Modelos de distribución de especies y estado de conservación de murciélagos amenazados en la región tumbesina de Ecuador y Perú / Species distribution models and conservation status of threatened bats in the Tumbesian region of Ecuador and Perú

Resumen Introducción: La biodiversidad se está perdiendo a un ritmo acelerado como resultado del cambio global. Herramientas como los modelos de distribución de especies (MDEs) han sido ampliamente usados para mejorar el conocimiento sobre el estado de conservación de las especies y ayudar a desarrollar estrategias de gestión para mitigar la pérdida de biodiversidad. Objetivo: Determinar cómo la distribución potencial predicha por los MDEs para ocho especies de murciélagos amenazados difiere de los mapas de distribución reportados por la UICN. También, inferir el área de distribución y estado de endemismo de cada especie, y evaluar la importancia de la región tumbesina para su conservación. Métodos: Basados en registros de presencia del rango global de las especies, usamos MDEs para evaluar el estado de conservación de estas ocho especies en la región tumbesina de Ecuador y Perú. Resultados: Las áreas estimadas por los MDEs eran 35-78 % más pequeñas para cuatro especies (Eptesicus innoxius, Lophostoma occidentale, Platalina genovensium y Lonchophylla hesperia) y 26-1 600 % más grandes para tres especies (Amorphochilus schnablii, Promops davisoni y Rhogeessa velilla) que aquellas reportadas por la UICN. Para Tomopeas ravus, el área estimada por el MDE y la UICN fue similar, pero difirió en la distribución espacial. Los MDEs coincidieron con áreas de endemismo informadas por autores previos para E. innoxius, R. velilla y T. ravus, pero fueron diferentes para A. schnablii, P. genovensium, P. davisoni y L. hesperia, debido en parte a las distribuciones proyectadas para estas últimas especies en valles secos interandinos según los MDEs. Conclusiones: La región tumbesina representa una porción significativa (40-96 %) de la distribución predicha de siete de las ocho especies estudiadas, subrayando la importancia de esta región para la conservación de murciélagos. Nuestros resultados muestran las probables distribuciones para estas especies y proporcionan una base importante para identificar vacíos de investigación y desarrollar medidas de conservación para murciélagos amenazados en el punto caliente de biodiversidad de Tumbes.

Abstract Introduction: Biodiversity is being lost at an accelerating rate because of global change. Tools such as species distribution models (SDMs) have been widely used to improve knowledge about species' conservation status and help develop management strategies to mitigate biodiversity loss. SDMs are especially important for species with restricted distributions, such as endemic species. Objective: To determine how potential distribution predicted by SDMs for eight threatened bat species differed from the distribution maps reported by the IUCN. Also, to infer the area of distribution and state of endemism of each specie, and to evaluate the importance of the Tumbesian region for their conservation. Methods: Based on presence records across the species' entire ranges, we used SDMs to assess the conservation status of these eight species in the Tumbesian region of Ecuador and Peru. Results: The areas estimated by SDMs were 35-78 % smaller for four species (Eptesicus innoxius, Lophostoma occidentale, Platalina genovensium and Lonchophylla hesperia) and 26-1 600 % larger for three species (Amorphochilus schnablii, Promops davisoni and Rhogeessa velilla) than those reported by the IUCN. For Tomopeas ravus, the area estimated by the SDM and IUCN was similar but differed in spatial distribution. SDMs coincided with areas of endemism reported by previous authors for E. innoxius, R. velilla, and T. ravus, but were different for A. schnablii, P. genovensium, P. davisoni, and L. hesperia, due in part to projected distributions for these latter species in dry inter-Andean valleys according to the SDMs. Conclusions: The Tumbesian region represents a significant portion (40-96 %) of the predicted distribution of seven of the eight species studied, underscoring the importance of this region for bat conservation. Our results show likely distributions for these species and provide an important basis for identifying research gaps and developing conservation measures for threatened bats in the Tumbes biodiversity hotspot.

Mapping the distribution of Nipah virus infections: a geospatial modelling analysis.

