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In the past two decades, there has been a dramatic increase in research on bat-associated viruses and other microbes. Here, we synthesize the main themes and topics from a conference symposium focused on advances in the research of bats and their microbes, including physiological, immunological, ecological, and epidemiological research that has improved our understanding of bat health and infectious disease transmission. We present priority areas for bat health and disease research at the individual, population, and community levels, and outline critical gaps and opportunities for future bat pathogen research., 2020 - 2022 (July) data download from WoS

Bats face diverse challenges that cause global bat population declines, including habitat loss and roost disturbance. Additionally, negative perceptions of bats and their potential role in several zoonotic diseases have led to actions against bats. We documented existing knowledge and perception of bats through interviews with 151 participants of fifteen tribes in Northern Uganda in 2020 and conducted a sensitization campaign that prevented planned actions against bats. The interviews revealed distinct firm beliefs, negative perceptions, limited knowledge on bats, and the influence of media in shaping actions against bats. In addition, modified landscapes and habitat loss increased encounters and subsequent deterioration of relations between humans and bats. Targeted threats towards bats were exacerbated by public misinformation during the SARS-CoV-2 pandemic. No deliberate conservation efforts exist, and negative perception largely hampers the implementation of bat conservation in Northern Uganda. Importantly, the study also demonstrates that sensitization campaigns can be effective tools to protect bats in the short term. Regular sensitizations and education are recommended for sustainable changes in attitudes to and coexistence with bats.

The general guidance is, and has always been, that handling bats should be avoided, particularly by the general public, but capturing and handling bats is often unavoidable for bat researchers. While bat researchers are aware of the potential for zoonotic pathogen transmission to occur when handling bats, most notably Rabies virus, some do not wear any (or insufficient) personal protective equipment (PPE) to reduce risks of exposure. This lack of adherence to even minimal biosafety practices may jeopardize both the safety of the bat and the handler. Such concerns became more pressing with the COVID-19 pandemic, but also had been raised as a result of previous outbreaks of human infections linked to contact with animals. The largely unknown potential for handled bats to become infected by a bat researcher, something not previously considered by most field workers, is now widely known in the research community due to the efforts of the IUCN SSC Bat Specialist Group and the Global Union of Bat Diversity Networks (GBatNet). It is also worth noting that the negative framing of bats during the pandemic may have serious consequences for bat conservation (Lopez-Baucells et al. 2017) and a refocusing of the conversation on the deficiencies of human interactions with bats would be a preferable direction. After all, bats are an important component of global ecosystems and provide many ecosystem services to humans (Kunz et al. 2011). Several bat-specific conservation groups have developed guidelines on how to safely handle bats to prevent anthropozoonotic transmission, including the IUCN SSC Bat Specialist Group (Nunez et al. 2020), the Bat Conservation Trust (Anonymous 2020), the Latin American and Caribbean Network for the Conservation of Bats (Suarez-Alvarez and Lopez-Berrizbeitia 2020) and Worksafe Queensland (Paterson 2016). These guidelines largely focus on the increased use of PPE, such as leather or nitrile/latex gloves, respirator masks, long sleeves and long trousers and protective eyewear or face shield, depending on the situation. These build on earlier PPE protocols deployed by some research groups to mitigate the risk of exposure to potential bat pathogens. Given the recent developments, we were interested to know if the use of PPE, in particular wearing gloves, has improved and whether we could detect a change by screening pictures of bats uploaded to iNaturalist. Clearly, it is not possible to evaluate the full adherance to bat handling guidlines, but we believe that use of gloves is a good indicator that best practices are being followed. iNaturalist is a mobile phone app for recording occurrences of wildlife and a social network for amateur and professional naturalists alike. It has about 100,000 to 300,000 active users and tens of thousands of observations of wildlife are recorded each day. On iNaturalist, most observations are evidenced by a picture of the organism. This allows the species to be identified, if possible, or verified by users who have the expertise, but also provides the context of the photograph as well. That context can show what the organism is doing, what developmental stage it is, what the habitat is or how it was photographed, such as whether a person is holding the organism. In our case, we wanted to verify whether people who were handling bats were wearing gloves and to determine whether there has recently been a change in behaviour (i.e. frequency of bat handlers wearing gloves).

