of considering surveillance and management at different phylogenetic scales.

Bats are increasingly studied as model systems for longevity and as natural hosts for some virulent viruses. Yet our ability to characterize immune mechanisms of viral tolerance and to quantify infection dynamics in wild bats is often limited by small sample volumes and few species-specific reagents. Here, we demonstrate how proteomics can overcome these limitations by using data-independent acquisition-based shotgun proteomics to survey the serum proteome of 17 vampire bats (Desmodus rotundus) from Belize. Using just 2 μL of sample and relatively short separations of undepleted serum digests, we identified 361 proteins across five orders of magnitude. Data are available via ProteomeXchange with identifier PXD022885. Levels of immunological proteins in vampire bat serum were then compared to human plasma via published databases. Of particular interest were anti-viral and anti-bacterial components, circulating 20S proteasome complex, and proteins involved in redox activity; whether any results are specific to vampire bats could be assessed by future pan-mammalian analyses. Lastly, we used known virus proteomes to identify Rh186 from Macacine herpesvirus 3 and ORF1a from Middle East respiratory syndrome-related coronavirus, indicating that mass spectrometry-based techniques show promise for pathogen detection. Overall, these results can be used to design targeted mass-spectrometry assays to quantify immunological markers and detect pathogens. More broadly, our findings also highlight the application of proteomics in advancing wildlife immunology and pathogen surveillance.

Bats are very diverse, including over 1400 species (Simmons and Cirranello 2020), meaning that one in every five living mammal species is a bat. These remarkable animals include species living on every continent except Antarctica. Many of them perform essential ecosystem services including consuming large quantities of insects, dispersing seeds, and pollinating flowers of numerous tropical and subtropical plants including many of economic importance (e.g., durian in southeast Asia, agaves used to make tequila in North America; Kunz et al. 2011). Lamentably, the International Union for the Conservation of Nature Red List (2020) identifies 77 species of bats as Endangered. Most bats are small mammals with low rates of reproduction (typically one or two young per year) and exceptionally long lifespans, with some individuals living over 40 years in the wild (Munshi-South and Wilkinson 2010).

Vaccines that autonomously transfer among individuals have been proposed as a strategy to control infectious diseases within inaccessible wildlife populations. However, rates of vaccine spread and epidemiological efficacy in real-world systems remain elusive. Here, we investigate whether topical vaccines that transfer among individuals through social contacts can control vampire bat rabies-a medically and economically important zoonosis in Latin America. Field experiments in three Peruvian bat colonies, which used fluorescent biomarkers as a proxy for the bat-to-bat transfer and ingestion of an oral vaccine, revealed that vaccine transfer would increase population-level immunity up to 2.6 times beyond the same effort using conventional, non-spreadable vaccines. Mathematical models showed that observed levels of vaccine transfer would reduce the probability, size and duration of rabies outbreaks, even at low but realistically achievable levels of vaccine application. Models further predicted that existing vaccines provide substantial advantages over culling bats-the policy currently implemented in North, Central and South America. Linking field studies with biomarkers to mathematical models can inform how spreadable vaccines may combat pathogens of health and conservation concern before costly investments in vaccine design and testing.

Most emerging pathogens can infect multiple species, underscoring the importance of understanding the ecological and evolutionary factors that allow some hosts to harbor greater infection prevalence and share pathogens with other species. Investigating such factors can inform surveillance efforts and help forecast disease emergence. However, our understanding of pathogen jumps is primarily based around viruses, despite bacteria accounting for the greatest proportion of zoonoses. Because bacterial pathogens in bats (Order: Chiroptera) can have conservation and human health consequences, studies that examine the ecological and evolutionary drivers of bacterial prevalence and barriers to pathogen sharing are crucially needed. We here studied hemotropic Mycoplasma spp. (i.e., hemoplasmas) across a species-rich bat community in Belize over two years. Across 469 bats spanning 33 species, half of individuals and two-thirds of species were hemoplasma positive. Infection prevalence was higher for males, heavier species, and those with larger colony sizes. Hemoplasmas displayed high genetic diversity (21 novel genotypes) and strong host specificity. Evolutionary patterns supported co-divergence of bats and bacterial genotypes alongside phylogenetically constrained host shifts. Bat species centrality to the network of shared hemoplasma genotypes was phylogenetically clustered and unrelated to prevalence, further suggesting rare—but detectable—bacterial sharing between species. Our study highlights the importance of using fine phylogenetic scales when assessing host specificity and suggests phylogenetic similarity may play a key role in host shifts for not only viruses but also bacteria. Such work more broadly contributes to increasing efforts to understand cross-species transmission and epidemiological consequences of bacterial pathogens.

Predation on swarms of prey, especially using visual information, has drawn much interest in studies of collective movement. Surprisingly, in the field of biosonar this aspect of prey detection, which is probably very common, has received little to no attention. Here, we combine computer simulations and actual echo measurements to accurately estimate the echo sound pressure of insect swarms of different size and density. We show that swarm echo sound pressure increases with 3dB for every doubling of insect number, irrespective of swarm density. Thus swarms will be much easier to detect than single insects. Many of the insects bats eat are so small that they are only detectable by echolocation at very short distances. By focusing on detection of swarms of insects, a bat may increase its operating range and diversify its diet. Interestingly, interference between the sound waves reflected from a swarm of insects can sometimes result in echoes that are much weaker than echoes from single insects. We show that bats can reduce this problem by increasing the bandwidth of their echolocation calls. Specifically, a bandwidth of 3–8 kHz would guarantee receiving loud echoes from any angle relative to the swarm. Indeed, many bat species, and specifically bats hunting in open spaces, where swarms are abundant, use echolocation signals with a bandwidth of several kHz. Our results might also explain how the first echolocating bats that probably had limited echolocation abilities, could detect insects through swarm hunting., Author summary When bats hunt, they often encounter insects that fly in swarms. Echolocating bats emit sonar signals to search for prey and it is currently unknown what such swarms look like to a bat. Unlike vision, sonar senses the delay or distance to objects directly. We show that when bats hunt for insects in the sky, the echoes from the insects in a swarm will most of the time sum up and therefore become much louder than the echo of a single insect. Every time an insect swarm would double in number, a bat would hear an echo that is 3dB stronger. This could enable a bat to detect prey from longer distances and some bats might thus profit from swarm hunting. However, the echoes reflected from the many insects in the swarm also create acoustic interference so that sometimes the summed echo is actually weak at a certain frequency. We show how bats could deal with this drawback. It is known that most bats do not use sonar signals with a single tone but that they modulate their tones. Our analysis shows that this modulation can solve the problem of spectral interference ensuring that the swarm-echo is always loud.

