ArticlePDF AvailableLiterature Review

Voles and weasels in the boreal Fennoscandian small mammal community: What happens if the least weasel disappears due to climate change?

Authors:
  • Professor,University of Jyväskylä
  • Ähtäri Zoo

Abstract

Climate change, habitat loss and fragmentation are major threats for populations and challenge for individual behavior, interactions, and survival. Predator‐prey interactions are modified by climate processes. In the northern latitudes strong seasonality is changing and the main predicted feature is shortening and instability of winter. Vole populations in the boreal Fennoscandia exhibit multiannual cycles. High amplitude peak numbers of voles and dramatic population lows alternate in 3–5 years cycles shortening from North to South. One key factor, or driver, promoting the population crash and causing extreme extended lows, is suggested to be predation by the least weasel. We review the arms race between prey voles and weasels along the multiannual density fluctuation, affected by the climate change, and especially the change in duration and stability of snow cover. Snow provides for ground‐dwelling small mammals thermoregulation, shelter for nest sites, and hide from most predators. Predicted increase in instability of winter forms a major challenge for species with coat color change between brown summer camouflage and white winter coat. One of these is the least weasel, Mustela nivalis nivalis. Increased vulnerability of wrong‐colored weasels to predation affect vole populations and may have dramatic effects on vole dynamics. It may have cascading effects to other small rodent – predator interactions and even to plant – animal interactions and forest dynamics.
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© 2019 The Authors. Integrative Zoology published by International Society of Zoological Sciences, Institute
of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd
This is an open access article under the terms of the Creative Commons Attribution License, which permits
use, distribution and reproduction in any medium, provided the original work is properly cited.
Integrative Zoology 2019; 14: 327–340 doi: 10.1111/1749-4877.12388
REVIEW
Voles and weasels in the boreal Fennoscandian small mammal
community: what happens if the least weasel disappears due to
climate change?
Hannu YLÖNEN,1 Marko HAAPAKOSKI,1 Thorbjörn SIEVERT1 and Janne SUNDELL2
1Department of Biological and Environmental Science and Konnevesi Research Station, University of Jyväskylä, Jyväskylä, Finland
and 2Lammi Biological Station, University of Helsinki, Lammi, Finland
Abstract
Climate change, habitat loss and fragmentation are major threats for populations and a challenge for individual
behavior, interactions and survival. Predator–prey interactions are modied by climate processes. In the north-
ern latitudes, strong seasonality is changing and the main predicted feature is shortening and instability of win-
ter. Vole populations in the boreal Fennoscandia exhibit multiannual cycles. High amplitude peak numbers of
voles and dramatic population lows alternate in 3–5-year cycles shortening from North to South. One key fac-
tor, or driver, promoting the population crash and causing extreme extended lows, is suggested to be predation
by the least weasel. We review the arms race between prey voles and weasels through the multiannual density
uctuation, affected by climate change, and especially the changes in the duration and stability of snow cover.
For ground-dwelling small mammals, snow provides thermoregulation and shelter for nest sites, and helps them
hide from predators. Predicted increases in the instability of winter forms a major challenge for species with
coat color change between brown summer camouage and white winter coat. One of these is the least weasel,
Mustela nivalis nivalis. Increased vulnerability of wrong-colored weasels to predation affects vole populations
and may have dramatic effects on vole dynamics. It may have cascading effects on other small rodent–predator
interactions and even on plant–animal interactions and forest dynamics.
Key words: cascading effects, climate change, least weasel, population cycles, predator–prey
Correspondence: Hannu Ylönen, Department of Biological
and Environmental Science and Konnevesi Research Station,
University of Jyväskylä, PO Box 35, FI-40014 Jyväskylä,
Finland.
Email: hannu.j.ylonen@jyu.
INTRODUCTION
Anthropogenic climate change has created many
stressors that threaten wild populations failing to adapt
to novel conditions. In places where there is typical-
ly snow in winter, the effects of climate change on spe-
cies may be driven by altered snow regimes (Penczy-
kowski et al. 2017). Snow cover affects the life of
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© 2019 The Authors. Integrative Zoology published by International Society of Zoological Sciences,
Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd
H. Ylönen et al.
ground-dwelling animals and food webs in many ways.
Importantly, snow creates thermoregulative shelter and
an insulated subnivean space, further providing a phys-
ical and visual refuge from predators. The duration and
end of snow cover also drive phenology through natural
selection in many animal species (reviewed by Penczy-
kowski et al. 2017).