Domestic and captive animals and cultivated plants should be recognised as integral components in contemporary ecosystems. They interact with wild organisms through such mechanisms as hybridization, predation, herbivory, competition and disease transmission and, in many cases, define ecosystem properties. Nevertheless, it is widespread practice for data on domestic, captive and cultivated organisms to be excluded from biodiversity repositories, such as natural history collections. Furthermore, there is a lack of integration of data collected about biodiversity in disciplines, such as agriculture, veterinary science, epidemiology and invasion science. Discipline-specific data are often intentionally excluded from integrative databases in order to maintain the “purity” of data on natural processes. Rather than being beneficial, we argue that this practise of data exclusivity greatly limits the utility of discipline-specific data for applications ranging from agricultural pest management to invasion biology, infectious disease prevention and community ecology. This problem can be resolved by data providers using standards to indicate whether the observed organism is of wild or domestic origin and by integrating their data with other biodiversity data (e.g. in the Global Biodiversity Information Facility). Doing so will enable efforts to integrate the full panorama of biodiversity knowledge across related disciplines to tackle pressing societal questions.

Abstract Resistance and tolerance allow organisms to cope with potentially life-threatening pathogens. Recently introduced pathogens initially induce resistance responses, but natural selection favors the development of tolerance, allowing for a commensal relationship to evolve. Mycosis by Pseudogymnoascus destructans, causing white-nose syndrome (WNS) in Nearctic hibernating bats, has resulted in population declines since 2006. The pathogen, which spread from Europe, has infected species of Palearctic Myotis for a longer period. We compared ecologically relevant responses to the fungal infection in the susceptible Nearctic M. lucifugus and less susceptible Palearctic M. myotis, to uncover factors contributing to survival differences in the two species. Samples were collected from euthermic bats during arousal from hibernation, a naturally occurring phenomenon, during which transcriptional responses are activated. We compared the whole-transcriptome responses in wild bats infected with P. destructans hibernating in their natural habitat. Our results show dramatically different local transcriptional responses to the pathogen between uninfected and infected samples from the two species. Whereas we found 1526 significantly upregulated or downregulated transcripts in infected M. lucifugus, only one transcript was downregulated in M. myotis. The upregulated response pathways in M. lucifugus include immune cell activation and migration, and inflammatory pathways, indicative of an unsuccessful attempt to resist the infection. In contrast, M. myotis appears to tolerate P. destructans infection by not activating a transcriptional response. These host-microbe interactions determine pathology, contributing to WNS susceptibility, or commensalism, promoting tolerance to fungal colonization during hibernation that favors survival. Graphic abstract

Connecting basic data about bats and other potential hosts of SARS-CoV-2 with their ecological context is crucial to the understanding of the emergence and spread of the virus. However, when lockdowns in many countries started in March, 2020, the world's bat experts were locked out of their research laboratories, which in turn impeded access to large volumes of offline ecological and taxonomic data. Pandemic lockdowns have brought to attention the long-standing problem of so-called biological dark data: data that are published, but disconnected from digital knowledge resources and thus unavailable for high-throughput analysis. Knowledge of host-to-virus ecological interactions will be biased until this challenge is addressed. In this Viewpoint, we outline two viable solutions: first, in the short term, to interconnect published data about host organisms, viruses, and other pathogens; and second, to shift the publishing framework beyond unstructured text (the so-called PDF prison) to labelled networks of digital knowledge. As the indexing system for biodiversity data, biological taxonomy is foundational to both solutions. Building digitally connected knowledge graphs of host-pathogen interactions will establish the agility needed to quickly identify reservoir hosts of novel zoonoses, allow for more robust predictions of emergence, and thereby strengthen human and planetary health systems. ispartof: LANCET PLANETARY HEALTH vol:5 issue:10 pages:E746-E750 ispartof: location:Netherlands status: published

