The effect of ambient temperature on the arousal frequency of the hibernating Greater horseshoe bat, Rhinolophus fermmequinum, in relation to site selection and the hibernation state

Undisturbed hibernating Greater horseshoe bats were studied over three winters to find the effect of temperature on arousal frequency, timing of arousals and the selection of a hibernation site. The study showed that temperature is important in all three aspects and the ability to select a temperature zone accurately is an important factor in the survival of hibernation by a bat.
The arousal frequency falls with falling ambient temperature then seems to rise again below 6°C. There is a clear seasonal effect, bats waking up on average once a day at 10.5°C in winter compared with 8.5°C in spring. An arousal frequency of once in six days occurs at 8°C in winter compared with 6°C in spring. This shift of 2°C is compensated for by a shift of 2°C in temperature selection by the bats in relation to the same external climatic temperatures on the day of arousal. It appears that bats may select the temperature zone which, if prolonged, will result in the most advantageous arousal frequency in relation to feeding experiences.
The seasonal effect discovered indicates that inhibition of the arousal process is important in hibernation and a hormone is postulated.     

Going, going, gone: the impact of white-nose syndrome on the summer activity of the little brown bat (Myotis lucifugus)

Since its discovery in the winter of 2005-2006, white-nose syndrome (WNS) has killed over one million little brown bats (Myotis lucifugus) in the American northeast. Although many studies have reported die-offs of bats at winter hibernacula, it is important to understand how bat mortality linked to WNS at winter hibernacula affects bat activity levels in their summer ranges. In the summer (May-August) of 2007, 2008 and 2009, we recorded echolocation calls to determine bat activity at sites along the Hudson River, NY (within approx. 100 km of where WNS was first reported). We documented a 78 per cent decline in the summer activity of M. lucifugus, coinciding with the arrival and spread of WNS. We suggest that mortality of M. lucifugus in winter hibernacula is reflected by reduced levels of activity in the summer and that WNS affects the entire bat population of an area, and not only individual hibernacula.     

Emergence activity at hibernacula differs among four bat species affected by white‐nose syndrome

Prior to the introduction of white‐nose syndrome (WNS) to North America, temperate bats were thought to remain within hibernacula throughout most of the winter. However, recent research has shown that bats in the southeastern United States emerge regularly from hibernation and are active on the landscape, regardless of their WNS status. The relationship between winter activity and susceptibility to WNS has yet to be explored but warrants attention, as it may enable managers to implement targeted management for WNS‐affected species. We investigated this relationship by implanting 1346 passive integrated transponder (PIT) tags in four species that vary in their susceptibility to WNS. Based on PIT‐tag detections, three species entered hibernation from late October to early November. Bats were active at hibernacula entrances on days when midpoint temperatures ranged from −1.94 to 22.78°C (mean midpoint temperature = 8.70 ± 0.33°C). Eastern small‐footed bats (Myotis leibii), a species with low susceptibility to WNS, were active throughout winter, with a significant decrease in activity in mid‐hibernation (December 16 to February 15). Tricolored bats (Perimyotis subflavus), a species that is highly susceptible to WNS, exhibited an increase in activity beginning in mid‐hibernation and extending through late hibernation (February 16 to March 31). Indiana bats (M. sodalis), a species determined to have a medium–high susceptibility to WNS, remained on the landscape into early hibernation (November 1 to December 15), after which we did not record any again until the latter portion of mid‐hibernation. Finally, gray bats (M. grisescens), another species with low susceptibility to WNS, maintained low but regular levels of activity throughout winter. Given these results, we determined that emergence activity from hibernacula during winter is highly variable among bat species and our data will assist wildlife managers to make informed decisions regarding the timing of implementation of species‐specific conservation actions.     

