4.
Discussion
We examined intra-population variation in energy density and storage
energy, temporal dynamics in energetics, and the influence of sea ice
dynamics on WH polar bear population energetics from 1985 to 2018. All
age/sex classes, except adult males and adult females with offspring
declined in energy density over time, all classes except adult females
with offspring declined in storage energy over time, and reduced energy
values were associated with earlier sea ice breakup across classes.
Furthermore, we found that the WH population energy density and storage
energy both declined significantly over time in relation to earlier sea
ice breakup and longer lagged open water periods. This research is
important for monitoring trends in individual physiological condition,
understanding implications for population dynamics, and predicting
future responses of polar bears to climate warming.
Age/sex class
patterns
We found variation in energetic dynamics from 1985 to 2018 among WH
polar bear age/sex classes. All classes except adult males and adult
females with offspring showed decreases in energy density over time, and
all classes except adult females with offspring declined in storage
energy over time, with the most significant declines for solitary adult
females and yearlings. Energy density is determined as the ratio of
storage energy to body mass (Molnár et al. 2009) and was less variable
than storage energy. In contrast, storage energy indicates the total
amount of energy in an individual (Molnár et al. 2009) and is therefore
more sensitive to changes in body condition given that the amount of
storage energy is lower at smaller body sizes. Decreases in storage
energy indicate that the bears had less energy available for
maintenance, growth, and survival (Molnár et al. 2009; Sciullo et al.
2016). These results are similar to Sciullo et al. (2016) where WH polar
bear storage energy declined from 2004-2013 across classes. Due to the
relationship between energy reserves/body condition and fitness (Jakob
et al. 1996; Sciullo et al. 2016), the observed reductions in available
energy will influence survival and reproduction, with consequences for
individual fitness. The significant reduction in energy density and
storage energy over time for solitary adult females and the significant
reduction in storage energy for yearlings further indicates the
vulnerability of these classes to future environmental changes. The
small body size, dietary constraints, energetic demands of growth, and
inexperienced hunting skills of younger bears make them more vulnerable
to reductions in sea ice and thus prey availability (Rode et al. 2010;
Thiemann et al. 2011a; Pilfold et al. 2016; Johnson et al. 2019; Laidre
et al. 2020). In contrast, adult males can best buffer against
sub-optimal conditions given their larger body size, broader diets, more
effective hunting skills, and ability to take kills away from smaller
bears (Stirling 1974; Regehr et al. 2007; Thiemann et al. 2011a; Pilfold
et al. 2016; Johnson et al. 2019). These patterns highlight the
importance of continued monitoring of the condition of young bears.
The reproductive status of adult female polar bears in WH influenced
their energy patterns. Solitary adult females had higher energy density
and storage energy than adult females with offspring, but solitary
females experienced significant declines in both energy metrics over
time whereas females with offspring had lower but relatively stable
energy values. These results are consistent with observations that
solitary adult females have higher body condition due to their
accumulation of body fat in preparation for the energetic requirements
of gestation and lactation (Atkinson & Ramsay 1995; Thiemann et al.
2006; Sciullo et al. 2016). The amount of energy a solitary adult female
accumulates before denning determines the likelihood of successfully
producing cubs as well as subsequent cub survival (Atkinson & Ramsay
1995; Derocher & Stirling 1994, 1996, 1998) and litter size (Laidre et
al. 2020). Decreases in solitary adult female condition can therefore
translate into a decline in cub survival and reproductive success, both
of which have already been observed in WH (Derocher & Stirling 1995;
Stirling et al. 1999). The observed declines in solitary adult female
energy may reflect difficulty in accumulating sufficient resources. In
contrast, females with offspring have lower energy reserves due to
lactational energetic demands (Derocher et al. 1993; Arnould & Ramsay
1994; Atkinson & Ramsay 1995). There is likely a threshold of energetic
reserves that is required to successfully reproduce (Molnár et al. 2010;
Reimer et al. 2019). For instance, Derocher et al. (1992) found that the
lowest weight of an adult female that was known to have successfully
reproduced was 189 kg, while Robbins et al. (2012) indicated that
females require 20% body fat when entering a den to successfully
produce cubs. Similarly, our results indicated that adult females with
offspring had relatively stable energy density (median: 19.8 MJ
kg-1; Fig. 2) and storage energy (median: 2241 MJ;
Fig. 3), suggesting energetic thresholds for reproduction. In agreement
with Robbins et al. (2012), our results highlight the vulnerability of
females with offspring due to their already-reduced energetic reserves,
as well as the sensitivity of solitary adult females that need to
accumulate sufficient energy in preparation for future reproductive
events yet are nutritionally stressed.
Our study also demonstrated the association between age/sex class
energetic patterns and environmental conditions. Reduced energy density
and storage energy were associated with earlier sea ice breakup and this
relationship was most significant for adult males, subadult
males/females, and COY. These results are consistent with the
relationship between earlier breakup and reduced body condition in WH
(Stirling et al. 1999; Sciullo et al. 2016). Our finding that the lagged
open water period was an important predictor for solitary adult female
storage energy suggests that the previous year’s sea ice conditions
influenced the ability of solitary females to accumulate energy reserves
in preparation for reproduction. Similarly, Derocher & Stirling (1994)
found that an adult female’s condition in the previous year was a strong
determining factor for reproductive success in WH. In addition, the
previous year’s breakup date influenced body condition of Davis Strait
polar bears, whereby earlier breakup in the previous year forced bears
ashore earlier, resulting in poorer body condition (Galicia et al.
2019), while Baffin Bay polar bear body condition was associated with
the previous ice-free period (Laidre et al. 2020). Our observed decline
in solitary adult female energy and the relationship with the lagged
open water period suggests that females may not be able to recover from
poor conditions in previous years, which may build up over time and
affect lifetime reproductive success. Overall, our results indicate that
polar bear energetic balances are negatively affected by sea ice
declines and that vulnerable demographic groups include younger bears
and adult females.
