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.     

Host,Pathogen, and Environmental Characteristics Predict White-Nose Syndrome Mortality in Captive Little Brown Myotis (Myotis lucifugus)

An estimated 5.7 million or more bats died in North America between 2006 and 2012 due to infection with the fungus Pseudogymnoascus destructans (Pd) that causes white-nose syndrome (WNS) during hibernation. The behavioral and physiological changes associated with hibernation leave bats vulnerable to WNS, but the persistence of bats within the contaminated regions of North America suggests that survival might vary predictably among individuals or in relation to environmental conditions. To investigate variables influencing WNS mortality, we conducted a captive study of 147 little brown myotis (Myotis lucifugus) inoculated with 0, 500, 5 000, 50 000, or 500 000 Pd conidia and hibernated for five months at either 4 or 10°C. We found that female bats were significantly more likely to survive hibernation, as were bats hibernated at 4°C, and bats with greater body condition at the start of hibernation. Although all bats inoculated with Pd exhibited shorter torpor bouts compared to controls, a characteristic of WNS, only bats inoculated with 500 conidia had significantly lower survival odds compared to controls. These data show that host and environmental characteristics are significant predictors of WNS mortality, and that exposure to up to 500 conidia is sufficient to cause a fatal infection. These results also illustrate a need to quantify dynamics of Pd exposure in free-ranging bats, as dynamics of WNS produced in captive studies inoculating bats with several hundred thousand conidia may differ from those in the wild.     

Antibodies to Pseudogymnoascus destructans are not sufficient for protection against white‐nose syndrome

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.     

Hibernation in warm hibernacula by free-ranging Formosan leaf-nosed bats, <Emphasis Type="Italic">Hipposideros terasensis</Emphasis>, in subtropical Taiwan

The subtropical Formosan leaf-nosed bats, Hipposideros terasensis (Hipposideridae), show little activity during winter. It has never been determined whether in winter they exhibit hibernation and multi-day periods of low body temperature. The objectives of this study were to understand the winter activity pattern of H. terasensis and to examine whether it enters hibernation during winter. We monitored the skin temperature (T _sk) of nine free-ranging H. terasensis by attaching temperature-sensitive transmitters during the winters of 2007–2008 and 2008–2009. The results showed that H. terasensis entered hibernation from late December to early March. H. terasensis, however, differs from temperate hibernating bats in several ways: (1) it is capable of hibernation at roost temperature (T _r) and T _sk > 20°C; (2) hibernation at high T _r and T _sk does not lead to a relatively high arousal frequency; and (3) adults do not increase body mass in autumn prior to hibernation. To test the hypothesis that H. terasensis feeds frequently during the hibernation period to compensate for the high energetic demands of hibernating in warm hibernacula, we recorded the number and timing of bats that emerged from and entered into a hibernaculum, which contained more than 1,000 bats. From 30 December 2007 to 29 February 2008, an average of only 8.4 bats (<1%) per night (29 nights) emerged from the hibernaculum. Adult bats lost an average of 13–14% of body mass during an approximately 70-day hibernation period. We suggest that H. terasensis might have remarkably low torpid metabolic rates during hibernation.     

Hibernation does not affect memory retention in bats

Long-term memory can be critically important for animals in a variety of contexts, and yet the extreme reduction in body temperature in hibernating animals alters neurochemistry and may therefore impair brain function. Behavioural studies on memory impairment associated with hibernation have been almost exclusively conducted on ground squirrels (Rodentia) and provide conflicting results, including clear evidence for memory loss. Here, we for the first time tested memory retention after hibernation for a vertebrate outside rodents—bats (Chiroptera). In the light of the high mobility, ecology and long life of bats, we hypothesized that maintenance of consolidated memory through hibernation is under strong natural selection. We trained bats to find food in one out of three maze arms. After training, the pre-hibernation performance of all individuals was at 100 per cent correct decisions. After this pre-test, one group of bats was kept, with two interruptions, at 7°C for two months, while the other group was kept under conditions that prevented them from going into hibernation. The hibernated bats performed at the same high level as before hibernation and as the non-hibernated controls. Our data suggest that bats benefit from an as yet unknown neuroprotective mechanism to prevent memory loss in the cold brain.     

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.     