Changes in hibernating tricolored bat (Perimyotis subflavus) roosting behavior in response to white‐nose syndrome

Understanding animals'' behavioral and physiological responses to pathogenic diseases is critical for management and conservation. One such disease, white‐nose syndrome (WNS), has greatly affected bat populations throughout eastern North America leading to significant population declines in several species. Although tricolored bat (Perimyotis subflavus) populations have experienced significant declines, little research has been conducted on their responses to the disease, particularly in the southeastern United States. Our objective was to document changes in tricolored bat roost site use after the appearance of WNS in a hibernaculum in the southeastern U.S. and relate these to microsite temperatures, ambient conditions, and population trends. We censused a tricolored bat hibernaculum in northwestern South Carolina, USA, once each year between February 26 and March 2, 2014–2021, and recorded species, section of the tunnel, distance from the entrance, and wall temperature next to each bat. The number of tricolored bats in the hibernaculum dropped by 90.3% during the first 3 years after the arrival of WNS. However, numbers stabilized and slightly increased from 2018 to 2021. Prior to the arrival of WNS, 95.6% of tricolored bats roosted in the back portion of the tunnel that was the warmest. After the arrival of WNS, we observed a significant increase in the proportion of bats using the front, colder portions of the tunnel, particularly during the period of population stabilization and increase. Roost temperatures of bats were also positively associated with February external temperatures. Our results suggest that greater use of the colder sections of the tunnel by tricolored bats could have led to increased survival due to slower growth rates of the fungus that causes WNS in colder temperatures or decreased energetic costs associated with colder hibernation temperatures. Thus, management actions that provide cold hibernacula may be an option for long‐term management of hibernacula, particularly in southern regions.     

Winter behavior of bats and the progression of white‐nose syndrome in the southeastern United States

Understanding the winter behavior of bats in temperate North America can provide insight into how bats react to perturbations caused by natural disturbances such as weather, human‐induced disturbances, or the introduction of disease. This study measured the activity patterns of bats outside of their hibernaculum and asked how this winter activity varied by time, temperature, bat species, body condition, and WNS status. Over the course of three winters (2011–2013), we collected acoustic data and captured bats outside of five hibernacula in Tennessee, United States. During this time, Pseudogymnoascus destructans, the causative agent of white‐nose syndrome, became established in hibernacula throughout the region, allowing us to track disease‐related changes in the winter behavior of ten bat species. We determined that bats in the southeastern United States were active during winter regardless of disease. We recorded activity outside of hibernacula at temperatures as low as ?13°C. Although bat activity was best determined by a combination of variables, the strongest factor was mean daily temperature (R ² = .2879, F _1,1450 = 586.2, p  < .0001). Bats that left the hibernacula earlier in evening had lower body condition than those that left 2–4 hr after sunset (F _7,932 = 7.225, p  < .0001, Tukey HSD, p  < .05). The number of daytime emergences from hibernacula, as determined via acoustic detection, increased the longer a site was P. destructans positive (F _{3,17 808} = 124.48, p  < .0001, Tukey HSD, p  < .05). Through the use of passive acoustic monitoring and monthly captures, we determined that winter activity was driven by both ambient temperature and the presence of P. destructans .     

Hibernacula microclimate and declines in overwintering bats during an outbreak of white‐nose syndrome near the northern range limit of infection in North America

We document white‐nose syndrome (WNS), a lethal disease of bats caused by the fungus Pseudogymnoascus destructans (Pd), and hibernacula microclimate in New Brunswick, Canada. Our study area represents a more northern region than is common for hibernacula microclimate investigations, providing insight as to how WNS may impact bats at higher latitudes. To determine the impact of the March 2011 arrival of Pd in New Brunswick and the role of hibernacula microclimate on overwintering bat mortality, we surveyed bat numbers at hibernacula twice a year from 2009 to 2015. We also collected data from iButton temperature loggers deployed at all sites and data from HOBO temperature and humidity loggers at three sites. Bat species found in New Brunswick hibernacula include Myotis lucifugus (Little Brown Bat) and M. septentrionalis (Northern Long‐eared Bat), with small numbers of Perimyotis subflavus (Tricolored Bat). All known hibernacula in the province were Pd‐positive with WNS‐positive bats by winter 2013. A 99% decrease in the overwintering bat population in New Brunswick was observed between 2011 and 2015. We did not observe P. subflavus during surveys 2013–2015 and the species appears to be extirpated from these sites. Bats did not appear to choose hibernacula based on winter temperatures, but dark zone (zone where no light penetrates) winter temperatures did not differ among our study sites. Winter dark zone temperatures were warmer and less variable than entrance or above ground temperatures. We observed visible Pd growth on hibernating bats in New Brunswick during early winter surveys (November), even though hibernacula temperatures were colder than optimum for in vitro Pd growth. This suggests that cold hibernacula temperatures encountered near the apparent northern range limit for Pd do not sufficiently slow fungal growth to prevent the onset of WNS and associated bat mortality over the winter.     

