We investigated the individual hibernation phenology in two common sympatric temperate-zone bat species over multiple years using RFID-tags to quantify the longest period concurrently spent within a hibernaculum. We observed marked differences in overall hibernation duration between species, with Daubenton’s bats hibernating up to twice as long as Natterer’s bats. Linear mixed models found that sex was the strongest predictor of hibernation phenology in Natterer’s bats, whereas in Daubenton’s bats age was more important. Nevertheless, the effects of sex and age were similar in both species; adult females had the longest hibernation duration, and juveniles generally had shorter hibernation durations than adults, with the exception of adult male Natterer’s bats, which had the shortest overall duration. Finally, timing of all parameters varied over years, with Daubenton’s bats showing a conspicuous progressive regression in hibernation entry, potentially indicating an influence of changing environmental conditions on hibernation phenology.
The timing of hibernation phenology has important consequences for an individual’s survival and reproductive success. The importance of minimizing the ecological and physiological costs of hibernation have recently been highlighted as an important driver that may favor reduced expression of hibernation when possible (see optimal hibernation theory; ). Characterizing the entrance and emergence phenology across demographic classes within and between species allows for an understanding of the broader pressures shaping hibernation behavior. In this context, several of the differences observed between the two species investigated here may point to more general patterns driving hibernation phenology across fat-storing hibernators.
The observed differences in hibernation phenology between our two study species are likely a reflection of their different foraging niches, as the experienced local weather conditions were identical and their body size, and thus their fat storage capacity and energy metabolism, are broadly comparable. Daubenton’s bats primarily forage on aquatic insects , whose emergence starts in April, peaks in August, and terminates in October , closely matching the hibernation phenology observed here. In contrast, the gleaning abilities of Natterer’s bats allow them to exploit inactive prey , allowing them to efficiently hunt at lower temperatures, thereby potentially explaining their much shorter overall hibernation duration. Previous studies have similarly highlighted the role of species-specific foraging niches and food availability in shaping the timing of reproduction in sympatric Myotis species [31, 38]. Nevertheless, when compared to the hibernation phenology of M. lucifugus in central Canada , it is clear that broader extrinsic factors such as climate also play a large role. In this species, mean hibernation duration in all sex/age classes was over 230 days, roughly three times longer than observed for Natterer’s bats in this study.
The far shorter overall duration of hibernation may allow Natterer’s bats to reduce the ecological and physiological costs of hibernation on the whole, but may also increase their susceptibility to variations in prey availability and climate instability. A clear example of this is the winter-period 2010/2011, during which there was an unusually heavy snowfall and a long-lasting snow cover from the second half of November onwards. Reusch et al.  observed a survival rate of only 38% in Natterer’s bats in our study population during this winter (compared to over 80% in other years), suggesting many individuals were forced to enter hibernation before their energy resources were sufficiently high to ensure a successful hibernation. More broadly, winter survival rates of Natterer’s bats were consistently lower than of Daubenton’s bats, but summer survival rates were higher , potentially suggesting that the theoretical ability to feed throughout longer periods of the year does not mean that it is necessarily advantageous to do so, or that the increased mortality during winter is compensated by higher survival during summer due to the avoided physiological costs of hibernation.
The observed sex differences in hibernation phenology generally corresponded to predicted effects of the desynchronization of reproductive investment between males and females seen in temperate-zone bats , with the exception that males not only entered hibernation later but also emerged from hibernation earlier than females. Males invest heavily in spermatogenesis and mating behavior immediately prior to hibernation. Indeed, Kohyt et al.  found that the seasonal and nightly body condition of adult male Natterer’s bats only increased after the species swarming activity peak in early October. This suggests that their special foraging ability enables the males to postpone the accumulation of fat reserves until just before entering the hibernaculum. Unlike in M. lucifugus , adult males emerged from the hibernaculum earlier than adult females in both study species. By strongly investing in mating activities in autumn, it is conceivable that male bats may be forced to emerge from hibernation early because of depleted fat reserves . Males may be able to compensate for reduced foraging success in spring by using daily torpor as a strategy to avoid bad feeding conditions . In contrast, females pay a cost of reduced fetal growth if they use daily torpor in spring . As a result, if spring foraging success is unpredictable, it may be that delaying the departure from the hibernaculum until feeding conditions are more stable is favorable for females despite the advantages of early parturition.
Both delayed entry and early emergence from the hibernaculum in juveniles, may be caused by a large energetic investment into growth and a slower accumulation of sufficient energy reserves prior to hibernation [36, 42]. In addition, in both of our study species, juvenile males may already invest in reproduction in their first year [43, 44], suggesting an increased energy investment of juvenile males relative to juvenile females. This may explain why juvenile males entered the hibernaculum considerably later than juvenile females. This strategy may however come with a considerable trade-off when a species hibernation onset is already generally very late and may explain why juvenile male Natterer’s bats have the lowest winter survival rate of all sex/age classes . Age related differences in emergence were considerably less pronounced, suggesting that increased investment in filling up energy reserves prior to hibernation is preferable to early emergence. As in the observed later emergence of adult females, this may be related to the unpredictability of foraging success in spring. In M. lucifugus and Myotis volans, Schowalter  found that juveniles were active later than adults, although Norquay and Willis  did not observe a difference. However, they did find that juvenile female Myotis lucifugus emerged from hibernation significantly later than adult females , likely emphasizing the importance of early emergence for early parturition in the species where females do not reproduce in their first year.
Annual variation in hibernation phenology
We detected shifts in yearly hibernation phenology in both species, suggesting some ability to flexibly time hibernation, depending on yearly environmental conditions. Zervanos et al.  observed differences in hibernation timing along a latitudinal gradient for woodchucks (Marmota monax) suggesting phenotypic plasticity allowing them to adjust energy use in response to different climatic conditions. However, other factors may limit plasticity in hibernation phenology based on environmental conditions alone as seen in Edible dormice (Glis glis), where individuals entered hibernation despite favorable feeding conditions presumably as a result of increased predation risk during autumn .
How these effects interact to shape hibernation timing have important consequences for their ability to adapt to climate change. Our findings imply that changing environmental conditions may influence sympatric bat populations divergently (see ). Bats with flexible diets such as Natterer’s bats may benefit from the successively extended activity period of some insect species in autumn and early spring [47, 48], and thus reduce their hibernation duration. Despite the potential advantages of such a reduction due to gradual weather changes, the predicted increase in volatility of summer and winter precipitation and storms , may strongly impact survival in some years, as seen for Natterer’s bats in 2010/2011 . Daubenton’s bats on the contrary, may be less flexible in exploiting warmer autumn und spring temperature and therefore may be more sensible to potential mismatches with their main food resource. Notably, Chironomidae, an important component of early spring aquatic insect biomass, have been shown to decline with warming temperatures , potentially limiting food availability on emergence from hibernation in Daubenton’s bats. Finally, it must be emphasized that in addition to changes in their phenology, species may also adapt with regard to their arousal rates, microclimate selection within the hibernaculum, or social behavior throughout the hibernation period [4,5,6,7,8,9].