INTRODUCTION
In temperate zones of North America, hibernating animals, includingMyotis lucifugus (little brown myotis), bridge resource poor
winters through energetic budgeting and behavioural changes (Hock 1951,
Wang 1978, Speakman and Rowland 1999, Ruf and Geiser 2015). Survival
over winter hibernation depends upon three main facets: 1) the amount of
energy stored, primarily in body fat, 2) energetic expenditure (rate of
metabolic consumption), and 3) the duration of hibernation (Humphries et
al. 2002). Hibernation is composed of bouts of torpor, during which body
temperature drops to near ambient temperature to limit heat loss and
results in reduced metabolism to restrict the consumption of finite
metabolic resources. Torpor is periodically interrupted by energy
intensive periods of arousal during which hibernators return to
euthermic body temperature (Hayman et al. 2010). Hibernators arouse for
a variety of proposed reasons (for a review see Carey [2019] and
citations within), including the need to eliminate metabolic waste,
regain water balance, or mate. While arousals represent a small fraction
of the total time spent in hibernation, they account for the majority of
energy consumed, with a single arousal costing as much as 5% of total
overwinter energetic costs (Thomas et al. 1990).
Microclimate selection is critical for hibernators (Boyles et al. 2007).
By allowing body temperature to drop during torpor, M. lucifugusconsumes roughly 80-fold less energy per unit time due to the
relationship between metabolic rate and temperature (Hock 1951, Speakman
and Thomas 2003). To maximize the utility of these metabolic reductions,
bats seek out caves, mines, scree slopes, or other locations generally
referred to as ”hibernacula” where they can overwinter (Speakman and
Thomas 2003). Relative to the surface landscape, subterranean locations
can provide suitable low temperature (i.e., 0 –10 ˚C) habitats for
hibernators (Thomas and Cloutier 1992). Microclimate selection will vary
greatly based on species-specific preferences (Haase et al. 2021), and
roost selection within the larger hibernaculum critically affects both
the frequency of arousals and efficiency of torpor (Humphries et al.
2002, Czenze et al. 2013, Haase et al. 2019). Species such as M.
lucifugus appear to choose roost locations with stable, nearly
saturated environments and low temperatures to ameliorate their
relatively high rates of evaporative water loss, while other bat species
are capable of using more arid, and less thermally-stable, roosts as
hibernacula (Klüg-Baerwald and Brigham 2017, Klüg-Baerwald et al. 2017).
Even so, within a cave or mine system, roost conditions may not remain
stationary throughout the duration of hibernation and some bats will
relocate within the hibernaculum to seek specific microclimate
conditions as their body condition changes (Hayman et al. 2010).
The duration of winter hibernation is another critical determinant to
the survival of hibernators. The stimuli that drive immergence
(entrance) to and emergence (exit) from hibernation, and their
geographic variation, are under-described (Norquay and Willis in press,
Lane et al. 2012, Czenze et al. 2013). The duration of winter
hibernation presents a strong selective pressure, as longer winters
result in shorter growing seasons and less time available for
pre-hibernation fattening (Kunz et al. 1998). While animals that
hibernate at more southern latitudes may be able to capitalize on breaks
in the winter weather to opportunistically feed (Thomas et al. 1990),
this is not always an option for other latitudes. Entrances to
hibernacula may be blocked by snow, preventing foraging even if breaks
in the weather did allow for the re-emergence of prey species (CLL,unpublished data ). Because North American hibernating bats feed
on insects, researchers have estimated effective hibernation duration
based upon the number of freezing days, with the assumption that
freezing temperatures prevent insect availability until spring
(Humphries et al. 2002, Hayman et al. 2016). However, some populations
of bats may emerge from hibernation while freezing temperatures are
still present, suggesting that there may be more complex determinants of
emergence times (Johnson et al. 2017). Additionally, site-level
differences, such as slope aspect, foliage cover, and proximity to water
may influence the density of prey insects and their ability to persist
on the landscape.
Beyond the normal challenges of hibernation, the epizootic white-nose
syndrome (WNS), caused by the psychrophilic fungusPseudogymnoascus destructans , has increased energetic demands for
hibernating bats (Blehert et al. 2009). The fungal pathogen responsible
for the disease has spread rapidly through North America since 2006 and
has killed millions of hibernating bats (Frick et al. 2015). Bats can be
exposed to the fungus during the swarming period or over hibernation in
the hibernacula. Once infected, the fungus grows during hibernation when
bat skin temperatures are reduced and immune function is suppressed
(Verant et al. 2012, Langwig et al. 2015, 2016). While there is still
discuss the ultimate cause of mortality in WNS-impacted bats, it has
been linked to the increased frequency of arousals in infected bats,
ultimately resulting in the depletion of fat stores prior to the end of
the hibernation period and subsequent starvation (Warnecke et al. 2012,
Lilley et al. 2016).
There has been much research on energy consumption over hibernation in
multiple bat species (Thomas et al. 1990, Cryan and Wolf 2003, Willis et
al. 2006, Jonasson and Willis 2012, McGuire et al. 2014, Haase et al.
2019) and across the distribution of single bat species (Humphries et
al. 2002, Hayman et al. 2016), but we have yet to determine how the
spatial variation in the other two critical parameters governs
overwinter survival for hibernators: duration of winter hibernation and
amount of fat stores taken into hibernation. Previous models (Hayman et
al. 2016) allowed for spatial variation in winter duration; however, the
definition of winter duration was made a priori and based solely
upon the number of nights with an average temperature below 0°C
(Humphries et al. 2002). Similarly, the amount of body fat has generally
been fixed as 25-30 % of total body mass in most studies (Humphries et
al. 2002, Hayman et al. 2016, Haase et al. 2021). Fat resources are a
major determinant of survival (Haase et al. 2019) and thus this
assumption of proportion of body fat warrants review. Here we used
generalized linear and linear models to: 1) estimate hibernation
duration, 2) relate body mass to pre-hibernation fat stores, and 3)
predict pre-hibernation body mass and fat across the distribution ofM. lucifugus . We focused on M. lucifugus due to the high
impact of WNS on M. lucifugus populations, its widespread
distribution, and the availability of published data. We predicted that
spatial variation in overwinter duration would drive variation of body
mass and fat to account for different energy requirements leading to
spatial variation in WNS disease outcomes. Finally, we used a
mechanistic model of hibernation energetics (Haase et al. 2019) to
estimate the total metabolic costs of hibernation with and without the
impacts of WNS across the species’ distribution of M. lucifugus .