Winter diet analysis in Rhinolophus euryale (Chiroptera)

We investigated the winter food of Mediterranean horseshoe bats (Rhinolophus euryale) in four winter cave roosts in southern Slovakia and northern Hungary and investigated the relationship between food and ambient temperature. The bats were active during the whole winter period and they produced excrement throughout the entire hibernation period, even when outside temperatures dropped below zero. The guano was in two forms, containing (1) prey items and (2) non-prey items. The identifiable items belonged to lepidopteran species, but only one was identified, on the basis of the genital fragments, the moth Colotois pennaria, which was the main prey species in autumn and early winter. Our results shed light on the extraordinarily high level of activity in this bat species during winter hibernation, which in temperate regions is a strategy that enables bats to survive when prey is reduced or absent. In R. euryale, the torpor in the course of hibernation is not continuous and our results help to explain how energy losses caused by bat movements are covered.     

Winter Versus Summer Habitat Selection in a Threatened Ground Squirrel

Hibernation is a strategy many species employ to survive periods of thermal stress or resource shortage (e.g., harsh thermal conditions, food limitations) and habitat requirements of hibernating species may differ between summer (the active season) and winter (during hibernation). Accounting for seasonal differences in habitat affinities will help ensure that management actions are more beneficial and land-use policies are more appropriate. The northern Idaho ground squirrel (Urocitellus brunneus) is a federally listed threatened species that is in decline and hibernates for approximately 8 months per year. We collared northern Idaho ground squirrels in Adams County, Idaho from 2013–2017. The majority of northern Idaho ground squirrels we collared selected hibernacula outside of the areas they used during the active season. Furthermore, habitat features of hibernacula locations differed from habitat features of active-season areas. Hibernacula locations had greater canopy closure compared to active-season locations (36.9% and 7.0% canopy closure, respectively) and hibernaculum habitat features (particularly distance to nearest log) influenced overwinter survival. Our results suggest that recovery efforts for northern Idaho ground squirrels should include protection and management for the full range of habitat conditions used throughout summer and winter. More broadly, we emphasize the need to identify and protect habitat during all seasons because habitat requirements can differ substantially during different portions of an animal's annual cycle and effective conservation will require management of year-round habitat needs. © 2020 The Wildlife Society.     

Comparison of Brain Transcriptome of the Greater Horseshoe Bats (Rhinolophus ferrumequinum) in Active and Torpid Episodes

Hibernation is an energy-saving strategy which is widely adopted by heterothermic mammals to survive in the harsh environment. The greater horseshoe bat (Rhinolophus ferrumequinum) can hibernate for a long period in the hibernation season. However, the global gene expression changes between hibernation and non-hibernation season in the greater horseshoe bat remain largely unknown. We herein reported a comprehensive survey of differential gene expression in the brain between winter hibernating and summer active greater horseshoe bats using next-generation sequencing technology. A total of 90,314,174 reads were generated and we identified 1,573 differentially expressed genes between active and torpid states. Interestingly, we found that differentially expressed genes are over-represented in some GO categories (such as metabolic suppression, cellular stress responses and oxidative stress), which suggests neuroprotective strategies might play an important role in hibernation control mechanisms. Our results determined to what extent the brain tissue of the greater horseshoe bats differ in gene expression between summer active and winter hibernating states and provided comprehensive insights into the adaptive mechanisms of bat hibernation.     