Despite being nearly 10 months into the COVID-19 (coronavirus disease 2019) pandemic, the definitive animal host for SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2), the causal agent of COVID-19, remains unknown. Unfortunately, similar problems exist for other betacoronaviruses, and no vouchered specimens exist to corroborate host species identification for most of these pathogens., Despite being nearly 10 months into the COVID-19 (coronavirus disease 2019) pandemic, the definitive animal host for SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2), the causal agent of COVID-19, remains unknown. Unfortunately, similar problems exist for other betacoronaviruses, and no vouchered specimens exist to corroborate host species identification for most of these pathogens. This most basic information is critical to the full understanding and mitigation of emerging zoonotic diseases. To overcome this hurdle, we recommend that host-pathogen researchers adopt vouchering practices and collaborate with natural history collections to permanently archive microbiological samples and host specimens. Vouchered specimens and associated samples provide both repeatability and extension to host-pathogen studies, and using them mobilizes a large workforce (i.e., biodiversity scientists) to assist in pandemic preparedness. We review several well-known examples that successfully integrate host-pathogen research with natural history collections (e.g., yellow fever, hantaviruses, helminths). However, vouchering remains an underutilized practice in such studies. Using an online survey, we assessed vouchering practices used by microbiologists (e.g., bacteriologists, parasitologists, virologists) in host-pathogen research. A much greater number of respondents permanently archive microbiological samples than archive host specimens, and less than half of respondents voucher host specimens from which microbiological samples were lethally collected. To foster collaborations between microbiologists and natural history collections, we provide recommendations for integrating vouchering techniques and archiving of microbiological samples into host-pathogen studies. This integrative approach exemplifies the premise underlying One Health initiatives, providing critical infrastructure for addressing related issues ranging from public health to global climate change and the biodiversity crisis.

A deep irony of COVID-19 likely originating from a bat-borne coronavirus (Boni et al. 2020) is that the global lockdown to quell the pandemic also locked up physical access to much basic knowledge regarding bat biology. Digital access to data on the ecology, geography, and taxonomy of potential viral reservoirs, from Southeast Asian horseshoe bats and pangolins to North American deer mice, was suddenly critical for understanding the disease's emergence and spread. However, much of this information lay inside rare books and personal files rather than as open, linked, and queryable resources on the internet. Even the world's experts on mammal taxonomy and zoonotic disease could not retrieve their data from shuttered laboratories. We were caught unprepared. Why, in this digitally connected age, were such fundamental data describing life on Earth not already freely accessible online? Understanding why biodiversity science was unprepared—and how to fix it before the next pandemic—has been the focus of our COVID-19 Taskforce since April 2020 and is continuing (organized by CETAF and DiSSCo). We are a group of museum-based and academic scientists with the goal of opening the rich ecological data stored in natural history collections to the research public. This information is rooted in what may seem an unlikely location—taxonomic names and their historical usages, which are the keys for searching literature and extracting linked ecological data (Fig. 1). This has been the core motivation of our group, enabled by the pioneering efforts of Plazi (Agosti and Egloff 2009) to build tools for literature digitization, extraction, and parsing (e.g., Synospecies, Ocellus) without which biodiversity science would be even less prepared. Our group led efforts to build an additional pipeline from Plazi to the Biodiversity Literature Repository at Zenodo, a free and unlimited data repository (Agosti et al. 2019), and then to GloBI, an open-source database of biotic interactions (Poelen et al. 2014, GloBI 2020). We also developed a direct integration from Pensoft Journals to GloBI, leveraging that publisher’s indexing of computer-readable terms (called semantic metadata; Senderov et al. 2018) to extract mammal host and virus information. Overall, considerable progress was made. In total, 85,492 new interactions were added to GloBI from 14 April to 21 May 2020 (see entire dataset on Zenodo: Poelen et al. 2020). Of those, 28,839 interactions are present when subset to "hasHost", "hostOf", "pathogenOf", "virus", and 4,101 unique name combinations are present after considering mammal species synonymies (from Meyer et al. 2015). Of those interactions, 892 species of mammals and 1,530 unique virus names are involved, which compares to 754 mammals and 586 viruses in the most recent data synthesis (Olival et al. 2017). While these liberated data may still include redundancies, they demonstrate the value of our approach and the expanse of known but digitally unconnected data that remains locked in publications. We can liberate host-virus data from publications, but doing so is expensive and does not scale to the continued influx of new articles that are inadequately digitized. Our efforts make it clear that Pensoft-style semantic publishing should be expanded to all major journals. The pandemic has created an opportunity for re-thinking the way we do science in the digital age. Thankfully, our future is not the past, so we do not have to keep wasting resources to digitially 'rediscover' biodiversity knowledge. We collectively call for changes to the publishing paradigm, so that research findings are directly accessible, citable, discoverable, and reusable for creating complete forms of digital knowledge.

