Large scale geographic differences in magnitude of seasonal
changes of braincase height and body mass in S. araneus
Our results from the literature review confirmed large variation in the
intensity of Dehnel’s Phenomenon between populations. The data on
decrease and regrowth of braincase height, brain mass and body mass inS. araneus are compiled in Table S1 (Supporting Information), and
the list of corresponding references in the Supporting Information file.
Mean ± SD decrease in braincase height from first summer peak to winter
minimum was 13.4 ± 2.4% and regrowth from winter subadults to
overwintered adults was 10.3 ± 2.8%. Proportion of braincase height
decrease was positively correlated with latitude, longitude and their
interaction (Fig. 1, Table 1) but not with altitude (Table 1). The large
amount of variation in the intensity of Dehnel’s Phenomenon between
natural populations is consistent with the great flexibility of skull
changes observed in the captive experiments when ambient temperature was
manipulated (Lázaro et al. , 2019). Specifically, when analyzing
braincase height variation across populations at each age stage, we
found a negative correlation of braincase height with longitude and with
the interaction of longitude and latitude at both the small subadult and
regrown adult stages (P (sub.-long.) < 0.05;P (sub.-long.:lat.) < 0.05; P (ad.-long.)
< 0.05; P (ad.-long.:lat.) < 0.05), but no
trends along with other variables. This means that braincase height of
subadults and adults, but not of juveniles, decreased towards the
Northeast. We found a positive correlation in the magnitude of the
decrease of braincase height with temperature seasonality, annual
temperature range, and precipitation seasonality. We also found a
negative correlation with isothermality and mean temperature of the
driest quarter (Table 2). This suggests a link between braincase height
decline and the intensity of seasonality, with a positive gradient
towards more continental climate. This is also supported by the
correlations we found between the intensity of Dehnel’s Phenomenon and
climate variables associated with seasonality. As it has been postulated
that the size decrease stage of Dehnel’s Phenomenon occurs in
anticipation of changes in climate and resource variability (which is
influenced by climate) this supports the hypothesis that shrews shrink
in preparation of winter to lower their energetic needs and thus
resource demands.
Even more interesting is then that we did not find a correlation between
braincase height regrowth and any geographical variable (Table1).
Braincase height regrowth was only positively correlated with
precipitation during the warmest quarter (Table 2). It is striking that
adult body mass as well as the size of several crucial organs greatly
exceed subadult and even juvenile mass, while the size of the brain and
skull are largest in juveniles and only partially regrow after the
winter decrease (Pucek, 1965). Similarly, energy expenditure is by far
the largest in these regrown adults (Schaeffer et al. , 2020) even
they are exposed to much higher ambient temperatures than the small
winter subadults. The most important investment shrews face during the
adult period is reproduction, associated with territory expansion,
territorial fights, and massive enlargement of the testes in the males
and the production of several large litters in the females (Vlasák,
1996, 1998). The correlation of brain case height with precipitation
might then be linked to the availability of high quality food during
regrowth and reproduction since the abundance of the main prey of common
shrews, the common earthworm (Churchfield, Rychlik, & Taylor, 2012), is
highly dependent on soil humidity. For both sexes reproduction appears
to be a more or less terminal investment as most individuals die shortly
after. Thus, regrowth with such a disproportional investment into mass
instead of the brain might be driven by the demands of reproduction.
This would mean that decrease and regrowth phases of Dehnel’s phenomenon
have evolved under different evolutionary pressures, which are caused
and modulated by independent factors. Decrease intensity would then
mainly be determined by the physiological limits of shrews, and the
regrowth by reproduction. Across all reviewed populations, mean body
mass decreased by 21.2 ± 6.2% and regrew by 81.9 ± 18.2%. Similar to
braincase height, the extent of body mass changes varied between
populations in the analysis of literature data. We found a positive
correlation between body mass decrease with longitude, and with the
interaction of latitude X longitude, but not with altitude or in this
case latitude alone (Fig. 1, Table 1). This matches results from a
previous study where no correlation between winter body mass decline and
latitude was found in S. araneus either (Ochocińska & Taylor,
2003). Again, matching results of skull measures, body mass regrowth
were not correlated with any geographical variable.
When comparing the three size extremes, there was no geographical
pattern in juvenile or adult body mass. However, there was a significant
negative correlation of body mass of winter subadults with latitude,
longitude and their interaction, i.e. winter subadults had lower body
mass towards Northeastern populations (P (long.) < 0.05;P (lat.) < 0.001; P (long.:lat.) <
0.01). We found significant correlations between body mass decrease and
most climate variables. In contrast, regrowth intensity was only
negatively correlated with mean temperature during the driest quarter
(the year quarter when precipitation is lowest) and, similar as in
braincase height, positively correlated with precipitation seasonality
(expressed as coefficient of variation, the more variation the more
concentrated the precipitation on a period of the year; Table 2). Again
these patterns support the hypothesis that different evolutionary
drivers are responsible for the decrease - shrinking as an adaptation to
save energy during cold periods with low resource availability, and the
increase - growing a large body size well adapted for territory defense
and to maximize reproductive output especially in females.
While the changes in body mass we describe are dramatic, seasonal
fluctuations in body mass are common in mammals. For example, North
American beavers (Castor canadensis ) lose 9-12% of their body
mass during autumn and winter, mainly because of the metabolic use of
their fat stores (Smith & Jenkins, 1997). During hibernation, marmots
can lose 32% of their body mass (Lenihan & Vuren, 1996), and hedgehogs
15-28% (Haigh, O’Riordan, & Butler, 2012). These fluctuations are
mainly caused by changes in fat tissues. However, none of these species
exhibit the changes in skull and brain size, which are characteristic of
Dehnel’s Phenomenon, as well as the changes in spine length (Saure &
Hyvärinen, 1965; Hyvarinen, 1969). Thus, changes in body mass are not
exclusive of Dehnel’s Phenomenon and should only be used to describe
Dehnel’s Phenomenon in combination with other variables, as the
combination all these morphological changes – body mass, brain mass,
skull size and spine length – are inherent parts of the unique Dehnel’s
phenomenon (see also general remarks below).