Approximately one-third of the world’s land area is
covered by snow during winter (Lemke et al. 2007).
The need for understanding how altered snow regimes
impact food webs is particularly urgent because climate
change is occurring most rapidly in regions of the world
that historically have had cold, snowy winters. A good
example of how altered snow regimes is driving phenol-
ogy is camouage mismatch in seasonally colored molt-
ing species confronting unpredictable snow cover. In
northern Europe, there are 6 species of birds and mam-
mals changing from summer pelage to a white winter
coat: the mountain hare (Lepus timidus Linnaeus, 1758),
the arctic fox [Vulpes lagopus (Linnaeus, 1758)], 2 arc-
tic grouse species [Lagopus lagopus (Linnaeus, 1758)
and Lagopus muta (Montin, 1781)] and 2 small muste-
lids (Mustela nivalis nivalis Linnaeus, 1766 and Mus-
tela erminea Linnaeus, 1758). The combination of coat
color change and climate change cause a dilemma; the
late and unpredictable onset of snow cover and its ear-
lier melting threatens the survival of animals with the
wrong coat color compared to the background. For ex-
ample, the weekly survival of snowshoe hares with mis-
matched fur to the background decreases up to 7% due
to predation (Zimova et al. 2016).
Small mammals, either as prey for carnivores or as
consumers of plants or insects, are a key component of
the boreal ecosystem. In Finland, small mammals con-
sist of grass-eating Microtus species and more for-
est-dwelling Myodes species (Sundell & Ylönen 2008)
and insectivorous shrews (Sorex spp.). Microtine ro-
dents are known to uctuate in 3–5-year cycles (Hanski
et al. 2001). Besides affecting food webs as consumers,
many other species are affected by changes in rodent
density. For instance, ground-nesting forest grouse pop-
ulations decline when vole numbers crash after peak
years because predators focusing on voles change to al-
ternative prey (Angelstam et al. 1984).
The least weasel is suggested to be the strongest sin-
gle factor shaping the multiannual dynamics of boreal
voles (Korpimäki et al. 1991; Hanski et al. 2001). The
predator–prey interaction between weasels and voles
is of great importance in vole life history in different
phases of the population cycle. During the population
increase after the crash, the predation pressure is not in-
tense as the numbers of specialist predators increase
with a delay of half a year (Sundell et al. 2013). During
the peaks of vole abundances, predation pressure is
high, and during the decline or crash of the populations,
extremely high, as the ratio between weasels and voles
increases strongly in favor of predators. The dramatic
impact of weasels alone on the mortality of voles during
the population crash was documented by Norrdahl and
Korpimäki (1995) in a radio-telemetry eld study where
the mortality rate of radio-collared voles caused by wea-
sels was close to 80% of all study voles.
From the vole survival point of view, the intense pre-
dation pressure by weasels means increased alert and
the need for early recognition of weasel presence in the
home area. This is possible for the voles using the body
odors and scent markings excreted by anal glands of
weasels, which, like in all mustelids, are strong (Brinck
et al. 1983). It is recognizable as a cue for increased
predation risk in the hunting terrain of weasels by prey
animals (Ylönen & Ronkainen 1994; Ylönen 2001; Ap-
felbach et al. 2005). Weasel–vole contact normally oc-
curs in shady or dark cavities, under grass and shrubs,
in holes under stones or tree-trunks, as well as under
the snow in winter. Here the visual sense is not import-
ant but the olfactory is: both for weasels to smell prey
(Ylönen et al. 2003) and for voles to recognize risk
through the presence of weasels early enough and to
respond accordingly, by fleeing or hiding (Sundell &
Ylönen 2004).
Weasel have a high energy demand and in order to
breed, female weasels require high enough rodent den-
sities close to the nest to be able to feed the litter or to
survive during the cold season (Haapakoski et al. 2013).
Due to its small size, weasels can hunt voles and shrews
under the snow in winter. However, their small body
size makes weasels themselves vulnerable to attacks by
a range of different avian and larger mammalian preda-
tors (Korpimäki & Norrdahl 1989). As the vole popula-
tions decline, the resident avian predators may also tar-
get their hunting on small predators like weasels. This
may be especially true during autumn, as food for most
animals becomes scarce. In addition, when vegetation
withers, hunting weasels may be more visible to avian
predators. Furthermore, the onset of winter and camou-
age mismatch may expose weasels to avian predation
(Atmeh et al. 2018).