The COVID-19 pandemic highlights the substantial public health, economic, and societal consequences of virus spillover from a wildlife reservoir. Widespread human transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) also presents a new set of challenges when considering viral spillover from people to naïve wildlife and other animal populations. The establishment of new wildlife reservoirs for SARS-CoV-2 would further complicate public health control measures and could lead to wildlife health and conservation impacts. Given the likely bat origin of SARS-CoV-2 and related beta-coronaviruses (β-CoVs), free-ranging bats are a key group of concern for spillover from humans back to wildlife. Here, we review the diversity and natural host range of β-CoVs in bats and examine the risk of humans inadvertently infecting free-ranging bats with SARS-CoV-2. Our review of the global distribution and host range of β-CoV evolutionary lineages suggests that 40+ species of temperate-zone North American bats could be immunologically naïve and susceptible to infection by SARS-CoV-2. We highlight an urgent need to proactively connect the wellbeing of human and wildlife health during the current pandemic and to implement new tools to continue wildlife research while avoiding potentially severe health and conservation impacts of SARS-CoV-2 "spilling back" into free-ranging bat populations.

ispartof: Bioscience vol:70 issue:7 pages:531-534 status: published

Novel pathogens can cause massive declines in populations, and even extirpation of hosts. But disease can also act as a selective pressure on survivors, driving the evolution of resistance or tolerance. Bat white-nose syndrome (WNS) is a rapidly spreading wildlife disease in North America. The fungus causing the disease invades skin tissues of hibernating bats, resulting in disruption of hibernation behavior, premature energy depletion, and subsequent death. We used whole-genome sequencing to investigate changes in allele frequencies within a population of Myotis lucifugus in eastern North America to search for genetic resistance to WNS. Our results show low FST values within the population across time, i.e., prior to WNS (Pre-WNS) compared to the population that has survived WNS (Post-WNS). However, when dividing the population with a geographical cut-off between the states of Pennsylvania and New York, a sharp increase in values on scaffold GL429776 is evident in the Post-WNS samples. Genes present in the diverged area are associated with thermoregulation and promotion of brown fat production. Thus, although WNS may not have subjected the entire M. lucifugus population to selective pressure, it may have selected for specific alleles in Pennsylvania through decreased gene flow within the population. However, the persistence of remnant sub-populations in the aftermath of WNS is likely due to multiple factors in bat life history.

Hibernation, the use of prolonged torpor to depress metabolism, is employed by mammals to conserve resources during extended periods of extreme temperatures and/or resource limitation. Mammalian hibernators arouse to euthermy periodically during torpor for reasons that are not well understood, and these arousals may facilitate immune processes. To determine whether arousals enable host responses to pathogens, we used dual RNA-Seq and a paired sampling approach to examine gene expression in a hibernating bat, the little brown myotis (Myotis lucifugus). During torpor, transcript levels differed in only a few genes between uninfected wing tissue and adjacent tissue infected with Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome. Within 70-80 min after emergence from torpor, large changes in gene expression were observed due to local infection, particularly in genes involved in pro-inflammatory host responses to fungal pathogens, but also in many genes involved in immune responses and metabolism. These results support the hypothesis that torpor is a period of relative immune dormancy and arousals allow for local immune responses in infected tissues during hibernation. Host-pathogen interactions were also found to regulate gene expression in the pathogen differently depending on the torpor state of the host. Hibernating species must balance the benefits of energy and water conservation achieved during torpor with the costs of decreased immune competence. Interbout arousals allow hibernators to optimize these, and other, trade-offs during prolonged hibernation by enabling host responses to pathogens within brief, periodic episodes of euthermy.