BACKGROUND: Nipah virus is a zoonotic paramyxovirus responsible for disease outbreaks with high fatality rates in south and southeast Asia. However, knowledge of the potential geographical extent and risk patterns of the virus is poor. We aimed to establish an integrated spatiotemporal and phylogenetic database of Nipah virus infections in humans and animals across south and southeast Asia. METHODS: In this geospatial modelling analysis, we developed an integrated database containing information on the distribution of Nipah virus infections in humans and animals from 1998 to 2021. We conducted phylodynamic analysis to examine the evolution and migration pathways of the virus and meta-analyses to estimate the adjusted case-fatality rate. We used two boosted regression tree models to identify the potential ecological drivers of Nipah virus occurrences in spillover events and endemic areas, and mapped potential risk areas for Nipah virus endemicity. FINDINGS: 749 people and eight bat species across nine countries were documented as being infected with Nipah virus. On the basis of 66 complete genomes of the virus, we identified two clades-the Bangladesh clade and the Malaysia clade-with the time of the most recent common ancestor estimated to be 1863. Adjusted case-fatality rates varied widely between countries and were higher for the Bangladesh clade than for the Malaysia clade. Multivariable meta-regression analysis revealed significant relationships between case-fatality rate estimates and viral clade (p=0·0021), source country (p=0·016), proportion of male patients (p=0·036), and travel time to health-care facilities (p=0·036). Temperature-related bioclimate variables and the probability of occurrence of Pteropus medius were important contributors to both the spillover and the endemic infection models. INTERPRETATION: The suitable niches for Nipah virus are more extensive than previously reported. Future surveillance efforts should focus on high-risk areas informed by updated projections. Specifically, intensifying zoonotic surveillance efforts, enhancing laboratory testing capacity, and implementing public health education in projected high-risk areas where no human cases have been reported to date will be crucial. Additionally, strengthening wildlife surveillance and investigating potential modes of transmission in regions with documented human cases is needed. FUNDING: The Key Research and Development Program of China.

Animal cognition: Time mapping in the wild.

Foraging involves searching for resources distributed in space and time with varying nutritional values. New research suggests that free-ranging wild fruit bats track tree phenology, implicating the use of spatio-temporal mental maps.

A chemo-mechanical constitutive model for muscle activation in bat wing skins.

Birds, bats and insects have evolved unique wing structures to achieve a wide range of flight capabilities. Insects have relatively stiff and passive wings, birds have a complex and hierarchical feathered structure and bats have an articulated skeletal system integrated with a highly stretchable skin. The compliant skin of the wing distinguishes bats from all other flying animals and contributes to bats' remarkable, highly manoeuvrable flight performance and high energetic efficiency. The structural and functional complexity of the bat wing skin is one of the least understood although important elements of the bat flight anatomy. The wing skin has two unusual features: a discrete array of very soft elastin fibres and a discrete array of skeletal muscle fibres. The latter is intriguing because skeletal muscle is typically attached to bone, so the arrangement of intramembranous muscle in soft skin raises questions about its role in flight. In this paper, we develop a multi-scale chemo-mechanical constitutive model for bat wing skin. The chemo-mechanical model links cross-bridge cycling to a structure-based continuum model that describes the active viscoelastic behaviour of the soft anisotropic skin tissue. Continuum models at the tissue length-scale are valuable as they are easily implemented in commercial finite element codes to solve problems involving complex geometries, loading and boundary conditions. The constitutive model presented in this paper will be used in detailed finite element simulations to improve our understanding of the mechanics of bat flight in the context of wing kinematics and aerodynamic performance.

Heart rate monitoring reveals differential seasonal energetic trade-offs in male noctule bats.

Understanding how animals meet their daily energy requirements is critical in our rapidly changing world. Small organisms with high metabolic rates can conserve stored energy when food availability is low or increase energy intake when energetic requirements are high, but how they balance this in the wild remains largely unknown. Using miniaturized heart rate transmitters, we continuously quantified energy expenditure, torpor use and foraging behaviour of free-ranging male bats (Nyctalus noctula) in spring and summer. In spring, bats used torpor extensively, characterized by lowered heart rates and consequently low energy expenditures. In contrast, in summer, bats consistently avoided torpor, even though they could have used this low-energy mode. As a consequence, daytime heart rates in summer were three times as high compared with the heart rates in spring. Daily energy use increased by 42% during summer, despite lower thermogenesis costs at higher ambient temperatures. Likely, as a consequence, bats nearly doubled their foraging duration. Overall, our results indicate that summer torpor avoidance, beneficial for sperm production and self-maintenance, comes with a high energetic cost. The ability to identify and monitor such vulnerable energetic life-history stages is particularly important to predict how species will deal with increasing temperatures and changes in their resource landscapes.