Climate change is causing unpredictability of the on-
set and end of winters and has the potential to threat-
en the viability of specialist predator species, possibly
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© 2019 The Authors. Integrative Zoology published by International Society of Zoological Sciences,
Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd
Boreal voles and weasels under climate change
leading to cascading trophic effects at the ecosystem
level (Terraube et al. 2015). Specialist predators can
have a major impact on food webs. A good example of
this kind of species is the least weasel (hereafter wea-
sel), which is a specialist predator of small mammals.
The reason why this weasel is so important is that it is
thought to regulate small mammal populations such as
those of voles and shrews in Scandinavia (Hanski et al.
2001).
In this review paper we aim to illustrate the predator–
prey interaction between voles and their major preda-
tor, the least weasel, in the northern boreal environment
of Fennoscandia. We focus on both vole ability to rec-
ognize the increased risk and to behaviorally respond,
in the evolutionary arms race, to weasel risk in breeding
or survival adaptations. We then include the predicted
climate change scenario to the vole–weasel interaction.
This may alter the population dynamics of both prey
and predators, or more explicitly change the patterns in
the regular multiannual cyclicity of vole populations. If
the high impact of weasels in the multiannual pattern of
vole dynamics (Hanski et al. 2001) were to change due
to climate change, the decline or disappearance of spe-
cialist predators might dampen small mammal popula-
tion cycles (Korpela et al. 2014). Dampened prey cycles
theoretically could then drive small mammal specialist
predator populations towards extinction (Millon et al.
2014), and the dramatic changes would have substantial
cascading effects on the small rodent community and on
their predator guild in the north.
BOREAL VOLE CYCLE AND
PREDATOR–PREY INTERACTION
Factors causing regular multiannual density fluctu-
ations in organisms, so-called population cycles, have
been the subject of intensive investigation and debate
for almost 100 years (e.g. Stenseth 1999). One of the
most studied species group has been small rodents liv-
ing in the Northern Hemisphere. Especially regular and
pronounced are cycles of voles and lemmings living in
strongly seasonal environments. Many hypotheses have
been proposed to explain these cycles. Presently, most
popular hypotheses are related to biological extrinsic
factors, such as food and predation (Hanski et al. 2001;
Turchin & Batzli 2001), alone but also most recent-
ly combined with occurrence of pathogens and diseases
(Huitu et al. 2003; Forbes et al. 2015).
Predation was long seen only as a factor prolonging
the low phase of the cycle or deepening the crash. How-
ever, later, the different relative roles of various kinds of
predators were recognized (Andersson & Erlinge 1977).
In general, generalist predators’ effect on prey cycles is
thought to be stabilizing due to their habit of switching
between prey types according to their availability. Simi-
larly, avian predators, even though they might have spe-
cialized diets concentrating on small rodents, can stabi-
lize population uctuations of the prey because they can
respond fast numerically by moving without signicant
delay from low prey populations to the sites with high
prey availability over the vast landscapes. In this way,
nomadic avian predators can also cause spatial synchro-
ny of small rodent populations. In contrast, the resident
specialist predators of small rodents, which are often
small carnivorous mammals, especially the small muste-
lids the weasel and the stoat, cannot travel long distanc-
es and are highly dependent on local prey availability.
They tend to have a destabilizing effect on prey popu-
lations (Hanski et al. 1993). These animals cannot re-
spond as fast numerically as avian predators, and their
response is likely to involve a time lag.
Avian predators and generalist predators are more
common and numerous in southern areas than resident
predators, meaning that resident predators’ role is rel-
atively larger in the north. This is commonly linked to
the increasing gradient observed in cycle length and am-
plitude from south to north (Hanski et al. 1991). This
gradient is also associated with climate with longer du-
ration of snow cover and snow thickness in the north,
which gives partial protection from many non-special-
ized predators (Hansson & Henttonen 1985).
The special role of the smallest carnivore in the
world: the least weasel
Common resident vole specialists in the north are
small mustelids, the stoat and the weasel. The northern
subspecies of weasels, the least weasel, which is also the
smallest carnivore mammal in the world, is thought to
be the most important predator of voles and lemmings.
Weasels cause overwhelming mortality of populations,
especially in declining vole populations (Norrdahl &
Korpimäki 1995). This species has characteristics that
make it a real threat to voles.
