Shifts in population density centers of a hibernating mammal driven by conflicting effects of climate change and disease.

Populations wax and wane over time in response to an organism's interactions with abiotic and biotic forces. Numerous studies demonstrate that fluctuations in local populations can lead to shifts in relative population densities across the geographic range of a species over time. Fewer studies attempt to disentangle the causes of such shifts. Over four decades (1983-2022), we monitored populations of hibernating Indiana bats (Myotis sodalis) in two areas separated by ~110 km. The number of bats hibernating in the northern area increased from 1983 to 2011, while populations in the southern area remained relatively constant. We used simulation models and long-term weather data to demonstrate the duration of time bats must rely on stored fat during hibernation has decreased in both areas over that period, but at a faster rate in the northern area. Likewise, increasing autumn and spring temperatures shortened the periods of sporadic prey (flying insect) availability at the beginning and end of hibernation. Climate change thus increased the viability of northern hibernacula for an increasing number of bats by decreasing energetic costs of hibernation. Then in 2011, white-nose syndrome (WNS), a disease of hibernating bats that increases energetic costs of hibernation, was detected in the area. From 2011 to 2022, the population rapidly decreased in the northern area and increased in the southern area, completely reversing the northerly shift in population densities associated with climate change. Energy balance during hibernation is the singular link explaining the northerly shift under a changing climate and the southerly shift in response to a novel disease. Continued population persistence suggests that bats may mitigate many impacts of WNS by hibernating farther south, where insects are available longer each year.

White-nose syndrome fungus: a generalist pathogen of hibernating bats.

Host traits and phylogeny can determine infection risk by driving pathogen transmission and its ability to infect new hosts. Predicting such risks is critical when designing disease mitigation strategies, and especially as regards wildlife, where intensive management is often advocated or prevented by economic and/or practical reasons. We investigated Pseudogymnoascus [Geomyces] destructans infection, the cause of white-nose syndrome (WNS), in relation to chiropteran ecology, behaviour and phylogenetics. While this fungus has caused devastating declines in North American bat populations, there have been no apparent population changes attributable to the disease in Europe. We screened 276 bats of 15 species from hibernacula in the Czech Republic over 2012 and 2013, and provided histopathological evidence for 11 European species positive for WNS. With the exception of Myotis myotis, the other ten species are all new reports for WNS in Europe. Of these, M. emarginatus, Eptesicus nilssonii, Rhinolophus hipposideros, Barbastella barbastellus and Plecotus auritus are new to the list of P. destructans-infected bat species. While the infected species are all statistically phylogenetically related, WNS affects bats from two suborders. These are ecologically diverse and adopt a wide range of hibernating strategies. Occurrence of WNS in distantly related bat species with diverse ecology suggests that the pathogen may be a generalist and that all bats hibernating within the distribution range of P. destructans may be at risk of infection.

White-nose syndrome and wing damage index scores among summer bats in the northeastern United States.

White-nose syndrome (WNS) adversely affects millions of bats hibernating in caves of the eastern United States. Beginning in 2009, the US Fish and Wildlife Service supported use of a wing damage index (WDI) scoring system (scale of 0 to 3, or no damage to severe) to assess wing damage of bats captured during summer. Based on bat captures at 459 mist net sites in Pennsylvania, New York, Maryland, Virginia, and New Jersey, USA, we questioned whether WDI scores varied by species group, date, and distance to the closest known affected hibernaculum. We also compared relative health (body mass index [BMI] scores) to WDI scores. Of 3,419 bats (nine species), only four individuals (0.1%; little brown [Myotis lucifugus] and northern bats [Myotis septentrionalis]) were scored as a 3 and 47 (1.4%; big brown [Eptesicus fuscus], little brown, and northern bats) as a 2. All tree bats (eastern red [Lasiurus borealis], hoary [Lasiurus cinereus], and silver-haired bats [Lasionycteris noctivagans]) scored a 0 or 1, suggesting that these species were not affected by WNS. The average WDI score decreased as summer progressed, although trends were weak. Average WDI score and number of bats with class 2 and 3 damage increased with proximity to a known WNS-positive hibernaculum. Similarly, the number of bats with severe wing damage (scoring 2 or 3) was greater at sites closer to infected hibernacula, but little variance was explained by the trend. When species-specific BMI was examined, trends were consistent by sex (female BMI scores were higher than those of males), but no relationship was discovered between BMI and WDI scores. We conclude that, at this larger geographic scale, WDI is not a clear indicator of bat health.

Thermocron iButton and iBBat temperature dataloggers emit ultrasound.

