1 Introduction
Global climate change affects animals in many ways, from phenology,
geographic distribution, and phenotypic traits to distributions and
population dynamics (Walther et al. 2002; Parmesan 2006; Gardner et al.
2011). Changes in phenotypic traits correlated with global warming
mainly involve temporal trends in body mass and size (Gardner et al.
2011), two traits that are pivotal for individual life histories (Sauer
and Slade 1987). Importantly, although mass and size are often used
interchangeably, their change arises from different underlying
physiological mechanisms. Mass is more sensitive to short-term
environmental conditions affecting fat stores and the mass of the
gastrointestinal tract and other organs (Piersma et al. 1999; Hume et
al. 2002; Canale et al. 2016).
How climate influences body size is often described based on Bergmann’s
rule, which in its commonly used version describes a positive
relationship between body size and latitude within species. Individuals
of many homeothermic species are smaller at lower latitudes where
temperatures are higher (e.g., Ashton et al. 2000; Ashton 2002). This
implies that a similar relationship should occur in response to
temperature change over time. It has been postulated that a decrease in
body size is the third universal response to contemporary global warming
in addition to changes in distribution and phenology (Gardner et al.
2011). Although the majority of studies did not find significant
temporal changes in the sizes of birds and mammals, there are many
examples of long-term body size and body mass changes (recorded over one
to several decades) correlated with global climate change. While a
decrease in size is indeed the major response in birds, the situation is
much less clear in mammals, where many species increase in size
(Teplitsky and Millien 2014; Naya et al. 2017; Nengovhela et al. 2020).
This increase in size is usually explained as a reaction to increased
food availability as a result of increasing temperatures (Yom-Tov and
Geffen 2011; Boutin and Lane 2014 and references cited therein).
Soricine (red-toothed) shrews, especially Sorex shrews, are an
excellent study system to investigate climate change-induced patterns in
species-level body size changes. They have extremely high metabolic
rates, much higher than expected for their body mass (Taylor 1998;
Ochocińska and Taylor 2005). Consequently, shrews require a constant
high food supply (Hanski 1994; Keicher et al. 2017). In addition, the
body size of several Sorex species, represented by skull length,
shows positive correlations with temperature and negative correlations
with latitude across their distribution range, contrary to Bergmann’s
rule (Ochocińska and Taylor 2003). It was suggested that food scarcity
during winter in cold northern climates is a major factor selecting for
small body size in shrews. This is in line with the “Resource Rule” of
McNab (2010), which posits that “mammalian species will become larger
or smaller depending on the size, abundance and availability of
resources”. A decrease in body size with latitude and in cold areas was
also found in the masked shrew, Sorex cinereus , in Alaska and was
also interpreted as related to better food resources in warmer areas
(Yom-Tov and Yom-Tov 2005). In agreement with this, the body size ofS. cinereus in Alaska increased during the second half of the
twentieth century along with increasing temperature, presumably due to
increasing food availability in winter (Yom-Tov and Yom-Tov 2005).
However, an increasing temperature, especially when coupled with a
decrease in precipitation, can also lead to a decrease in food
resources. Drought has a negative impact on the abundance of the shrews’
invertebrate prey (Coyle et al. 2017). This includes earthworms
(Lumbricidae), the main food of the common shrew, S.araneus(Shchipanov et al. 2019), the availability of which depends on high soil
moisture (Coyle et al. 2017; Singh et al. 2019).
The importance of small size in soricine shrews under unfavourable
conditions (caused directly or indirectly by climate) is also visible in
the remarkable seasonal morphological changes they exhibit.
Individual skeletal size in
endotherms remains more or less inert once full size is reached, which
occurs rapidly in small mammals, and climate change causes size changes
in the skeleton at the species or population level. However, soricine
shrews undergo a profound seasonal and reversible transformation:
individual seasonal shrinkage and regrowth of the skull and brain along
with other organs and tissues (Dechmann et al. 2017; Lázaro et al.
2017). This change in the skull
shape and height as well as the body mass of soricine shrews and some
other small high-metabolic animals is called Dehnel’s phenomenon (Dehnel
1949; Pucek 1963, 1970; Dechmann et al. 2017). After juveniles are fully
grown, their brain mass decreases by 21% on average, and skull height
decreases by 13% in S. araneus . Their brain mass reaches a
minimum value in winter and then partially regrows in spring (Lázaro et
al. 2021). Body mass, in contrast, decreases in anticipation of winter
and then almost doubles in spring as the animals achieve sexual
maturity. S. araneus, born in early summer, has a maximum
lifespan of approximately 14 months, and almost all individuals die
before the second winter (Pucek 1981). The size decrease in winter is
thought to be an adaptation to harsh climatic conditions in these
nonhibernating, high-metabolic animals. The low body mass in shrews in
winter has been hypothesized to reduce absolute food requirements when
food availability is limited (Mezhzherin 1964; McNab 1991; Taylor et al.
2013). Accordingly, small winter animals have the same mass-corrected
energy consumption as larger, first and second summer shrews, even under
ambient conditions with temperatures differing by as much as 30 °C
(Schaeffer et al. 2020). This results in absolute energy savings in
winter and correlates with reduced food requirements. Disproportionally
reducing the size of the brain, an energetically expensive tissue
(Aiello and Wheeler 1995; Isler and Schaik 2006), may lead to further
energy savings.
The magnitude of the decline in skull height in S. araneus , a
commonly used proxy for Dehnel’s phenomenon, increases towards the
northeast and is linked to large-scale environmental conditions and
probably also the local habitat structure (Pucek 1970; Lázaro et al.
2021). It is positively correlated with temperature seasonality, annual
temperature range, and other climate parameters, although no such
relationships have been observed with the skull height regrowth (Lázaro
et al. 2021), which has led to the hypothesis that the shrinking may be
the result of different evolutionary drivers than the regrowth. In line
with these observations, the individual decrease in skull height inS. araneus is flexible and modulated by ambient temperature
(Lázaro et al. 2019).
Our aim was to confirm that the change in climate over several decades
has had an impact on 1) the overall size of S. araneus as
measured by skull dimensions and 2) the intensity of the reversible
seasonal size change (Dehnel’s phenomenon). We combined climate data and
skull size measurements of S. araneus from a 52-year series of
specimens collected in the Białowieża primeval forest, NE Poland, from
1953 to 2004.
We first hypothesized that, because they are larger at lower, warmer
latitudes, the body size of S. araneus increased over the years
as a response to increasing temperatures or decreased as a response to a
dryer climate leading to a decreasing soil water level and thus lower
earthworm availability in the Białowieża Forest. We further hypothesized
that there should be a negative relationship between the winter skull
height decrease and winter temperatures. Conversely, the winter skull
height decrease should become greater if climate change is combined with
increasingly less favourable food availability in winter than in summer.