The least weasel is unique among carnivores because
of its fast reproductive potential. Female weasels can
have 2 litters per breeding season, in favorable condi-
tions even 3, and occasionally they may breed in win-
ter outside of their normal breeding season. Young fe-
males can mature in the same breeding season they have
been born and produce a litter of their own. Litter siz-
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© 2019 The Authors. Integrative Zoology published by International Society of Zoological Sciences,
Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd
H. Ylönen et al.
es can be large, on average 6–10, but litters of 14 have
been observed (Sundell 2003). Even if the least weasel
has high reproductive capacity, they cannot cope with
their prey, voles, which are even more efcient in repro-
duction. Because of this, weasel numbers often follow-
ing those of their prey with a time lag, in theory a neces-
sary condition for classic predator–prey cycles to occur
(May 1973).
The least weasel is about the size of its main prey,
meaning that it has a very restricted diet containing al-
most no other prey items than small rodents (Korpimä-
ki et al. 1991). Their small size and slender body shape
mean they have a high surface to volume ratio, result-
ing in high heat loss and high energy needs. Thus, the
least weasel needs a relatively large amount of food
even for maintaining its basic metabolic level (Gilling-
ham 1984). The small-sized weasel can enter the tunnels
and cavities of voles, whether they are under ground or
snow, making it a very efcient predator in all seasons
compared to other vole predators. Weasels can also en-
ter the nests of voles and eat the pups. It cannot store
much energy as fat as it needs to be slim to follow voles
into their refuges, and, therefore, it kills more than is re-
quired for its immediate needs whenever possible, and
stores the excess food for later use (Oksanen et al. 1985;
Jędrzejewska & Jędrzejewski 1989). However, the least
weasel prefers fresh food and, therefore, its kill rate can
be much higher than its consumption rate and its effect
on vole populations is higher than can be concluded just
based on energy needs and weasel numbers. Because of
its specialized diet, the least weasel is observed to have
type II functional response, leading in theory to unstable
dynamics and even cycles in its prey population (Sundell
et al. 2000).
Its small size and the fact that the least weasel lives
in the same habitat as its prey exposes it to other larg-
er vole predators. In fact, the least weasel is often ob-
served to be preyed upon by avian predators. This hap-
pens more often when vole numbers are declining and
weasels need to move more to nd the remaining prey
(Korpimäki & Norrdahl 1989). In the snowy season this
means that weasels have to move more on top of the
otherwise protective snow cover.
VOLE PERSPECTIVE IN THE ARMS
RACE BETWEEN VOLES AND WEASELS
Recognition of fear
In the tunnels and cavities on the ground and in the
darkness under the snow, weasels hunt using olfacto-
ry sense. In an experiment using the Y-maze, Ylönen et
al. (2003) clearly showed that weasels preferred to en-
ter the maze branch providing odor cues of either bank
voles [Myodes glareolus (Schreber, 1780)] or eld vo-
les [Microtus agrestis (Linnaeus, 1761)] over a bran-
ch with clean vole cage bedding at the end of the tube.
Similarly, voles or other small rodent prey try to recei-
ve correct information on the presence and vicinity of a
predator using the smell left by moving predators. Most
mammalian predators have a typical smell, which they
use for their own social communication, which is com-
monly excreted from anal glands via urine and/or feces,
or through body rubbing (Erlinge et al. 1982). These
predator social scents, widespread throughout all mam-
malian taxa, have common sulfur and/or nitrogen com-
pounds (Apps et al. 2015), which are perceived to our
nose as strong and sticky. Prey species, like voles in our
case, can use these odor cues as a measure of risk by
mammalian predators, and decrease their activity, inclu-
ding diel activity, foraging and even reproductive acti-
vities (Ylönen & Ronkainen 1994; Ylönen et al. 2006;
Sundell et al. 2008; Haapakoski et al. 2013, 2015).
It is almost trivial to state that “Olfaction is a central
aspect of mammalian communication, providing infor-
mation about individual attributes such as identity, sex,
group membership or genetic quality” (Weiß et al. 2018,
p. 420). We know a lot about the importance of olfacto-
ry sense in mate choice from mice to men: on the role
of, for instance, major histocompatibility complex in
mate quality recognition and avoidance of inbred mat-
ings (Wedekind et al. 2000). Also in food selection, ol-
faction is of essential importance (Nevo et al. 2015).
However, in most experiments, using the odor of pred-
ators as the mean of manipulation of the risk of preda-
tion, we tend to use very rough and broad mixtures of
predator scents. This is especially true in larger-scale
eld studies where bedding of small mustelid cages is
commonly distributed in the environment of study voles
(e.g. Mappes & Ylönen 1997; Fuelling & Halle 2004;
Trebatická et al. 2012). In contrast, studies dealing with
single synthetic odor components out of the big bouquet
of natural odors have problems nding the components
carrying a biological meaning (Apfelbach et al. 2015;
Sievert & Laska 2016).
