4. Discussion
4.1 Decrease in skull and
thus overall size over time (1953-2004)
Skull dimensions of juvenile and adult S. araneus significantly
decreased during the study period (Table 1). Skull length, the
often-used proxy for overall body size, decreased significantly in
juveniles between 1953 and 2004 and in adults between 1970 and 2004.
Skull height and width also decreased significantly in juveniles and
adults. This outcome adds to the very mixed picture of the change in
body size in mammals under global climate change. The analysis of 50
species of rodents from seven families revealed no significant temporal
change in body size (represented mainly by skull dimensions) in 29
species, a significant decline in 13, and an increase in size in eight
species (Nengovhela et al. 2020). Of the three carnivore species in
which skull size was measured in the second half of the 20th century and
analysed in the context of climate change, skull size showed a
significant increase in two species and a significant decline in the
other (Yom-Tov et al. 2008, 2010a, 2010b). Thus, S. araneus in
Białowieża adds to the number of rather rare cases of decreased body
sizes among mammals.
The decrease in body size in S. araneus in Białowieża is in
contrast with the observed increased body size (body and foot length) inSorex cinereus in Alaska during the second half of the twentieth
century along with increasing temperature. In S. cinereus, the
increase was presumably due to higher food availability in winter as a
result of improved weather conditions for its prey (Yom-Tov and Yom-Tov
2005). We argue that the smaller size of S. araneus in summer
could be an effect of increasing drought leading to reduced food
availability. The negative impact of decreased soil moisture on the
abundance of epigeic and endogeic invertebrates has been well documented
(Coyle et al. 2017; Singh et al. 2019). S. araneus strongly
depend on the abundance of food because their metabolic rates measured
under natural conditions equals 258% of the value predicted for an
average mammal of the same body mass (Ochocińska and Taylor 2005).
Drought leading to soil moisture deficits may specifically impact
earthworms, the main food source of S. araneus . S. araneusprefer humid habitats with humus-rich soil, as in our study plot, which
harbour large numbers of earthworms (Shchipanov et al. 2019).
In support of this, the decrease in skull length in adults between 1970
and 2004 was significantly correlated with the increase in soil moisture
deficit, which started to increase in the Białowieża Forest in the 1970s
and accelerated in the 1980s (Figures 4e and S2e) as a result of
decreasing precipitation (Figures 4d and S2d) and increasing
temperatures (Figures 4C, S2a, S2b). The decrease in skull height in
both juveniles and adults was correlated with an increase in the mean
lifetime temperature (Table 2) and was stronger after 1970, which
coincided with the inflection point in precipitation and soil moisture
deficit.
There were no regular measurements of the soil water level in the
Białowieża Forest before 1985, and those that existed were not
comparable with later measurements. However, between 1985 and 2001, the
water level decreased in mixed deciduous biotopes by 40 cm. This
resulted from an increase in temperature, a decrease in rainfall, and
winters without snow and thus a lack of water accumulation at the
beginning of the vegetation period (Pierzgalski 2002). The progressive
decrease in the soil water level was certainly magnified by the intense
drainage work on peatlands in the eastern Belorussian part of the
Białowieża Forest in the late 1950s. The average biomass of earthworms
in the upper soil layer in the mixed deciduous areas of the Białowieża
Forest was 42.2 g m-2 between 1997 and 2000 and
depended on soil moisture: it was highest in spring, decreased to 22%
of the spring values in summer, and increased to 41% in autumn
(Kowalczyk et al. 2003). This pattern followed the annual course of soil
humidity in the Białowieża mixed deciduous forest (Pierzgalski 2002).
Earthworms were not available in the forest in winter (Kowalczyk et al.
2003).
While the increasing lifetime temperature affected both juveniles and
adults, resulting in lower skull heights, the adults were additionally
affected by the conditions in the preceding winter. Milder minimum
temperatures in February and decreasing number of days with snow cover
in the coldest months of January and February resulted in adults with
lower skull heights (Table 2). The lack of snow cover leads to freezing
of the upper soil layer and substantially reduces the abundance of
various arthropods, which are important components of the winter diet inS. araneus (Templer et al. 2012). Snow generates a relatively
mild and stable subnivean microclimate in the litter layer where the
shrews live (Coulianos and Johnels 1962; Churchfield et al. 2012) that
is not only favourable for their prey but may also diminish the costs of
thermoregulation and consequently the food requirements of the shrews
(Aitchison 1987). However, the importance of the insulative value of
snow for adult S. araneus is less convincing, as concluded by the
weak relationship between skull height and the number of days with snow
cover at least 5 cm thick in January and February (Table 2).
Skull dimensions in juvenile S. araneus from the northeastern
part of European Russia were correlated with temperature and
precipitation from 1976 to 2003, but in contrast to our results, there
was no clear directional trend to the change (Poroshin et al. 2010).