White nose syndrome (WNS) is caused by the psychrophilic fungus Pseudogymnoascus destructans that can grow in the environment saprotrophically or parasitically by infecting hibernating bats. Infections are pathological in many species of North American bats, disrupting hibernation and causing mortality. To determine what fungal pathways are involved in infection of living tissue, we examined fungal gene expression using RNA-Seq. We compared P. destructans gene expression when grown in culture to that during infection of a North American bat species, Myotis lucifugus, that shows high WNS mortality. Cultured P. destructans was grown at 10 to 14 C and P. destructans growing in vivo was presumably exposed to temperatures ranging from 4 to 8 C during torpor and up to 37 C during periodic arousals. We found that when P. destructans is causing WNS, the most significant differentially expressed genes were involved in heat shock responses, cell wall remodeling, and micronutrient acquisition. These results indicate that this fungal pathogen responds to host-pathogen interactions by regulating gene expression in ways that may contribute to evasion of host responses. Alterations in fungal cell wall structures could allow P. destructans to avoid detection by host pattern recognition receptors and antibody responses. This study has also identified several fungal pathways upregulated during WNS infection that may be candidates for mitigating infection pathology. By identifying host-specific pathogen responses, these observations have important implications for host-pathogen evolutionary relationships in WNS and other fungal diseases.

The devastating bat fungal disease, white-nose syndrome (WNS), does not appear to affect all species equally. To experimentally determine susceptibility differences between species, we exposed hibernating naïve little brown myotis (Myotis lucifugus) and big brown bats (Eptesicus fuscus) to the fungus that causes WNS, Pseudogymnoascus destructans (Pd). After hibernating under identical conditions, Pd lesions were significantly more prevalent and more severe in little brown myotis. This species difference in pathology correlates with susceptibility to WNS in the wild and suggests that survival is related to different host physiological responses. We observed another fungal infection, associated with neutrophilic inflammation, that was equally present in all bats. This suggests that both species are capable of generating a response to cold tolerant fungi and that Pd may have evolved mechanisms for evading host responses that are effective in at least some bat species. These host-pathogen interactions are likely mediated not just by host physiological responses, but also by host behavior. Pd-exposed big brown bats, the less affected species, spent more time in torpor than did control animals, while little brown myotis did not exhibit this change. This differential thermoregulatory response to Pd infection by big brown bat hosts may allow for a more effective (or less pathological) immune response to tissue invasion.

Candidatus Bartonella mayotimonensis was detected in 2010 from an aortic valve sample of a patient with endocarditis from Iowa, the United States of America. The environmental source of the potentially new endocarditis-causing Bartonella remained elusive. We set out to study the prevalence and diversity of bat-associated Bartonella in North America. During 2015, mist nets and harp traps were used to capture 92 bats belonging to two species: little brown myotis (Myotis lucifugus Le Conte 1831, n = 73) and the gray myotis (M. grisescens A.H. Howell 1909, n = 19) in Kentucky, Michigan, Pennsylvania, and Tennessee. DNA preparations of peripheral blood samples from bats were subjected to a three-marker (gltA, rpoB, and intergenic spacer region [ISR]) multilocus sequence analysis. Sequence-verified gltA-positive PCR amplicons were obtained from nine samples. Three sequences were 99.7-100% identical with the gltA sequence of the Iowa endocarditis patient strain. Analysis of rpoB and ISR sequences demonstrated that one little brown myotis sample from the Upper Peninsula of Michigan contained Bartonella DNA, with 100% sequence identity with the Iowa endocarditis patient strain DNA. It appears possible that bats are a reservoir of Candidatus Bartonella mayotimonensis in North America.

Novel pathogens can cause massive declines in populations, and even extirpation of hosts. But disease can also act as a selective pressure on survivors, driving the evolution of resistance or tolerance. Bat white-nose syndrome (WNS) is a rapidly spreading wildlife disease in North America. The fungus causing the disease invades skin tissues of hibernating bats, resulting in disruption of hibernation behavior, premature energy depletion, and subsequent death. We used whole-genome sequencing to investigate changes in allele frequencies within a population ofMyotis lucifugusin eastern North America to search for genetic resistance to WNS. Our results show low FSTvalues within the population across time, i.e. prior to WNS (Pre-WNS) compared to the population that has survived WNS (Post-WNS). However, when dividing the population with a geographical cut-off between the states of Pennsylvania and New York, a sharp increase in values on scaffold GL429776 is evident in the Post-WNS samples. Genes present in the diverged area are associated with thermoregulation and promotion of brown fat production. Thus, although WNS may not have subjected the entireM. lucifuguspopulation to selective pressure, it may have selected for specific alleles in Pennsylvania through decreased gene flow within the population. However, the persistence of remnant sub-populations in the aftermath of WNS is likely due to multiple factors in bat life history.