Migratory behaviour of the Schreiber's bat: when, where and why do cave bats migrate in a Mediterranean region?

Regional migrations are important elements of the biology of bats, but remain poorly understood. We obtained a large dataset of recoveries of ringed Miniopterus schreibersii to study the patterns and drivers of migration of a Mediterranean cave-dwelling bat. In spite of the mildness of Mediterranean winters, in average years bats hibernated, and few movements were recorded during this period. After hibernation, females migrated to spring roosts, and again to maternity roosts just before parturition. This late arrival at nurseries could be a strategy to avoid a harmful build-up of parasites. Soon after the juveniles were weaned, the mothers migrated to the roosts where they spent autumn and sometimes also winter. Juveniles remained in the warm nurseries longer, presumably because high roost temperatures speed up growth. The pattern of migration of males was similar to that of females, but they left hibernacula later and remained more mobile during the maternity season. They also arrived at the hibernacula later, possibly because they needed time to build up fat stores after the energetically costly mating season. Maternity colonies spent the yearly cycle in well-defined home ranges (mean=19 030 km²), which overlapped greatly. Bats were furthest from the maternity sites during hibernation, but even then 80% remained within 90 km of them. Each hibernaculum attracted bats from multiple nurseries, from within a mean range of 10 770 km². We tested two potential drivers for migration – temperature in the roosts and at the foraging areas – but our results supported only the first one. Bats migrated to reach the roosts most thermally suited for each phase of their life cycle, indicating that roost temperature and associated metabolic advantages are key drivers for regional migrations of cave-dwelling bats.     

Anticipating white‐nose syndrome in the Southern Hemisphere: Widespread conditions favourable to Pseudogymnoascus destructans pose a serious risk to Australia's bat fauna

There is a serious concern that white‐nose syndrome (WNS), a fungal disease causing severe population declines in North American bats, could soon threaten bats on the Australian continent. Despite an ‘almost certain' risk of incursion within the next ten years, and high virulence in naïve bat populations, we remain uncertain about the vulnerability of Australian bats to WNS. In this study, we intersected occurrences for the 27 cave roosting bat species in Australia with interpolated data on mean annual surface temperature, which provides a proxy for thermal conditions within a cave and hence its suitability for growth by the fungal pathogen Pseudogymnoascus destructans. Our analysis identifies favourable roost thermal conditions within 30–100% of the ranges of eight bat species across south‐eastern Australia, including for seven species already listed as threatened with extinction. These results demonstrate the potential for widespread exposure to P. destructans and suggest that WNS could pose a serious risk to the conservation of Australia's bat fauna. The impacts of exposure to P. destructans will depend, however, on the sensitivity of bats to developing WNS, and a more comprehensive vulnerability assessment is currently prevented by a lack of information on the hibernation biology of Australian bats. Thus, given the clear potential for widespread exposure of Australia's bats to P. destructans demonstrated by our study, two specific policy actions seem justified: (i) urgent implementation of border controls that identify and decontaminate cave‐associated fomites and (ii) dedicated funding to enable research on key aspects of bat winter behaviour and hibernation physiology. Further, as accidental translocation of this fungus could also pose a risk to other naïve bat faunas in cooler regions of southern Africa and South America, we argue that a proactive, globally coordinated approach is required to understand and mitigate the potential impacts of WNS spreading to Southern Hemisphere bats.     

