DISCUSSION
Here we examined the spatial variation in hibernation duration and
estimated pre-hibernation fat stores across North America and applied
these estimates to an updated model of hibernation energetics (Haase et
al. 2019) to estimate the overwinter fat necessary for M.
lucifugus to survive the hibernation. By comparing the required fat and
the fat available, we predicted survival of M. lucifugus across
its distribution for two different ecological situations: one in which
bats roost within their most preferred conditions and one in which they
roost in the best conditions predicted to be available. Finally, we
modelled the possible impact of P. destructans infection to
understand the implications for M. lucifugus populations where
bats have yet to be impacted by WNS.
Winter hibernation duration is a key determinant of the overwintering
survival for any hibernating species. While local variation in winter
onset due to unique landscape features may create refugia where bats may
persist later than or emerge from hibernation earlier than average, the
lack of any previous broad-scale estimates for this critical variable
highlights the need for this study. Prior work (Humphries et al. 2002,
Hayman et al. 2016) had defined the hibernation period a priorias the yearly number of nights with a mean nightly temperature below
freezing. Our results suggest that substantial improvements in the
estimation of hibernation duration can be made by including elevation,
latitude, and the number of days with frost. The number of days of
frost, rather than the number of days below freezing, and the
counter-intuitive negative coefficients for both Northing (-0.45)
and DEM (-0.04) in the model suggest that there is more nuance to
the relationship between bats and low temperatures than currently
understood. Our model is potentially biased in part by the
over-representation of Canadian data, low elevation sites, and the
collinearity of elevation and latitude with other explanatory variables.
Notably, however, when included in univariate models, the coefficient
signs regress as expected with the coefficients increasing with latitude
and elevation; yet the univariate models do not predict hibernation
duration as well and had higher AIC scores. Because we were interested
in prediction, we kept the best model by AIC; however, clearly more work
is required to understand what predicts overwinter duration in bats.
Also, there were few estimates of hibernation duration from the
western-most US states and the more southern latitudes within the
species’ distribution. These factors likely impacted model results in
unpredictable ways and highlights the need for additional data
collection.
Species such as M. lucifugus may not hibernate across their
broadest summer distribution, but likely seek out locations with more
favourable conditions to overwinter. The maximum winter hibernation
duration predicted within the distribution of M. lucifugus was a
month and a half longer than the longest observation within our dataset,
and this did not consider the portion of the species’ distribution that
extended into the Arctic Circle. In all probability, bats likely do not
overwinter within these regions for multiple reasons. First, while our
survival models predict that an uninfected bat could survive the longest
predicted winter hibernation, the necessary roosting microclimate
conditions may not exist on the landscape (Perry 2013, McClure et al.
2020). A series of complex interactions between surface features
(e.g., slope, aspect, elevation, suitable crevices) or cave
features (e.g., number of entrances, air flow, depth) ultimately
define when and where suitable hibernacula conditions exist (Perry 2013,
McClure et al. 2020). These site level determinants of microclimate
conditions make it difficult to define a relationship between
landscape-level features and the available subterranean conditions and
create challenges in attempting to predict where suitable hibernacula
conditions exist (McClure et al. 2020). Despite this, our use of
modelled subterranean temperatures offers an improvement over assuming
either static optimal conditions or mean annual surface temperature used
in Hayman et al. 2016. Second, and perhaps more importantly,
regions where extended winters reduce the summer active period to
<100 days likely create significant challenges to reproductive
success. With a gestation period of ~60 days (O’Farrrell
and Studier 1973, Kurta et al. 1989), a female bat would be hard pressed
to gestate, nurse, and wean young, while still allowing the young of the
year time to fatten sufficiently to survive such an extended hibernation
period. These results highlight the fact that only a subset of summer
distributions may be suitable for overwinter survival, an idea rarely
considered in the definition of bat species’ distributions.
Localized clines in body size and body mass of M. lucifugus have
previously been recorded (Lausen et al. 2008, Lacki et al. 2015). When
we compare more detailed metrics of body composition (lean mass and body
fat content), however, these clines are better understood: the lean mass
of bats generally stays consistent, while the difference in body mass is
due to increases in fat. Our model selection suggests that variation in
the duration of winter hibernation may in part drive variation in both
body mass and fat stores across the range of the species. The
relationships between mass (and thus fat) and latitude and days below
freezing also suggest stronger selection pressure for heavier bats in
more extreme conditions. While still useful, the relationship between
the selected abiotic variables and body mass of bats showed strong
spatial autocorrelations among residuals, and there may be additional
continental-scale drivers or local determinants not investigated in this
study.
The scaling relationship identified between pre-hibernation fat stores
and body mass is a departure from the fixed 30% value used in previous
energetic modelling studies (Humphries et al. 2002, Hayman et al. 2016)
and is supported by contemporary findings (Cheng et al. 2019). More
localized body mass–body fat relationships may exist, yet without
increased data resolution drivers of the true relationship will remain
difficult to assess. Here we assumed bats did not forage during
hibernation, but some bats (primarily from southern hibernacula) have
been known to forage over winter (Bernard and McCracken 2017). Without
data, we were required to assume bats relied exclusively on
pre-hibernation fat stores.