The price of staying warm Among vertebrates, zebrafish and salamanders can regenerate their hearts, whereas adult mice and humans cannot. Hirose et al. analyzed diploid cardiomyocyte frequency as a proxy for cardiac regenerative potential across 41 vertebrate species (see the Perspective by Marchianò and Murry). They observed an inverse correlation of these cells with thyroid hormone concentrations during the ectotherm-to-endotherm transition. Mice with defects in thyroid hormone signaling retained significant heart regenerative capacity, whereas zebrafish exposed to excessive thyroid hormones exhibit impaired cardiac repair. Loss of heart regenerative ability in mammals may represent a trade-off for increases in metabolism necessary for the development of endothermy. Science , this issue p. 184 ; see also p. 123

Several house bat specimens superficially resembling the white-bellied house bat Scotophilus leucogaster (Cretzschmar, 1830), were recently captured in southwestern Ethiopia and southern South Sudan. These S . cf. leucogaster differed from typical S. leucogaster by their slightly smaller size and ventral coloration, conforming instead with the original description of S . altilis Allen, 1914. Scotophilus altilis is an overlooked taxon known from the Blue Nile region in Sudan that is currently considered a junior synonym of S . leucogaster . Phylogenetic analysis of mitochondrial cytochrome b gene ( cytb ) sequences revealed S . cf. leucogaster as a sister clade to S . leucogaster with a genetic distance of ca. 10%. Comparative specimens of questionable S . nigritellus de Winton, 1899 from northwestern Ethiopia and a wing biopsy sample of another S . cf. leucogaster from western Kenya also fell within this clade. Sequence data from two nuclear markers ( zfy and fgb7 ) corroborated the distinction of S . cf. leucogaster from S . leucogaster . Likewise, morphometric analysis of cranial data largely supported this distinction, as well as taxonomic affiliation with S . altilis based on comparison with the only available paratype specimen. The position of this paratype specimen within the new Scotophilus clade, inferred from analysis of a short fragment of cytb , confirmed its taxonomic identity. Based on the presented evidence, the overlooked East African taxon S. altilis should be resurrected as a full species within the genus Scotophilus .

Despite being heavily exploited, pangolins (Pholidota: Manidae) have been subject to limited research, resulting in a lack of reliable population estimates and standardised survey methods for the eight extant species. Camera trapping represents a unique opportunity for broad-scale collaborative species monitoring due to its largely nondiscriminatory nature, which creates considerable volumes of data on a relatively wide range of species. This has the potential to shed light on the ecology of rare, cryptic and understudied taxa, with implications for conservation decision-making. We undertook a global analysis of available pangolin data from camera trapping studies across their range in Africa and Asia. Our aims were (1) to assess the utility of existing camera trapping efforts as a method for monitoring pangolin populations, and (2) to gain insights into the distribution and ecology of pangolins. We analysed data collated from 103 camera trap surveys undertaken across 22 countries that fell within the range of seven of the eight pangolin species, which yielded more than half a million trap nights and 888 pangolin encounters. We ran occupancy analyses on three species (Sunda pangolin Manis javanica, white-bellied pangolin Phataginus tricuspis and giant pangolin Smutsia gigantea). Detection probabilities varied with forest cover and levels of human influence for P. tricuspis, but were low (