Population
trends
WH total population energy density and storage energy declined
significantly over the 34 year study period. Both energy metrics were
correlated with estimated abundance, which indicates that the population
energy decline was related to reduced population abundance. The WH
population has declined from approximately 1185 to 806 bears over the
period of 1987 to 2011 (Lunn et al. 2016) with a continued decline in
recent years (ECCC unpublished data, 2019); furthermore, WH body
condition has also declined over time (Derocher & Stirling 1995;
Stirling et al. 1999; Sciullo et al. 2016). Reduced population abundance
in addition to declining body condition of individuals may both
contribute to the observed decline in the total energy stored in this
population. Declines in individual energy balances and subsequent
consequences for survival and reproduction illustrate the mechanism
linking climate change and population dynamics (Yodzis & Innes 1992;
Humphries et al. 2004; Molnár et al. 2009, 2010; Pagano et al. 2018).
Understanding the ecological mechanisms behind demographic change is
important for wildlife management and can improve our predictions about
how populations may respond to future climate warming (Cherry et al.
2009; Pagano et al. 2018, Reimer et al. 2019).
We found that western Hudson Bay experienced significant long-term
change in sea ice dynamics, with a lengthening of the open water period
by approximately 9.9 days per decade. WH polar bear population energy
density and storage energy were both significantly reduced when sea ice
breakup was earlier and the lagged open water period was longer,
demonstrating a linkage between declining sea ice and reduced energetic
balances. Sea ice is probably the most important single mechanism
influencing polar bear demographic responses in the changing Arctic
marine ecosystem. Our results are consistent with the association
between earlier breakup/later freeze-up and declining body condition
(Stirling et al. 1999; Obbard et al. 2016; Sciullo et al. 2016; Laidre
et al. 2020), altered foraging ecology (McKinney et al. 2009; Johnson et
al. 2019), and reduced reproduction/survival rates and abundance (Regehr
et al. 2007; Rode et al. 2010; Lunn et al. 2016; Obbard et al. 2018) in
various polar bear populations including WH, Southern Beaufort Sea,
Southern Hudson Bay, and Baffin Bay. Changes to energetic intake and
expenditure in response to sea ice dynamics have consequences for
energetic balances (Pagano et al. 2018). Polar bear energetic intake is
reduced when breakup occurs earlier and freeze-up occurs later because
the spring hunting period is shortened and bears are forced to fast on
land for longer periods in poorer condition (Cherry et al. 2009, 2013;
Rode et al. 2014, 2018). Meanwhile, energetic expenditure increases due
to declines in optimal habitat (Durner et al. 2009; Stern & Laidre
2016), increasingly fragmentated and drifting sea ice (Mauritzen et al.
2003; Sahanatien & Derocher 2012; Auger-Méthé et al. 2016; Durner et
al. 2017), and long-distance swims as a result of more open water
(Durner et al. 2011; Pagano et al. 2012; Pilfold et al. 2017). We found
that the open water period increased from 105 days in 1985 to 145 days
in 2018, with a maximum of 166 days in 2015. An increase in the fasting
period from 120 days in the 1980s to 165 days was predicted to lead to
higher starvation rates for adult male polar bears in WH (Robbins et al.
2012), while 180 day fasting was predicted to lead to additional
increases in starvation and mortality rates (Molnár et al. 2010, 2014;
Pilfold et al. 2016). Similarly, our predictions indicated that at 180
day previous fasting period, population energy density and storage
energy would decline to 58% and 63% lower than the mean estimated
values, respectively. Decreases in the length of the spring foraging
period are predicted to lead to declines in female polar bear expected
fitness (Reimer et al. 2019) and higher fasting rates have occurred
concurrently with reductions in survival and abundance (Cherry et al.
2009; Rode et al. 2014, 2018). Our predicted declines in WH population
energy at longer fasting periods would have implications for individual
fitness, population vital rates, and productivity. Moreover, the
importance of the lagged open water period suggests that there are
cumulative effects of prior conditions that affect the ability of bears
to recover from previous nutritional stressors. Hudson Bay is expected
to undergo continued sea ice loss in the future and WH polar bears are
therefore at risk of further declines to energetic balances leading to
reduced survival rates for young bears and decreased reproductive
success, which may ultimately result in a functionally extinct
population (Castro de la Guardia et al. 2013; Pilfold et al. 2016).
Ecosystem implications
While the Arctic marine ecosystem has already experienced various
alterations due to climate warming (Wassman et al. 2011), our observed
decline in population energy of a top predator may have further
implications for ecosystem dynamics. Altered top predator population
dynamics have the potential to cascade through ecosystems and influence
trophic interactions and food web dynamics (Pace et al. 1999; Schmitz et
al. 2000; Frank et al. 2005). For example, reduced body size of top
predators has been associated with a weakening of predation pressure on
lower trophic levels (Shackell et al. 2010). A potential consequence of
reduced WH polar bear energetic balances is therefore altered trophic
interactions with their primary prey species, ringed seals (Pusa
hispida ). However, Hudson Bay ringed seals have similarly shown
population declines over time (Young et al. 2015; Ferguson et al. 2017);
thus, our limited understanding of changing predator-prey interactions
in the Arctic would benefit from long-term monitoring of ecological
parameters across multiple trophic levels. Our study provides insights
into potential mechanisms linking WH polar bear population dynamics and
sea ice decline. As the Arctic continues to warm, polar bears can act as
an indicator species to improve our understanding of changing ecosystem
dynamics (Rode et al. 2018). Our research reinforces the importance of
long-term monitoring of individual physiological condition and broad
population patterns.