Thermocron iButton dataloggers are widely used to measure thermal microclimates experienced by wild animals. The iBBat is a smaller version of the datalogger, also commercially available, that is used to measure animal skin or core body temperatures when attached externally or surgically implanted. Field observations of bats roosting under a bridge suggested that bats avoided locations with iButtons. A heterodyne bat detector revealed that the dataloggers emitted ultrasound which was detectable from a distance of up to 30 cm. We therefore recorded and quantified the acoustic properties [carrier frequency (Hz) and root mean square sound pressure level (dB SPL)] of iButton and iBBat dataloggers. All units emitted a 32.9 kHz pure tone that was readily picked up with a time expansion bat detector at a distance of 1 cm, and most were detected at a distance of 15 cm. The maximum amplitude of iButton dataloggers was 46.5 dB SPL at 1.0 cm-a level within the range of auditory sensitivity for most small mammals. Wrapping iButtons in plastic insulation severely attenuated the amplitude of ultrasound. Although there was a statistically significant reduction in rates of warming and cooling with insulation, this effect was small and we suggest that insulation may be a viable solution to eliminate unwanted ultrasonic noise in instances when small delays in thermal response dynamics are not a concern. We recommend behavioural studies to assess if the electronic signals emitted by iButtons are disturbing to small mammals.

Energy availability influences microclimate selection of hibernating bats.

Many species hibernate to conserve energy during periods of low food and water availability. It has long been assumed that the optimal hibernation strategy involves long, deep bouts of torpor that minimize energy expenditure. However, hibernation has ecological (e.g. decreased predator avoidance) and physiological (e.g. sleep deprivation) costs that must be balanced with energy savings; therefore, individuals possessing sufficient energy reserves may reduce their use of deep torpor. We tested the hypothesis that energy (fat) availability influences temperature selection of two fat-storing bat species during hibernation. We predicted that individuals with small energy reserves would select colder temperatures for hibernation in order to minimize energy expenditure, while individuals with larger energy reserves would choose warmer temperatures to minimize the costs of hibernation. Results from our field experiment indicate that little brown myotis (Myotis lucifugus) hibernating in warm microclimates were significantly heavier than individuals hibernating in cooler microclimates. To determine if energy availability was mediating this relationship, we limited fatty acid availability with mercaptoacetate (MA) and quantified its effect on torpid metabolic rate (TMR) and thermal preference of big brown bats (Eptesicus fuscus). Administration of MA caused a 43% drop in TMR at 10 degrees C and caused bats to choose significantly colder temperatures for hibernation. Our results suggest that fat-storing bats minimize torpor expression using both physiological and behavioral mechanisms.

Temperatures and locations used by hibernating bats, including Myotis sodalis (Indiana bat), in a limestone mine: implications for conservation and management.

Understanding temperatures used by hibernating bats will aid conservation and management efforts for many species. A limestone mine with 71 km of passages, used as a hibernaculum by approximately 30,000 bats, was visited four times during a 6-year period. The mine had been surveyed and mapped; therefore, bats could be precisely located and temperatures (T (s)) of the entire hibernaculum ceiling accurately mapped. It was predicted that bats should hibernate between 5 and 10 degrees C to (1) use temperatures that allow a near minimal metabolic rate, (2) maximize the duration of hibernation bouts, (3) avoid more frequent and prolonged arousal at higher temperatures, (4) avoid cold and freezing temperatures that require an increase in metabolism and a decrease in duration of hibernation bouts or that could cause death, and (5) balance benefits of a reduced metabolic rate and costs of metabolic depression. The distribution of each species was not random for location (P < 0.000) or T (s) (P < 0.000). Myotis sodalis (Indiana bat) was most restricted in areas occupied, hibernating in thermally stable yet cold areas (X = 8.4 +/- 1.7 degrees C); 99% associated with cement block walls and sheltered alcoves, which perhaps dampened air movement and temperature fluctuations. Myotis lucifugus (little brown myotis) hibernated in colder, more variable areas (X = 7.2 +/- 2.6 degrees C). Myotis septentrionalis (northern myotis), Pipistrellus subflavus (eastern pipistrelle), and Eptesicus fuscus (big brown bat) typically hibernated in warm, thermally stable areas (X = 9.1 +/- 0.2 degrees C, X = 9.6 +/- 1.9 degrees C, and X = 9.5 +/- 1.5 degrees C, respectively). These data do not indicate that hibernacula for M. sodalis, an endangered species, should be manipulated to cool below 5 degrees C.

Use of artificial roost structures by bats at the Indianapolis International Airport.

From 1992-1996, 3204 artificial roosts of 9 types were placed in woodlots near Indianapolis International Airport in an effort to provide habitat for the federally-endangered Indiana myotis (Myotis sodalis) and to determine the feasibility of using these structures to manage bats in a rapidly developing suburban area. We surveyed these structures at least annually during 1992-1999 and found only northern myotis (Myotis septentrionalis) regularly using the structures. Four other species were occasionally found using structures including big brown bats (Eptesicus fuscus, n=14 individuals), little brown myotis (Myotis lucifugus, n=2), Indiana myotis (Myotis sodalis, n=2), and one silver-haired bat (Lasionycteris noctivagans). Single, triple, and Missouri-style batboxes were almost always used, rather than the six other types of experimental roosts that had been in place. However, after 10 years in place, it appears that Indiana bats are acclimated to boxes, as 6 of them were being used rather regularly by Indiana myotis. Bat boxes can provide roosting habitat for some species under conditions where few suitable roosts exist, but assuring an abundance of natural habitats is usually more desirable for conservation of tree-roosting bats.