No evidence for memory retention of a learned association between a cue and roost quality after hibernation in free-ranging bats

Hibernation is a physiological adaptation that allows animals to survive adverse environmental conditions. A commonly assumed cost of hibernation is impaired memory retention. So far, however, the effects of hibernation on memory retention have been assessed on only a few behavioral tasks, and exclusively under laboratory conditions. Taking advantage of the longevity and strict colony fidelity of female Bechstein's bats, we were able to evaluate memory retention in the same individuals over two consecutive summers in the field. We used a pairwise roost choice experiment with automatic monitoring of RFID-tagged bats. Roosts’ suitability as day roost was associated with a distinctive external echo-acoustic cue. Experiments were separated by a natural hibernation period of eight months. We determined associative learning and memory retention by comparing the bats’ proportion of visits to suitable roosts within and between breeding seasons, respectively. During the first breeding season, bats quickly learned to associate the suitable roosts with their external cue. After hibernating, we found no evidence that individuals remembered the association between the roosts’ suitability and their respective external cue, suggesting a lack of memory retention. Nevertheless, bats quickly re-learned the same association during the second breeding season, emphasizing the high behavioral flexibility of Bechstein's bats.     

Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome

White-nose syndrome (WNS) is a new disease of bats that has devastated populations in eastern North America. Infection with the fungus, Geomyces destructans, is thought to increase the time bats spend out of torpor during hibernation, leading to starvation. Little is known about hibernation in healthy, free-ranging bats and more data are needed to help predict consequences of WNS. Trade-offs presumably exist between the energetic benefits and physiological/ecological costs of torpor, leading to the prediction that the relative importance of spring energy reserves should affect an individual''s use of torpor and depletion of energy reserves during winter. Myotis lucifugus mate during fall and winter but females do not become pregnant until after spring emergence. Thus, female reproductive success depends on spring fat reserves while male reproductive success does not. Consequently, females should be “thrifty” in their use of fat compared to males. We measured body condition index (BCI; mass/forearm length) of 432 M. lucifugus in Manitoba, Canada during the winter of 2009/2010. Bats were captured during the fall mating period (n = 200), early hibernation (n = 125), and late hibernation (n = 128). Adult females entered hibernation with greater fat reserves and consumed those reserves more slowly than adult males and young of the year. Consequently, adult females may be more likely than males or young of the year to survive the disruption of energy balance associated with WNS, although surviving females may not have sufficient reserves to support reproduction.     

Bats and aquatic habitats: a review of habitat use and anthropogenic impacts

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Annual skeletal changes in the little brown bat, Myotis lucifugus lucifugus, with particular reference to pregnancy and lactation

Studies of bone from summer-active little brown bats, Myotis lucifugus lucifugus, have demonstrated sex differences in the renewal of skeletal mineral reserves following spring-arousal from hibernation. Patterns of bone remodeling in both sexes of bats indicate that new bone formation does not occur during hibernation: All new bone formation occurs during the summer-active season. Results show that a short period of time elapses after hibernation before the initial demands of a large fetus and rapidly growing neonate are expressed on maternal skeletal reserves. Bone loss in summer-active females was associated with pregnancy and lactation, whereas summer-active males did not show evidence of bone loss but, instead, uninterrupted bone accretion throughout the summer-active season. Osteoclasts and bone-forming osteoblasts, absent during the hibernation period, reappeared on bone surfaces following spring-arousal from hibernation. There was no apparent increase in osteoclast numbers or activity during lactation but resorption cavities were found in deep cortical lamellae distant from bone surfaces. The increase in bone resorption in lactating bats appeared to be by osteocytic osteolysis, suggesting that it might be a significant mechanism of bone/calcium regulation in this hibernating mammal throughout the year.     

Thermoregulatory variation among populations of bats along a latitudinal gradient

Most studies of hibernation physiology sample individuals from populations within a single geographic area, yet some species have large ranges meaning populations likely experience area-specific levels of energetic challenges. As well, few studies have assessed within-season variation. Since physiological adjustments often are influenced by environmental factors, and the types of environments vary with geography, we expected variance in hibernation patterns among geographically separated populations. Our specific goal was to measure intraspecific variation in torpid metabolic rate (TMR) and body temperature (T _b) as a function of ambient temperature (T _a) for a non-migratory and migratory species to determine whether there is a continuum in physiological responses based on latitude. We chose big brown (Eptesicus fuscus) and eastern red bats (Lasiurus borealis) as model species and sampled individuals from populations throughout each species’ winter range. In both species, individuals from southern populations maintained higher TMR at cooler T _as and lower TMR at warmer T _as than those from northern populations. Big brown bats from southern populations regulated T _b during torpor at higher levels and there was no significant difference in T _b between populations of eastern red bats. Although metabolic responses were similar across the gradient between species, the effect was more dramatic in big brown bats. Our data demonstrate a continuum in thermoregulatory response, ranging from classic hibernation in northern populations to a pattern more akin to daily torpor in southern populations. Our research highlights the potential usefulness of bats as model organisms to address questions about within-species physiological variation in wild populations.     