Parasite-host relationships create strong selection pressures that can lead to adaptation and increasing specialization of parasites to their hosts. Even in relatively loose host-parasite relationships, such as between generalist ectoparasites and their hosts, we may observe some degree of specialization of parasite populations to one of the multiple potential hosts. Salivary proteins are used by blood-feeding ectoparasites to prevent hemostasis in the host and maximize energy intake. We investigated the influence of association with specific host species on allele frequencies of salivary protein genes in Cimex adjunctus, a generalist blood-feeding ectoparasite of bats in North America. We analysed two salivary protein genes: an apyrase, which hydrolyses ATP at the feeding site and thus inhibits platelet aggregation, and a nitrophorin, which brings nitrous oxide to the feeding site, inhibiting platelet aggregation and vasoconstriction. We observed more variation at both salivary protein genes among parasite populations associated with different host species than among populations from different spatial locations associated with the same host species. The variation in salivary protein genes among populations on different host species was also greater than expected under a neutral scenario of genetic drift and gene flow. Finally, host species was an important predictor of allelic divergence in genotypes of individual C. adjunctus at both salivary protein genes. Our results suggest differing selection pressures on these two salivary protein genes in C. adjunctus depending on the host species.

Subdivided populations can be described by different models of population structure that reflect population organization, dynamics, and connectivity. We used genetic data to investigate population structure in two geographically sympatric, congeneric species of generalist ectoparasites of warm-blooded animals. We characterized the spatial genetic structure of the eastern bat bug (Cimex adjunctus Barber, 1939), an understudied and fairly abundant species, using microsatellite markers at a spatial scale representing contemporary dispersal of the species. We found seven genetic clusters, global [Formula: see text] of 0.2, 33% of genetic variation among sites, and nonsignificant isolation-by-distance. We compared these results with the common bed bug (Cimex lectularius L., 1758), a closely related but conversely well-known species, in the same geographic area. We found stronger genetic structuring in C. lectularius than in C. adjunctus, with 11 genetic clusters, [Formula: see text] of 0.7, 57% of genetic variation among sites, and significant but weak isolation-by-distance (R2= 0.09). These results suggest that while both species can be described as having classic metapopulation structure, C. adjunctus leans more towards a patchy population and C. lectularius leans more towards a nonequilibrium metapopulation. The difference in population structure between these species may be attributable to differences in movement potential and extinction–colonization dynamics.

Predation on swarms of prey, especially using visual information, has drawn much interest in studies of collective movement. Surprisingly, in the field of biosonar this aspect of prey detection, which is probably very common, has received little to no attention. Here, we combine computer simulations and actual echo measurements to accurately estimate the echo intensity of insect swarms of different size and density. We show that swarm echo intensity increases with 3dB for every doubling of insect number, irrespective of swarm density. Thus swarms will be much easier to detect than single insects. Many of the insects bats eat are so small that they are only detectable by echolocation at very short distances. By focusing on detection of swarms of insects, a bat may increase its operating range and diversify its diet. Interestingly, interference between the sound waves reflected from a swarm of insects can sometimes result in echoes that are much much weaker than echoes from single insects. We show that bats can reduce this problem by increasing the bandwidth of their echolocation calls. Specifically, a bandwidth of 3-8 kHz would guarantee receiving loud echoes from any angle relative to the swarm. Indeed, many bat species, and specifically bats hunting in open spaces, where swarms are abundant, use echolocation signals with a bandwidth of several kHz. Our results might also explain how the first echolocating bats that probably had limited echolocation abilities, could detect insects through swarm hunting.

Interspecific differences in traits can alter the relative niche use of species within the same environment. Bats provide an excellent model to study niche use because they use a wide variety of behavioral, acoustic, and morphological traits that may lead to multi‐species, functional groups. Predatory bats have been classified by their foraging location (edge, clutter, open space), ability to use aerial hawking or substrate gleaning and echolocation call design and flexibility, all of which may dictate their prey use. For example, high frequency, broadband calls do not travel far but offer high object resolution while high intensity, low frequency calls travel further but provide lower resolution. Because these behaviors can be flexible, four behavioral categories have been proposed: (a) gleaning, (b) behaviorally flexible (gleaning and hawking), (c) clutter‐tolerant hawking, and (d) open space hawking. Many recent studies of diet in bats use molecular tools to identify prey but mainly focus on one or two species in isolation; few studies provide evidence for substantial differences in prey use despite the many behavioral, acoustic, and morphological differences. Here, we analyze the diet of 17 sympatric species in the Chihuahuan desert and test the hypothesis that peak echolocation frequency and behavioral categories are linked to differences in diet. We find no significant correlation between dietary richness and echolocation peak frequency though it spanned close to 100 kHz across species. Our data, however, suggest that bats which use both gleaning and hawking strategies have the broadest diets and are most differentiated from clutter‐tolerant aerial hawking species.