Classifications and phylogenies of perceived natural entities change in the light of new evidence. Taxonomic changes, translated into Code-compliant names, frequently lead to name:meaning dissociations across succeeding treatments. Classification standards such as the Mammal Species of the World (MSW) may experience significant levels of taxonomic change from one edition to the next, with potential costs to long-term, large-scale information integration. This circumstance challenges the biodiversity and phylogenetic data communities to express taxonomic congruence and incongruence in ways that both humans and machines can process, that is, to logically represent taxonomic alignments across multiple classifications. We demonstrate that such alignments are feasible for two classifications of primates corresponding to the second and third MSW editions. Our approach has three main components: (i) use of taxonomic concept labels, that is name sec. author (where sec. means according to), to assemble each concept hierarchy separately via parent/child relationships; (ii) articulation of select concepts across the two hierarchies with user-provided Region Connection Calculus (RCC-5) relationships; and (iii) the use of an Answer Set Programming toolkit to infer and visualize logically consistent alignments of these input constraints. Our use case entails the Primates sec. Groves (1993; MSW2-317 taxonomic concepts; 233 at the species level) and Primates sec. Groves (2005; MSW3-483 taxonomic concepts; 376 at the species level). Using 402 RCC-5 input articulations, the reasoning process yields a single, consistent alignment and 153,111 Maximally Informative Relations that constitute a comprehensive meaning resolution map for every concept pair in the Primates sec. MSW2/MSW3. The complete alignment, and various partitions thereof, facilitate quantitative analyses of name:meaning dissociation, revealing that nearly one in three taxonomic names are not reliable across treatments-in the sense of the same name identifying congruent taxonomic meanings. The RCC-5 alignment approach is potentially widely applicable in systematics and can achieve scalable, precise resolution of semantically evolving name usages in synthetic, next-generation biodiversity, and phylogeny data platforms.

Additional ethical issues surrounding wildlife research compared with biomedical research include consideration of the harm of research to the ecosystem as a whole and the benefits of conservation to the same species of animals under study. Research on white-nose syndrome in bats provides a case study to apply these considerations to determine whether research that harms ecosystems under crisis is justified. By expanding well-established guidelines for animal and human subjects research, we demonstrate that this research can be considered highly justified. Studies must minimize the amount of harm to the ecosystem while maximizing the knowledge gained. However, the likelihood of direct application of the results of the research for conservation should not necessarily take priority over other considerations, particularly when the entire context of the ecologic disaster is poorly understood. Since the emergence of white-nose syndrome, researchers have made great strides in understanding this panzootic disease and are now in a position to utilize this knowledge to mitigate this wildlife crisis.

Host responses to infection with novel pathogens are costly and require trade-offs among physiologic systems. One such pathogen is the fungus Pseudogymnoascus destructans (Pd) that causes white-nose syndrome (WNS) and has led to mass mortality of hibernating bats in eastern North America. Although infection with Pd does not always result in death, we hypothesized that bats that survive infection suffer significant consequences that negatively impact the ability of females to reproduce. To understand the physiologic consequences of surviving infection with Pd, we assessed differences in wing damage, mass-specific resting metabolic rate, and reproductive rate between little brown myotis ( Myotis lucifugus) that survived a winter in captivity after inoculation with Pd (WNS survivors) and comparable, uninfected bats. Survivors of WNS had significantly more damaged wing tissue and displayed elevated mass-specific metabolic rates compared with Pd-uninfected bats after emergence from hibernation. The WNS survivors and Pd-uninfected bats did not significantly differ in their reproductive capacity, at least in captivity. However, our metabolic data demonstrated greater energetic costs during spring in WNS survivors compared with uninfected bats, which may have led to other consequences for postpartum fitness. We suggest that, after surviving the energetic constraints of winter, temperate hibernating bats infected with Pd faced a second energetic bottleneck after emerging from hibernation.

In August 2012, a wildlife biologist became ill immediately following a 6-wk field trip to collect bats and rodents in South Sudan and Uganda. After returning to the US, the biologist was admitted to the hospital with multiple symptoms including fever, malaise, headache, generalized myalgia and arthralgia, stiffness in the neck, and sore throat. Soon after admission, the patient developed a maculopapular rash and oropharynx ulcerations. The patient remained hospitalized for 14 d. Several suspect pathogens, including viral hemorrhagic fever viruses such as Ebola viruses and Marburg viruses, were ruled out through standard diagnostic testing. However, deep sequencing and metagenomic analyses identified a novel paramyxovirus, later named Sosuga virus, in the patient’s blood. To determine the potential source, bat tissues collected during the 3-wk period just prior to the onset of symptoms were tested for Sosuga virus, and several Egyptian rousette bats (Rousettus aegyptiacus) were found to be positive. Further analysis of archived Egyptian rousette tissues collected at other localities in Uganda found additional Sosuga virus–positive bats, suggesting this species could be a potential natural reservoir for this novel paramyxovirus.