A decade of hibernating bat communities along the periphery of a region of white-nose syndrome

Long-term monitoring programs are necessary to assess populations for conservation planning and management decisions. Hibernating bats in North America have declined because of numerous natural and human-induced disturbances. White-nose syndrome (WNS) has become the most serious threat to North American cave-dwelling bats, leading to significant population declines in several species. We examined trends in hibernating bat populations at 11 hibernacula in northern Georgia and Alabama, USA, from 2013–2022, beginning when WNS was first detected in the region. Although we observed interannual variation in numbers of the federally endangered gray bat (Myotis grisescens), mean counts remained stable over time. In contrast, the tricolored bat (Perimyotis subflavus) and the federally endangered northern long-eared bat (M. septentrionalis) declined by >90% in the first 5 years after WNS detection in the region. Although no northern long-eared bats have been reported since 2019, tricolored bat counts stabilized following initial declines. Understanding changes in bat populations as WNS continues to spread, and determining the extent of population declines, is necessary for making appropriate management decisions. Our findings elucidate the status of cave-dwelling bat species along the periphery of the white-nose syndrome endemic region and highlight the importance of monitoring bat communities on a regional scale to develop effective conservation strategies.     

Estimating the spatial distribution of wintering little brown bat populations in the eastern United States

Depicting the spatial distribution of wildlife species is an important first step in developing management and conservation programs for particular species. Accurate representation of a species distribution is important for predicting the effects of climate change, land‐use change, management activities, disease, and other landscape‐level processes on wildlife populations. We developed models to estimate the spatial distribution of little brown bat (Myotis lucifugus) wintering populations in the United States east of the 100th meridian, based on known hibernacula locations. From this data, we developed several scenarios of wintering population counts per county that incorporated uncertainty in the spatial distribution of the hibernacula as well as uncertainty in the size of the current little brown bat population. We assessed the variability in our results resulting from effects of uncertainty. Despite considerable uncertainty in the known locations of overwintering little brown bats in the eastern United States, we believe that models accurately depicting the effects of the uncertainty are useful for making management decisions as these models are a coherent organization of the best available information.     

The trans-boundary importance of artificial bat hibernacula in managed European forests

Many European migratory bat species hibernate in large hollow trees, a decreasing resource in present day silviculture. Here, we report on the importance of man-made hibernacula to support trans-boundary populations of noctule bats (Nyctalus noctula), a species that performs seasonal long distance movements throughout Europe. In winter, we surveyed nine bat roosts (eight artificial and one natural) in Germany and collected small tufts of fur from a total of 608 individuals. We then measured the stable isotope ratios of the non-exchangeable hydrogen in fur keratin and estimated the origin of migrants using a refined isoscape origin model that included information on expected flight distances and migration directions. According to the stable isotope signature, 78 % of hibernating bats originated from local populations. The remaining 22 % of hibernacula occupants originated from distant populations, mostly from places in northern or eastern countries such as Sweden, Poland and Baltic countries. Our results confirm that many noctule bats cross one or several political borders during migration. Data on the breeding origin of hibernating noctule bats also suggest that artificial roosts may not only be important for local but also for distant populations. Protection of natural and artificial hibernacula in managed forests may support the trans-boundary populations of migratory bats when hollow trees are scarce in managed forests.     

中国蝙蝠生物学研究进展及其保护对策

自2019年末,新冠肺炎的全球大流行使蝙蝠（翼手目动物）倍受关注,甚至人们“谈蝠色变”。蝙蝠在生态和分类上多样性极高,占哺乳动物种类的20%左右。蝙蝠不仅在害虫控制、种子传播、植物授粉等方面具有重要的生态作用和经济价值,也在健康长寿、生物仿生和语言进化等方面具有重要的科研价值。中国是全世界蝙蝠物种多样性最丰富的国家之一,已知的物种超过了140种。近几十年来,中国学者在蝙蝠分类学、生态学、行为学、进化生物学、神经生物学和病毒病源学等研究领域取得了丰硕的成果,然而涉及蝙蝠的生态系统服务和资源保护的相关研究比较少。由于生境退化、过度捕杀、栖息地破坏、城市化、杀虫剂使用、气候变化等原因,中国蝙蝠受到极大的威胁,约51%的物种位于近危等级之上。为了有效地保护中国蝙蝠物种的多样性,建议加强基础研究,建立中国蝙蝠多样性监测网络,加强蝙蝠栖息地保护,完善相关法律法规,加强蝙蝠公众教育,以促进中国蝙蝠生物学研究和保护。     