Torpor use in the wild by one of the world's largest bats.

Torpor is widespread among bats presumably because most species are small, and torpor greatly reduces their high mass-specific resting energy expenditure, especially in the cold. Torpor has not been recorded in any bat species larger than 50 g, yet in theory could be beneficial even in the world's largest bats (flying-foxes; Pteropus spp.) that are exposed to adverse environmental conditions causing energy bottlenecks. We used temperature telemetry to measure body temperature in wild-living adult male grey-headed flying-foxes (P. poliocephalus; 799 g) during winter in southern Australia. We found that all individuals used torpor while day-roosting, with minimum body temperature reaching 27°C. Torpor was recorded following a period of cool, wet and windy weather, and on a day with the coldest maximum air temperature, suggesting it is an adaptation to reduce energy expenditure during periods of increased thermoregulatory costs and depleted body energy stores. A capacity for torpor among flying-foxes has implications for understanding their distribution, behavioural ecology and life history. Furthermore, our discovery increases the body mass of bats known to use torpor by more than tenfold and extends the documented use of this energy-saving strategy under wild conditions to all bat superfamilies, with implications for the evolutionary maintenance of torpor among bats and other mammals.

Activity of DNA Repair Systems in the Cells of Long-Lived Rodents and Bats.

Damages of various origin accumulated in the genomic DNA can lead to the breach of genome stability, and are considered to be one of the main factors involved in cellular senescence. DNA repair systems in mammalian cells ensure effective damage removal and repair of the genome structure, therefore, activity of these systems is expected to be correlated with high maximum lifespan observed in the long-lived mammals. This review discusses current results of the studies focused on determination of the DNA repair system activity and investigation of the properties of its key regulatory proteins in the cells of long-lived rodents and bats. Based on the works discussed in the review, it could be concluded that the long-lived rodents and bats in general demonstrate high efficiency in functioning and regulation of DNA repair systems. Nevertheless, a number of questions around the study of DNA repair in the cells of long-lived rodents and bats remain poorly understood, answers to which could open up new avenues for further research.

Characterisation of germline progenitor cells in the testes of phylostomid bats: Artibeus jamaicensis and Sturnira lilium.

Context A population of sperm progenitor cells, known as Asingle spermatogonia, has been described in mammalian testes. During division cycles in spermatogenesis, some cells will form part of the Asingle spermatogonia group, while others form primary spermatocytes. Thus, during spermatogenesis, spermatogonia are the progenitor cells of spermatozoa. Aims In this study, we characterise the spermatogonial stem cells (SSCs) in the testicles of Artibeus jamaicensis and Sturnira lilium bats. The knowledge generated from this will contribute to the understanding of the biology of germ cells and the mechanisms of spermatogenesis in mammals, generating information on wildlife species that are important for biodiversity. Methods Testes were analysed by light and electron microscopy. Likewise, the expression of specific factors of stem cells (Oct4 and C-kit), germ cells (Vasa), cell proliferation (pH3 and SCP1) and testicular somatic cells (MIS, 3ßHSD and Sox9) was characterised by immunofluorescence and western blot. Key results The histological analysis enabled the location of type Asingle, Apaired and Aaligned spermatogonia in the periphery of the seminiferous tubules adjacent to Sertoli cells. The expression of genes of stem and germ cells made it possible to corroborate the distribution of the SSCs. Conclusions Results indicate that type Asingle spermatogonia were not randomly distributed, since proliferative activity was detected in groups of cells adjacent to the seminiferous tubules membrane, suggesting the localisation of spermatogonial niches in a specific region of testes. Implications This study provides evidence for the existence of SSCs in the testis of chiropterans that contribute to the renewal of germline progenitor cells to maintain the reproduction of the organisms.

Pathogenic strategies of Pseudogymnoascus destructans during torpor and arousal of hibernating bats.

