DISCUSSION
We show that criticality occurs in the hibernation dynamics of dormice.
Around fold bifurcation points, a tiny change in ambient temperature
pushes body temperature across boundaries of alternative states (from a
euthermic temperature to a hibernation temperature) through large
transitions. These critical transitions are characterized by flickering
and punctuated changes in body temperature. Flickering is a type of
complex dynamics that occur when a system rapidly moves back and forth
to the vicinity of an alternative state preceding the upcoming critical
transition (Scheffer et al. 2009; Dakos et al. 2013). In
our study, flickering of body temperature started far from bifurcation
points and it increased when the system approached these points. Thus,
flickering anticipated critical transitions in hibernating dormice, as
it likely does for dormice from the core of the range distribution and
for other hibernating mammals, when looking at the dynamics of body
temperatures (Hut et al. 2002; e.g. Talaei et al. 2011;
Hoelzl et al. 2015). In humans, flickering may also anticipate
physiological responses, such as epileptic seizures and narcolepsy
(Scheffer 2009; Yang et al. 2016). Together with flickering,
other indicators of EWS anticipated the approaching of critical
transitions in hibernation dynamics. Previous studies suggest that,
contrary to critical slowing down, flickering is associated with an
increase in both variance and lag-1 autocorrelation, as we found in our
study (Wang et al. 2012; Dakos et al. 2013). Nevertheless,
the rest of indicators were less informative and even erratic: for
instance, CH did not anticipate bifurcation, while DDJ metrics were very
noisy. As Dakos et al. (2012) pointed out when developing the
indicators, the performance of any indicator, as well as the
interpretations based on them, is likely depending on the features and
dynamics of the biological system studied.
Hibernation dynamics of dormice also have hysteresis, which shows the
tendency of body temperature to remain on the same attractor until
attaining a critical threshold value of air temperature, with the
particularity that bifurcations occurred at different air temperatures
for each of the two cyclic transitions. These cyclic transitions
resemble the dynamics of wake-sleep and microsleeps occurring for
circadian cycles in mammals (Yang et al. 2016). Since hibernation
is driven by seasonal climate, its dynamics follow cycles that are
locked into phase (Scheffer 2009). This type of complex cyclic dynamics
occur between coupled oscillators and commonly occurs in nature (e.g.
heart beating, reproductive events, and predator-prey fluctuations).
Epileptic seizures mentioned above occur by the phase locking of firing
in neural cells (Scheffer et al. 2009). In our study, locking of
forced hibernation by forcing winter occurs with 1:1 rhythm, which means
that little climate forcing is enough for locking (Scheffer 2009). Phase
locking occurs for global climatic indexes such as NAO and ENSO, which
are known to be coupled with a number of local seasonal ecological
processes.
Statistical indicators of EWS quantify critical transitions and
resilience for very different ecological systems (Scheffer et al.2015), and we show that these generic indicators can be also applied to
other dynamical systems sharing their fundamental properties, such as
physiological hibernation. Other physiologically critical transitions
during hibernation dynamics may occur and may be anticipated, such as
lipid structure and enzyme function of mitochondrial membranes from
liver, kidney, brown fat, and heart tissues. High-dimensional
physiological systems, such as blood cells with functional heterogeneity
or neurons involved in sleep-wake cycles, also show critical transitions
that can be predicted before bifurcation (Mojtahedi et al. 2016).
The same dynamics occur for homeostatic changes in hormone regulation,
immune responses, gene expression and asthma incidence (Krotov et
al. 2014; Trefois et al. 2015). Our capacity to anticipate
pathological changes and loss of resilience, e.g. due to opposite
physiological commitment to that intended in normal conditions, is
crucial for human health (Scheffer et al. 2018). Interestingly,
hibernation dynamics and human health converge due to the increased
scientific interest in the benefits of dormancy for humans in coping
with different stresses, e.g. the potential of a hibernating state in
astronauts for deep space travel (Lovegrove et al. 2014).
Similarly, EWS can be used to detect changes in the non-linear dynamics
of body temperature and the resilience of hibernating mammals due to
increasing climatic stress. Physiological variables can perform better
to anticipate non-linear dynamics than noisier ecological variables
(Perretti & Munch 2012; Benedetti-Cecchi et al. 2015), and the
former may be a good bio-indicator of ecological changes and temporal
variability in resilience. Given the potential consequences that
hibernation dynamics may have on population fluctuations and extinction,
there is a growing concern about the impacts of climate warming on
hibernating species (Inouye et al. 2000).
The influence of climate may be greater for species such as edible
dormice in our Mediterranean study area. Here, heat and drought waves
are associated and their frequency is increasing (Diffenbaugh et
al. 2007; Vautard et al. 2007), which is affecting
cold‐temperate forests, the preferred habitat of dormice (Peñuelas &
Boada 2003). The potential impact on hibernating mammals in many regions
is likely related to a loss of suitable habitat, mediated by climate
variability, and not to a direct impact on hibernation dynamics. This is
because hibernation is a very effective resilient physiological
mechanism to cope with climatic stress (Lebl et al. 2011; Boutin
& Lane 2014; Mitchell et al. 2018). Animals can adjust
hibernation to maximize fitness, because it influences life-history
traits such as recruitment by age and the onset of reproduction (Bieberet al. 2018). The evolution of hibernation has selected for a
very plastic trait. The duration of hibernation may change with seasonal
climate variability and with the availability of resources. For
instance, rising temperatures cause earlier emergence from hibernation
in the yellow-bellied marmot (Marmota flaviventris ), which has
led to a longer growing season and larger body masses before entering
hibernation (Ozgul et al. 2010). The demographic consequences
included higher adult survival and a sharp increase in population growth
rate. Hibernation in dormice shows large differences between populations
depending on local climate, and harsher and longer winter means longer
hibernation times, e.g. up to 11 months (Hoelzl et al. 2015).
Interestingly, life history strategies of dormice are very plastic
depending on those local climatic conditions, since as long as the
duration of hibernation increases, adult survival is higher and
fertility is lower (Pilastro et al. 2003; Ruf et al. 2006;
Lebl et al. 2011). Hysteresis, such as that shown by the studied
Mediterranean edible dormice, may also increase resilience by avoiding
the termination of hibernation earlier than the optimal time, which may
occur in regions where temperatures are sharply rising, especially
during winter (Mitchell et al. 2018). Experimental studies
looking at how environmental stress affects hibernation dynamics (e.g.
Siutz et al. 2018) are promising to assess the changes in leading
indicators of critical transitions. Exploring how criticality and
tipping points appear in different hibernating animals with different
evolutionary life histories and with varying ecological features may
also shed light on how resilience of physiological systems cope with
environmental stress.