Population changes of Greater horseshoe bats studied near Bristol over the past twenty-six years

Capture censuses of Greater horseshoe bats involving about 35 hibernacula were consistently carried out over twenty-six years in two separate areas. Hibernacula were visited three times per winter. A control area (reduced disturbance) was visited once annually. Censuses showed similar trends in all three areas, and counts of bats at a breeding site showed similar trends to those hibernacula, hut much greater stability. All numbers fell sharply to about 50%, of the original level between the winters or 1962/3 and 1966/7, then more-or-less stabilized until the mid 1970s; rose in the late 1970s and early 1980s, and finally declined precipitiously in all areas in 1986 to about 30% of the 1962/3 figure. Numbers of juveniles born annually showed no relationship to the numbers reaching hibernacula during the subsequent winter, but was negatively related to the mean birth time in July. The final forearm length of juveniles is negatively related to birth time. A population control mechanism based on birth timing and subsequent growth is postulated and supported by reproductive studies.     

Roost selection by Formosan leaf-nosed bats (Hipposideros armiger terasensis)

Patterns of roost use by Formosan leaf-nosed bats (Hipposideros armiger terasensis) were studied from November 1998 to April 2000. Structural characteristics, microclimates, and disturbance levels of 17 roosts used by H. a. terasensis and 15 roosts either used by other bat species (2) or not occupied by any bat species were compared. Roosts used by these bats were significantly larger in size and had greater areas covered by water compared to unused roosts. Entrances of active roosts were more likely to be east-west oriented. Hibernacula had lower entrances and ceilings than did roosts used only in summer. Higher temperatures were recorded in non-breeding roosts than in breeding roosts, but temperature gradients in these two types of roosts did not differ. In winter, hibernacula were warmer, and the temperature fluctuated less than in non-hibernacula. The relative humidities in summer roosts and hibernacula were nearly 100%. Disturbance levels were significantly higher in non-breeding roosts than in breeding roosts, and in non-hibernacula than in hibernacula. These results suggest that the Formosan leaf-nosed bats are selective of their roosts, but the pattern of their roost selection differs from those reported for bats of temperate regions. The reasons for such differences may be related to differences in body size, behavior, and reproductive strategy of the Formosan leaf-nosed bats living in a subtropical climate in Taiwan.     

Differences in seasonal survival suggest species‐specific reactions to climate change in two sympatric bat species

Long‐lived animals with a low annual reproductive output need a long time to recover from population crashes and are, thus, likely to face high extinction risk, if the current global environmental change will increase mortality rates. To aid conservation of those species, knowledge on the variability of mortality rates is essential. Unfortunately, however, individual‐based multiyear data sets that are required for that have only rarely been collected for free‐ranging long‐lived mammals. Here, we used a five‐year data set comprising activity data of 1,445 RFID‐tagged individuals of two long‐lived temperate zone bat species, Natterer's bats (Myotis nattereri) and Daubenton's bats (Myotis daubentonii), at their joint hibernaculum. Both species are listed as being of high conservation interest by the European Habitats Directive. Applying mixed‐effects logistic regression, we explored seasonal survival differences in these two species which differ in foraging strategy and phenology. In both species, survival over the first winter of an individual's life was much lower than survival over subsequent winters. Focussing on adults only, seasonal survival patterns were largely consistent with higher winter and lower summer survival but varied in its level across years in both species. Our analyses, furthermore, highlight the importance of species‐specific time periods for survival. Daubenton's bats showed a much stronger difference in survival between the two seasons than Natterer's bats. In one exceptional winter, the population of Natterer's bats crashed, while the survival of Daubenton's bats declined only moderately. While our results confirm the general seasonal survival pattern typical for hibernating mammals with higher winter than summer survival, they also show that this pattern can be reversed under particular conditions. Overall, our study points toward a high importance of specific time periods for population dynamics and suggests species‐, population‐, and age class‐specific responses to global climate change.