Millions of hibernating bats across North America have died from white-nose syndrome (WNS), an emerging disease caused by a psychrophilic (cold-loving) fungus, Pseudogymnoascus destructans, that invades their skin. Mechanisms of P. destructans invasion of bat epidermis remain obscure. Guided by our in vivo observations, we modeled hibernation with a newly generated little brown bat (Myotis lucifugus) keratinocyte cell line. We uncovered the stealth intracellular lifestyle of P. destructans, which inhibits apoptosis of keratinocytes and spreads through the cells by two epidermal growth factor receptor (EGFR)-dependent mechanisms: active penetration during torpor and induced endocytosis during arousal. Melanin of endocytosed P. destructans blocks endolysosomal maturation, facilitating P. destructans survival and germination after return to torpor. Blockade of EGFR aborts P. destructans entry into keratinocytes.

Adaptive fungal invasion of bat cells.

A fungus uses different cell entry strategies, depending on its host's hibernation status.

Coronaviruses (Coronaviridae) of bats in the northern Caucasus and south of western Siberia.

INTRODUCTION: Bats are natural reservoirs of coronaviruses (Coronaviridae), which have caused three outbreaks of human disease SARS, MERS and COVID-19 or SARS-2 over the past decade. The purpose of the work is to study the diversity of coronaviruses among bats inhabiting the foothills and mountainous areas of the Republics of Dagestan, Altai and the Kemerovo region. MATERIALS AND METHODS: Samples of bat oral swabs and feces were tested for the presence of coronavirus RNA by reverse transcription-polymerase chain reaction (RT-PCR). RESULTS: It has been shown that the greater horseshoe bats (Rhinolophus ferrumequinum), inhabiting the Republic of Dagestan, are carriers of two different coronaviruses. One of the two coronaviruses is a member of the Sarbecovius subgenus of the Betacoronavirus genus, which includes the causative agents of SARS and COVID-19. The second coronavirus is assigned to the Decacovirus subgenus of the Alphacoronavirus genus and is most similar to viruses identified among Rhinolophus spp. from European and Middle Eastern countries. In the Altai Republic and Kemerovo region, coronaviruses belonging to the genus Alphacoronavirus, subgenus Pedacovirus, were found in the smooth-nosed bats: Ikonnikov`s bat (Myotis ikonnikovi) and the eastern bat (Myotis petax). The virus from the Altai Republic from M. ikonnikovi is close to viruses from Japan and Korea, as well as viruses from Myotis spp. from European countries. The virus from the Kemerovo region from M. petax groups with coronaviruses from Myotis spp. from Asian countries and is significantly different from coronaviruses previously discovered in the same natural host.

A wingless fly on a winged mammal: host-parasite dynamics between Basilia travassosi (Diptera: Nycteribiidae) and Myotis lavali (Chiroptera: Vespertilionidae).

Nycteribiidae encompasses a specialized group of wingless blood-sucking flies that parasitize bats worldwide. Such relationships are frequently species- or genus-specific, indicating unique eco-evolutionary processes. However, despite this significance, comprehensive studies on the relationships of these flies with their hosts, particularly in the New World, have been scarce. Here, we provide a detailed description of the parasitological patterns of nycteribiid flies infesting a population of Myotis lavali bats in the Atlantic Forest of northeastern Brazil, considering the potential influence of biotic and abiotic factors on the establishment of nycteribiids on bat hosts. From July 2014 to June 2015, we captured 165 M. lavali bats and collected 390 Basilia travassosi flies. Notably, B. travassosi displayed a high prevalence and was the exclusive fly species parasitizing M. lavali in the surveyed area. Moreover, there was a significant predominance of female flies, indicating a female-biased pattern. The distribution pattern of the flies was aggregated; most hosts exhibited minimal or no parasitism, while a minority displayed heavy infestation. Sexually active male bats exhibited greater susceptibility to parasitism compared to their inactive counterparts, possibly due to behavioral changes during the peak reproductive period. We observed a greater prevalence and abundance of flies during the rainy season, coinciding with the peak reproductive phase of the host species. No obvious correlation was observed between the parasite load and bat body mass. Our findings shed light on the intricate dynamics of nycteribiid-bat interactions and emphasize the importance of considering various factors when exploring bat-parasite associations.

Parameter estimation of the hyperbolic frequency-modulated bat calls using hyperbolic scale transform.