Warming up for dinner: torpor and arousal in hibernating Natterer’s bats (Myotis nattereri) studied by radio telemetry

The frequency and function of arousals during hibernation in free-living mammals are little known. We used temperature-sensitive radio transmitters to measure patterns of torpor, arousal and activity in wild Natterer’s bats Myotis nattereri during hibernation. Duration of torpor bouts ranged from 0.06 to 20.4 days with individual means ranging from 0.9 to 8.9 days. Arousals from torpor occurred most commonly coincident with the time (relative to sunset) typical for bats emerging from summer roosts to forage. Bats with lower body condition indices had a shorter average duration of their torpor bouts. We found a non-linear relationship between duration of torpor bout and ambient temperature: the longest average torpor bouts were at temperatures between 2 and 4°C with shorter bouts at lower and higher ambient temperatures. One individual was radio-tracked for ten nights, remained active for an average of 297 min each night and was active for longer on warmer nights. Our results suggest that vespertilionid bats use relatively short torpor bouts during hibernation in a location with a maritime climate. We hypothesise that Natterer’s bats time arousals to maximise opportunities for potential foraging during winter although winter feeding is not the sole determinant of arousal as bats still arouse at times when foraging is unlikely.     

Histopathology confirms white-nose syndrome in bats in Europe

White-nose syndrome, associated with the fungal skin infection geomycosis, caused regional population collapse in bats in North America. Our results, based on histopathology, show the presence of white-nose syndrome in Europe. Dermatohistopathology on two bats (Myotis myotis) found dead in March 2010 with geomycosis in the Czech Republic had characteristics resembling Geomyces destructans infection in bats confirmed with white-nose syndrome in US hibernacula. In addition, a live M. myotis, biopsied for histopathology during hibernation in April 2011, had typical fungal infection with cupping erosion and invasion of muzzle skin diagnostic for white-nose syndrome and conidiospores identical to G. destructans that were genetically confirmed as G. destructans.     

Short-faced bats (Phyllostomidae: Stenodermatina): a Caribbean radiation of strict frugivores

Aim  To test the hypothesis that Caribbean Short-faced bats descended from a single recent ancestor that originated in the continental Neotropics (Mexico, Central America and/or South America).
Location  The Neotropics, including the West Indies.
Methods  New mitochondrial cytochrome b and nuclear Rag2 sequences were combined with published molecular data to estimate phylogenetic relationships and sequence divergence among Short-faced bats. The resulting phylogenies were compared with those compatible with the single-origin hypothesis using two model-based statistical tests. Confidence limits on sequence divergence were estimated using a parametric bootstrap.
Results  All molecular phylogenies revealed two independent Caribbean lineages and showed that continental Short-faced bats share a recent common ancestor. Morphology-based trees compatible with the single-origin hypothesis were significantly worse at explaining the molecular data than any molecular phylogeny.
Main conclusions  The ancestor of all Short-faced bats reached the Antilles in the Miocene, too recently to have used a proposed Oligocene land bridge, and well before the Pleistocene glaciations that are thought to have facilitated dispersal for many bats. After a long period of isolation, Short-faced bats diversified quickly on the Caribbean islands. A single Short-faced lineage then reached the continent and subsequently expanded its range and diversified into the four extant genera. Among bats, independent lineages of aerial insectivores and nectarivores have also recolonized the continent after evolving in the West Indies. The evidence for an insular origin of the short-faced frugivorous radiation completes a dynamic model of Caribbean biogeography that encompasses an entire biological community.     

Latitudinal patterns of mammalian species richness in the New World: the effects of sampling method and faunal group

Abstract. Although the latitudinal gradient of species richness for mammals in North America is well documented, few investigators have quantified the relationship in South America. We examined the pattern in North and South America, at two spatial scales (2.5° and 5°) for each of two sampling methods (quadrats and latitudinal bands). A scale effect was evident for quadrats but not for bands. Significant linear relationships between species richness and latitude were found for three faunal groups: all mammals, nonvolant species, and bats. Effects of area confound the latitudinal relationship. By statistically removing such effects, we found that the latitudinal gradient is not an artifact of the species-area relationship, and that the latitudinal gradients for North and South America were statistically indistinguishable. Our data suggest that both faunal subgroups, nonvolant species and bats, contributed substantially to the overall mammalian pattern. Further, multiple regression analyses showed that only latitude is a necessary variable to explain bat richness; for nonvolant species, in addition to latitude, area and longitude may be important.     