White-nose syndrome (WNS) is a fungal disease caused by Pseudogymnoascus destructans (Pd) that affects bats during hibernation. Although millions of bats have died from WNS in North America, mass mortality has not been observed among European bats infected by the fungus, leading to the suggestion that bats in Europe are immune. We tested the hypothesis that an antibody-mediated immune response can provide protection against WNS by quantifying antibodies reactive to Pd in blood samples from seven species of free-ranging bats in North America and two free-ranging species in Europe. We also quantified antibodies in blood samples from little brown myotis (Myotis lucifugus) that were part of a captive colony that we injected with live Pd spores mixed with adjuvant, as well as individuals surviving a captive Pd infection trial. Seroprevalence of antibodies against Pd, as well as antibody titers, was greater among little brown myotis than among four other species of cave-hibernating bats in North America, including species with markedly lower WNS mortality rates. Among little brown myotis, the greatest titers occurred in populations occupying regions with longer histories of WNS, where bats lacked secondary symptoms of WNS. We detected antibodies cross-reactive with Pd among little brown myotis naïve to the fungus. We observed high titers among captive little brown myotis injected with Pd. We did not detect antibodies against Pd in Pd-infected European bats during winter, and titers during the active season were lower than among little brown myotis. These results show that antibody-mediated immunity cannot explain survival of European bats infected with Pd and that little brown myotis respond differently to Pd than species with higher WNS survival rates. Although it appears that some species of bats in North America may be developing resistance to WNS, an antibody-mediated immune response does not provide an explanation for these remnant populations.

Parasitic protozoan parasites have evolved many co-evolutionary paths towards stable transmission to their host population. Plasmodium spp., the causative agents of malaria, and related haemosporidian parasites are dipteran-borne eukaryotic pathogens that actively invade and use vertebrate erythrocytes for gametogenesis and asexual development, often resulting in substantial morbidity and mortality of the infected hosts. Here, we present results of a survey of insectivorous bats from tropical Africa, including new isolates of species of the haemosporidian genus Nycteria. A hallmark of these parasites is their capacity to infect bat species of distinct families of the two evolutionary distant chiropteran suborders. We did detect Nycteria parasites in both rhinolophid and nycterid bat hosts in geographically separate areas of Sub-Saharan Africa, however our molecular phylogenetic analyses support the separation of the parasites into two distinct clades corresponding to their host genera, suggestive of ancient co-divergence and low levels of host switching. For one clade of these parasites, cytochrome b genes could not be amplified and cytochrome oxidase I sequences showed unusually high rates of evolution, suggesting that the mitochondrial genome of these parasites may have either been lost or substantially altered. This haemosporidian parasite-mammalian host system also highlights that sequential population expansion in the liver and gametocyte formation is a successful alternative to intermediate erythrocytic replication cycles.

Reduced space can lead to crowding in social animals. Crowding increases the risk of agonistic interactions that, in turn, may require additional physiological defensive coping mechanisms affecting health. To determine the stress induced from increased social density in a group of nineteen baboons living in an indoor/outdoor enclosure, saliva cortisol levels and rates of anxiety-related behavior were analyzed across two unique crowding episodes. Initially, mean salivary cortisol levels when animals were restricted to their indoor quarters were compared to those when they also had access to their larger outdoor enclosure. Then, mean cortisol levels were compared before, during, and after two distinct crowding periods of long and short duration. Crowding resulted in significantly elevated cortisol during crowding periods compared to non-crowded periods. Cortisol levels returned to baseline following two crowding episodes contrasting in their length and ambient climate conditions. These cortisol elevations indicate greater metabolic costs of maintaining homeostasis under social stress resulting from reduced space. Self-directed behavior, conversely, was not reliably elevated during crowding. Results suggest that the potential for negative social interactions, and/or the uncertainty associated with social threat can cause physiological stress responses detected by salivary cortisol. Self-directed behavioral measures of stress may constitute inadequate indicators of social stress in colony-housed monkeys or represent subjective emotional arousal unrelated to hypothalamic-pituitary adrenal axis activation. Am. J. Primatol. 77:462–467, 2015. © 2015 Wiley Periodicals, Inc.