Echolocating bats are known to vary their waveforms at the phases of searching, approaching, and capturing the prey. It is meaningful to estimate the parameters of the calls for bat species identification and the technological improvements of the synthetic systems, such as radar and sonar. The type of bat calls is species-related, and many calls can be modeled as hyperbolic frequency- modulated (HFM) signals. To obtain the parameters of the HFM-modeled bat calls, a reversible integral transform, i.e., hyperbolic scale transform (HST), is proposed to transform a call into two-dimensional peaks in the "delay-scale" domain, based on which harmonic separation and parameter estimation are realized. Compared with the methods based on time-frequency analysis, the HST-based method does not need to extract the instantaneous frequency of the bat calls, only searching for peaks. The verification results show that the HST is suitable for analyzing the HFM-modeled bat calls containing multiple harmonics with a large energy difference, and the estimated parameters imply that the use of the waveforms from the searching phase to the capturing phase is beneficial to reduce the ranging bias, and the trends in parameters may be useful for bat species identification.

Different species of Chiroptera: Immune cells and molecules.

The distinct composition and immune response characteristics of bats' innate and adaptive immune systems, which enable them to serve as host of numerous serious zoonotic viruses without falling ill, differ substantially from those of other mammals, it have garnered significant attention. In this article, we offer a systematic review of the names, attributes, and functions of innate and adaptive immune cells & molecules across different bat species. This includes descriptions of the differences shown by research between 71 bat species in 10 families, as well as comparisons between bats and other mammals. Studies of the immune cells & molecules of different bat species are necessary to understand the unique antiviral immunity of bats. By providing comprehensive information on these unique immune responses, it is hoped that new insights will be provided for the study of co-evolutionary dynamics between viruses and the bat immune system, as well as human antiviral immunity.

Temperature sensitivity of bat antibodies links metabolic state of bats with antigen-recognition diversity.

The bat immune system features multiple unique properties such as dampened inflammatory responses and increased tissue protection, explaining their long lifespan and tolerance to viral infections. Here, we demonstrated that body temperature fluctuations corresponding to different physiological states in bats exert a large impact on their antibody repertoires. At elevated temperatures typical for flight, IgG from the bat species Myotis myotis and Nyctalus noctula show elevated antigen binding strength and diversity, recognizing both pathogen-derived antigens and autoantigens. The opposite is observed at temperatures reflecting inactive physiological states. IgG antibodies of human and other mammals, or antibodies of birds do not appear to behave in a similar way. Importantly, diversification of bat antibody specificities results in preferential recognition of damaged endothelial and epithelial cells, indicating an anti-inflammatory function. The temperature-sensitivity of bat antibodies is mediated by the variable regions of immunoglobulin molecules. Additionally, we uncover specific molecular features of bat IgG, such as low thermodynamic stability and implication of hydrophobic interactions in antigen binding as well as high prevalence of polyreactivity. Overall, our results extend the understanding of bat tolerance to disease and inflammation and highlight the link between metabolism and immunity.

Unraveling genomic features and phylogenomics through the analysis of three Mexican endemic Myotis genomes.

Background: Genomic resource development for non-model organisms is rapidly progressing, seeking to uncover molecular mechanisms and evolutionary adaptations enabling thriving in diverse environments. Limited genomic data for bat species hinder insights into their evolutionary processes, particularly within the diverse Myotis genus of the Vespertilionidae family. In Mexico, 15 Myotis species exist, with three-M. vivesi, M. findleyi, and M. planiceps-being endemic and of conservation concern. Methods: We obtained samples of Myotis vivesi, M. findleyi, and M. planiceps for genomic analysis. Each of three genomic DNA was extracted, sequenced, and assembled. The scaffolding was carried out utilizing the M. yumanensis genome via a genome-referenced approach within the ntJoin program. GapCloser was employed to fill gaps. Repeat elements were characterized, and gene prediction was done via ab initio and homology methods with MAKER pipeline. Functional annotation involved InterproScan, BLASTp, and KEGG. Non-coding RNAs were annotated with INFERNAL, and tRNAscan-SE. Orthologous genes were clustered using Orthofinder, and a phylogenomic tree was reconstructed using IQ-TREE. Results: We present genome assemblies of these endemic species using Illumina NovaSeq 6000, each exceeding 2.0 Gb, with over 90% representing single-copy genes according to BUSCO analyses. Transposable elements, including LINEs and SINEs, constitute over 30% of each genome. Helitrons, consistent with Vespertilionids, were identified. Values around 20,000 genes from each of the three assemblies were derived from gene annotation and their correlation with specific functions. Comparative analysis of orthologs among eight Myotis species revealed 20,820 groups, with 4,789 being single copy orthogroups. Non-coding RNA elements were annotated. Phylogenomic tree analysis supported evolutionary chiropterans' relationships. These resources contribute significantly to understanding gene evolution, diversification patterns, and aiding conservation efforts for these endangered bat species.