CYTOCHEMICAL DIFFERENCES IN KIDNEYS FROM WINTER-HIBERNATING AND AROUSED BATS (MYOTIS LUCIFUGUS), WITH PARTICULAR REFERENCE TO THE GOLGI ZONE

Kidneys from winter bats (Myotis lucifugus) were removed and fixed in cold formalin-calcium while the animals were in the following states: (a) natural hibernation; (b) arousal from hibernation for 24 hours; (c) laboratory maintained hibernation; and (d) no hibernation since the previous winter. With fixed frozen sections, the lead salt method of Wachstein and Meisel with adenosine triphosphate as substrate (pH 7.2) showed enzymic activity localized in large vacuoles and smaller vesicles or droplets in the Golgi region of distal and proximal tubular epithelial cells of kidneys from hibernating bats. No ATPase activity was detected in the basal lamellae of tubular epithelium from hibernating bats. ATPase activity in the Golgi region was not seen in cells from kidney tubules of bats aroused from hibernation 24 hours previously or of animals that had not hibernated, whereas activity for ATPase was present in the basal infoldings of tubular epithelium from these animals. Inosine di- and triphosphatase and calcium activated ATPase activities were also detected in the Golgi region of hibernating bats but were not present in the basal infoldings of tubular epithelium from active animals. There was little or no activity toward the mono- and diphosphates of adenine, thiamine pyrophosphate, and the di- or triphosphates of guanidine, cytidine, or deoxyadenosine. The loss of enzymic activity from the Golgi region of the tubular epithelium from hibernating bats and its increase in the region of the basal infoldings of tubular epithelium in aroused bats suggests that the Golgi region plays a role in the synthesis of enzymic protein usually identified with the external cell membrane.     

Molecular mechanism underlying muscle mass retention in hibernating bats: Role of periodic arousal

Hibernators like bats show only marginal muscle atrophy during prolonged hibernation. The current study was designed to test the hypothesis that hibernators use periodic arousal to increase protein anabolism that compensates for the continuous muscle proteolysis during disuse. To test this hypothesis, we investigated the effects of 3‐month hibernation (HB) and 7‐day post‐arousal torpor (TP) followed by re‐arousal (RA) on signaling activities in the pectoral muscles of summer‐active (SA) and dormant Murina leucogaster bats. The bats did not lose muscle mass relative to body mass during the HB or TP‐to‐RA period. For the first 30‐min following arousal, the peak amplitude and frequency of electromyographic spikes increased 3.1‐ and 1.4‐fold, respectively, indicating massive myofiber recruitment and elevated motor signaling during shivering. Immunoblot analyses of whole‐tissue lysates revealed several principal outcomes: (1) for the 3‐month HB, the phosphorylation levels of Akt1 (p‐Akt1) and p‐mTOR decreased significantly compared to SA bats, but p‐FoxO1 levels remained unaltered; (2) for the TP‐to‐RA period, p‐Akt1 and p‐FoxO1 varied little, while p‐mTOR showed biphasic oscillation; (3) proteolytic signals (i.e., atrogin‐1, MuRF1, Skp2 and calpain‐1) remained constant during the HB and TP‐to‐RA period. These results suggest that the resistive properties of torpid bat muscle against atrophy might be attained primarily by relatively constant proteolysis in combination with oscillatory anabolic activity (e.g., p‐mTOR) corresponding to the frequency of arousals occurring throughout hibernation. J. Cell. Physiol. 222: 313–319, 2010. © 2009 Wiley‐Liss, Inc.     

Antioxidant Defenses in the Brains of Bats during Hibernation

Hibernation is a strategy used by some mammals to survive a cold winter. Small hibernating mammals, such as squirrels and hamsters, use species- and tissue-specific antioxidant defenses to cope with oxidative insults during hibernation. Little is known about antioxidant responses and their regulatory mechanisms in hibernating bats. We found that the total level of reactive oxygen species (ROS) and reactive nitrogen species (RNS) in the brain of each of the two distantly related hibernating bats M. ricketti and R. ferrumequinum at arousal was lower than that at torpid or active state. We also found that the levels of malondialdehyde (product of lipid peroxidation) of the two hibernating species of bats were significantly lower than those of non-hibernating bats R. leschenaultia and C. sphinx. This observation suggests that bats maintain a basal level of ROS/RNS that does no harm to the brain during hibernation. Results of Western blotting showed that hibernating bats expressed higher amounts of antioxidant proteins than non-hibernating bats and that M. ricketti bats upregulated the expression of some enzymes to overcome oxidative stresses, such as superoxide dismutase, glutathione reductase, and catalase. In contrast, R. ferrumequinum bats maintained a relatively high level of superoxide dismutase 2, glutathione reductase, and thioredoxin-2 throughout the three different states of hibernation cycles. The levels of glutathione (GSH) were higher in M. ricketti bats than in R. ferrumequinum bats and were significantly elevated in R. ferrumequinum bats after torpor. These data suggest that M. ricketti bats use mainly antioxidant enzymes and R. ferrumequinum bats rely on both enzymes and low molecular weight antioxidants (e.g., glutathione) to avoid oxidative stresses during arousal. Furthermore, Nrf2 and FOXOs play major roles in the regulation of antioxidant defenses in the brains of bats during hibernation. Our study revealed strategies used by bats against oxidative insults during hibernation.