For our modelled roost conditions, virtually all uninfected M.
lucifugus could survive the estimated duration of winter. Observed
rates of survival among uninfected overwintering bats is high (Boyles
and Brack 2009) and bats are likely capable of overwintering across most
of their summer distribution where suitable hibernacula exist. These
results are an improvement over previous models which did not predict
survival where hibernation duration > 6 months (Hayman et
al. 2016) despite our prediction that some 51% of the study extent may
experience winters longer than that. In previous models, roosting
microclimatic space was derived exclusively from surface metrics (i.e.,
mean annual surface temperature and relative humidity). Our use of a
static, optimal roosting scenario served as a baseline for a best
available temperature scenario and provided a more biologically relevant
conditions for M. lucifugus, as bats are known to preferentially
roost in these conditions when available (Thomas and Cloutier 1992,
Haase et al. 2019). In areas where WNS has devastated hibernating
colonies of M. lucifugus , available microclimates are often
warmer with temperatures reaching 10°C (Perry 2013).
This warmer microclimate has a significant impact on energy expenditure
during hibernation (Figure S4). Despite this, our predictions for
overwinter survival using estimates of the best roosting temperatures
available suggest that survival may still be possible, if bats use the
coldest areas within the cave or mine system. In a rare ray of hope, all
of the hibernation temperatures that we recorded in the West were well
below the 10°C mark, with hibernating M.
lucifugus in northeastern Alberta and Northwest Territories roosting at
about 2˚C and 100% relative humidity (CLL, unpublished data ).
While the high relative humidity is generally beneficial to the growth
of P. destructans (and thereby a promoter of WNS pathology), the
cooler temperatures may slow fungal growth in comparison to the warmer
roosts of the Eastern United States.
Our model predicted uninfected bats to emerge from hibernation with
remaining fat quantities far greater than the amount of fat thought to
be needed to hibernate for the entire duration of winter. Some of this
may be an artifact of our modelling, as we may be missing additional
energetic costs such as flight during the arousal periods or sex-related
differences, and we did not model deviance from the most optimal arousal
patterns that can result from arousals of individuals sharing the
hibernacula (neighbour-initiated arousals; Hayman et al. 2010, Jonasson
and Willis 2012, Turner et al. 2015, Czenze et al. 2017). Alternatively,
remaining fat stores may be retained as a buffer against adverse abiotic
conditions experienced after emergence, especially among females that
undergo pregnancy immediately upon exit from hibernation (Johnson et al.
2017, Czenze et al. 2017) and whose reproductive success stands to
benefit from a longer growing season. Early emergence would provide a
selective advantage to the young of the year, as even one or two extra
weeks foraging on the landscape could increase fat stores, making them
more prepared for hibernation (Reynolds and Kunz in press). Currently,
little is known about the energetic demands of the emergent bats as they
return to the landscape, and accurate parameterization of this factor
could significantly change our definition of survival capacity and
increase our estimates of WNS-related mortality.
Modelled hibernation survival predictions of bats infected with P.
destructans at either \(4\)˚C and 98% relative humidity or using the
best available temperature do not match observations from the Eastern
United States where mass mortality events have occurred due to WNS
(Blehert et al. 2009, Frick et al. 2010, 2015) (23,24,54). While our
analysis did demonstrate infection with P. destructansdramatically increases the amount of energy expended during hibernation,
nearly 95% of all cells analysed predicted survival despite infection.
Interestingly, however, the areas with the greatest increase in
hibernation energy expenditure using the best available temperature were
much more in line with regions where bat populations have experienced
the greatest mortality.
Irrespective of the absolute values for survival predicted within this
work, our modelling predicts that M. lucifugus populations where
WNS is currently absent, especially those along the Rocky Mountains,
Alberta, British Columbia, and Alaska will require similar increases in
energetic expenditure as populations currently impacted by WNS. Thereby,
if the increase in energy expenditure results in the same pattern of
mortality, M. lucifugus populations in western North America may
be expected to suffer mortality events similar to those experienced in
the eastern and central populations (Frick et al. 2010, 2015). The long
duration winters, especially in northern British Columbia, northern
Alberta, Alaska, Yukon, Northwest Territories, and portions of the Rocky
Mountains, may result in severe WNS-associated pathology and disruption
to hibernation physiology, although use of cool available hibernacula
microclimates in some of these areas may slow fungal growth (Reeder et
al. 2012, Verant et al. 2014). Identifying and describing roosting
microclimates in these areas will allow for better predictive models at
a regional scale. Some northern hibernacula may provide a refugia forM. lucifugus infected with WNS; however, this cannot be defined
until the availability of microclimates and spring energy requirements
are quantified. For example, if gleaning of arthropod prey in spring is
typically required for successful reproduction in northern latitudeM. lucifugus (Talerico 2008, Kaupas and Barclay 2017), then the
extra energy expenditure associated with gleaning (Norberg et al. 1987)
may require additional fat stores and WNS-related mortality rate may in
fact be higher than predicted. Additionally, even if WNS related
mortality is not directly observed, reproductive success may decline
resulting in more long-term population decline.
The outputs of the energetic model that we applied are sensitive to a
number of parameters and assumptions (Haase et al. 2019). The
hibernation energetic model is largely derived from first principles and
deviations in parameters, especially those defining the frequency or
duration of arousal (cluster-based arousal, partial arousals,
disturbances, etc. 8) or increasing these costs (e.g. increased number
of mid-winter flights or disease pathophysiology), have the potential to
alter the amount of resources required to survive hibernation. Roost
microclimates are important to survival predictions and impact bat
energetic and fungal growth dynamics (Marroquin et al. 2017), and
further study is required to understand how relative humidity may vary
across the landscape and within hibernacula.
Overall, this work
represents an effort to iteratively refine both individual and landscape
models of bat hibernation physiology and the impacts of WNS on bat
populations. By specifically addressing the spatial heterogeneity of
both abiotic phenomena and host traits, we offer some of the most
detailed predictions for the potential impacts of WNS on M.
lucifugus as P. destructans continues to spread through western
North America.