This might have been caused by the lack of clear change in weather
parameters and/or the shorter time period covered in that study than in
ours.
Recent evidence suggests a relationship between the tendency of body
size to decline over time and metabolic rates in small mammals. In
rodents that do not use torpor, there is a significant negative
correlation between the temporal body mass change and basal metabolic
rate (BMR; Villar and Naya 2018). Species with a high BMR have become
smaller in the last six decades. The size decrease in S. araneus ,
with their lack of ability to hibernate, and the BMR in juvenileS. araneus, which equals 278% of the value predicted for an
average mammal of the same body mass (Ochocińska and Taylor 2005), fits
this pattern. It is likely that the relationship between the body size
decrease and high metabolic rate is generally true for soricine shrews.
Three out of four Sorex species (not including S.
cinereus ) had a decreased body mass during the 20thcentury, and two of them had a significantly decreased body mass (Naya
et al. 2017). However, data from different ages and thus Dehnel stages
were pooled in this study, potentially affecting the results and hiding
the effects of seasonal body size changes.
4.2 Changes in the
magnitude of Dehnel’s phenomenon (1955-1985)
We found that the decline in skull height from summer to winter inS. araneus from the Białowieża Forest became stronger between
1955 and 1985 (Figures 6a and b). We standardized skull height with
skull length in the analysis of Dehnel’s phenomenon to describe changes
in relative skull height. Relative skull height is strongly correlated
with brain size (Bielak and Pucek 1960; Lázaro et al. 2018). Thus, our
results also reflected changes in the magnitude of brain size changes.
Initially, the skull height of juveniles did not differ between July and
August from 1955 to the 1970s (Figure 6b). The skull height in these two
months then diverged over the following years (Figure 6b). The smaller
skull height in August than in July after 1970 meant that the decrease
in skull height started earlier. The magnitude of the decrease was also
higher because the relative skull height of winter subadults decreased
even more over time (Figure 6).
What is the environmental background of these temporal changes? The
increasing magnitude of Dehnel’s phenomenon was largely due to the
significant decline in the skull height in January and February
subadults (Figure 6). Unfortunately, the numbers of available subadult
specimens each year were too low to statistically correlate them with
weather conditions. The significant decrease in January temperatures
until 1972 might explain the increasing magnitude of Dehnel’s
phenomenon, but January temperatures did not change significantly later
on. A seasonal decrease in skull height in S. araneus is thought
to be anticipatory of harsh winter conditions. The question then arises
whether weather conditions in summer and autumn can have direct or
indirect impacts on the skull height in winter. Mean daily July
temperatures did not change from 1955 to 1985, but August temperatures
significantly increased in this period. One may speculate that
increasing temperatures and possibly drought could decrease the
availability of earthwormsand other invertebrates in August and speed up
the decrease in skull height over time (as discussed above), leading to
a decrease in skull height in winter. Lower amount of invertebrate food
in summer could lead to a greater reduction of resources in winter.
Although we did not find a significant change in the soil moisture
deficit in August between 1955 and 1985, the sharper skull height
decrease with the increasing mean temperature in the driest quarter of
the year in a geographic comparison of S. araneus (Lázaro et al.
2021) supported the hypothesis that soil moisture deficit might be an
important factor for this species. To elucidate this, the role of summer
and winter availability of food in Dehnel’s phenomenon should be tested
under controlled laboratory conditions.
We also found a significantly greater skull height regrowth from 1955 to
1985, which resulted from a steep decrease in skull height in the
subadults, while adults did not change (Figure 6). Almost nothing is
known about the drivers of this regrowth, which are presumably different
from those of the decrease and are likely associated with preparation
for the terminal reproductive period in shrews (Lázaro et al. 2019,
2021). Comparison of the skull height regrowth in different S.
araneus populations revealed only one correlation with weather
parameters, namely, a positive correlation with precipitation during the
warmest quarter of the year (Lazaro et al. 2021). This also points at
changes in food availability.
In summary, we documented a decrease in overall size as represented by
absolute skull height and length in the 52-year (1953-2004) skull series
and identified increasing temperature and drought as the main correlates
of the decrease. Interpreting the results regarding Dehnel’s phenomenon,
which increased in magnitude because of a sharp size decrease in winter
subadults, was more difficult. Our dataset about winter subadults
stopped shortly before the time point when climate change became
significant, and it would have been interesting to see how subadult size
developed after this. There are strong indications that there are
important effects of climate on food availability that indirectly cause
trends in both skull size and the magnitude of Dehnel’s phenomenon.
However, this must be clarified experimentally.
With continued climate change, all the parameters that we found to be of
importance for the size of the common shrew and its unique winter
adaptation are expected to increase even more strongly. The shrew’s
distribution ranges may be affected by this, as many regions may become
too hot and/or dry for these and other cold-adapted animals.