SARS-CoV-2 envelope protein-derived extracellular vesicles act as potential media for viral spillover.

Extracellular vesicles (EVs) are shown to be a novel viral transmission model capable of increasing a virus's tropism. According to our earlier research, cells infected with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) or transfected with envelope protein plasmids generate a novel type of EVs that are micrometer-sized and able to encase virus particles. Here, we showed the capacity of these EVs to invade various animals both in vitro and in vivo independent of the angiotensin-converting enzyme 2 receptor. First, via macropinocytosis, intact EVs produced from Vero E6 (monkey) cells were able to enter cells from a variety of animals, including cats, dogs, bats, hamsters, and minks, and vice versa. Second, when given to zebrafish with cutaneous wounds, the EVs showed favorable stability in aqueous environments and entered the fish. Moreover, infection of wild-type (WT) mice with heterogeneous EVs carrying SARS-CoV-2 particles led to a strong cytokine response and a notable amount of lung damage. Conversely, free viral particles did not infect WT mice. These results highlight the variety of processes behind viral transmission and cross-species evolution by indicating that EVs may be possible vehicles for SARS-CoV-2 spillover and raising risk concerns over EVs' potential for viral gene transfer.

A social foraging trade-off in echolocating bats reveals that they benefit from some conspecifics but are impaired when many are around.

Social foraging is very common in the animal kingdom. Numerous studies have documented collective foraging in various species and many reported the attraction of various species to foraging conspecifics. It is nonetheless difficult to quantify the benefits and costs of collective foraging, especially in the wild. We examined the benefits and costs of social foraging using on-board microphones mounted on freely foraging Molossus nigricans bats. This allowed us to quantify the bats' attacks on prey and to assess their success as a function of conspecific density. We found that the bats spent most of their time foraging at low conspecific densities, during which their attacks were most successful in terms of prey items captured per time unit. Notably, their capture rate dropped when conspecific density became either too high or too low. Our findings thus demonstrate a clear social foraging trade-off in which the presence of a few conspecifics probably improves foraging success, whereas the presence of too many impairs it.

Myotis bat STING attenuates aging-related inflammation in female mice.

Bats, notable as the only flying mammals, serve as natural reservoir hosts for various highly pathogenic viruses in humans (e.g., SARS-CoV and Ebola virus). Furthermore, bats exhibit an unparalleled longevity among mammals relative to their size, particularly the Myotis bats, which can live up to 40 years. However, the mechanisms underlying these distinctive traits remain incompletely understood. In our prior research, we demonstrated that bats exhibit dampened STING-interferon activation, potentially conferring upon them the capacity to mitigate virus- or aging-induced inflammation. To substantiate this hypothesis, we established the first in vivo bat-mouse model for aging studies by integrating Myotis davidii bat STING ( MdSTING) into the mouse genome. We monitored the genotypes of these mice and performed a longitudinal comparative transcriptomic analysis on MdSTING and wild-type mice over a 3-year aging process. Blood transcriptomic analysis indicated a reduction in aging-related inflammation in female MdSTING mice, as evidenced by significantly lower levels of pro-inflammatory cytokines and chemokines, immunopathology, and neutrophil recruitment in aged female MdSTING mice compared to aged wild-type mice in vivo. These results indicated that MdSTING knock-in attenuates the aging-related inflammatory response and may also improve the healthspan in mice in a sex-dependent manner. Although the underlying mechanism awaits further study, this research has critical implications for bat longevity research, potentially contributing to our comprehension of healthy aging in humans.