Just recently we have started to think that animals re-
ceiving important, life-saving odor information of pre-
dation risk from the environment must be as accurate
as the odors used in social communication and mate
choice. Biological odors are organic materials, which
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© 2019 The Authors. Integrative Zoology published by International Society of Zoological Sciences,
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Boreal voles and weasels under climate change
have normal metabolism and dilution paths in time.
Thus, predator scent that is left behind should be recog-
nized by prey animals and provide accurate information
about not only who was there but also when (Bytheway
et al. 2013). Small mustelids like stoats and weasels do
not have large ranges (Erlinge & Sandell 1986; Geh-
ring & Swihart 2004). If there is enough rodent prey,
they are typically resident to a certain area and visit in
certain time intervals prey patches they had been visit-
ing previously (Erlinge & Sandell 1986). During these
visits, the risk for voles is high, but in between the vis-
its low. Thus, aging of predator scent, disappearance
of odor compounds in time, and the effects of different
aged odors on prey response need to be studied more as
there are only a few relevant studies so far (Hegab et al.
2014; Sánchez-González et al. 2018).
Predator scent or the smell of an acute fear
shock by an actual predator?
A growing eld of exploration and experimental test-
ing in mammalian predator–prey interactions is olfac-
tory intra-species communication via so-called alarm
pheromones. Alarm pheromones or “Schreckstoff” (von
Frisch 1938) are used for communication across phy-
la (Bowers et al. 1972; Boissy et al. 1998; Beale et al.
2006). It is generally assumed that alarm pheromones
serve as a warning signal within a colony/group or fam-
ily for social species of insects, sh and mammals (Breed
et al. 2004; Kiyokawa et al. 2004; Gomes et al. 2013).
Several publications have succeeded in describing the
chemical properties of alarm pheromones for differ-
ent groups of invertebrate species (Bowers et al. 1972;
Howe & Sheikh 1975; Kuwahara et al. 1989). Howev-
er, there is so far little work on mammalian alarm pher-
omones. Brechbühl et al. (2013) discovered in strains of
laboratory rats (Wistar) and mice (C57BL/6J and OMP-
GFP) that their alarm pheromones are structurally simi-
lar to predator odors.
Contrary to predator-based odor cues, vertebrate prey
species do not habituate to alarm pheromones (Hutchi-
son & Marvin 1995; Hartman & Abrahams 2000). This
could be caused by different information transferred in
those components. While predator odors could inform
about a general predator presence in the area, alarm
pheromones are only released after a successful escape,
signaling an immediate risk in the area.
There is ongoing debate about whether the chemicals
currently referred to as alarm pheromones are true pher-
omones in a strict sense (Magurran et al. 1996; Viney &
Franks 2004), but there is no argument about the elicited
behavioral response. As the methods for chemical anal-
ysis have massively improved in the past decade, it will
only be a matter of time before the true nature of these
“odors of stress” is revealed.
Do voles respond to olfactory weasel risk cues
and to live weasels similarly?
There are ample studies, as well as experiments and
information, demonstrating that small rodents use the
predator scent as a measure of risk of predation. How
accurately we do not know yet, but, in general, the re-
sponses are plausible and enhance prey vole probabili-
ties of surviving over a risky period. Reviews by Lima
and Dill (1990), Ylönen (2001) and Apfelbach et al.
(2005, 2015) depict how prey animals perceive risk of
predation and respond to experimentally increased risk.
The normal responses are either freezing or fleeing,
staying still or seeking shelter where predators would
not be able to enter. There seems to be a dichotomy in
either doing nothing or doing something very rapidly.
Both seem to be better anti-predatory adaptations than
moving a bit or slowly, where the prey individual only
attracts predator attention and possibly provokes an at-
tack.
In our own experiments we were able to verify the
dichotomy in bank vole movements and choice of se-
lecting a hole for escape. Some voles stayed at the site
where they recognized the presence of a weasel and
froze. If running to a hole, the voles did not take the risk
of getting stuck in too small a hole but selected the next
larger one, which was easier to enter (Sundell & Ylönen
2004). By this means the escaping voles may have es-
caped from larger male weasels at least, if not the small-
er female voles. In a study where the living environment
of voles and also weasels was experimentally fragment-
ed consisting of the same amount of protective tall grass
habitat, but either in one large or 4 small patches, the
vole trappability decreased, especially in the continu-
ous habitat where the weasel was living inside the same
large patch as the voles were. The presence or visit of a
weasel forced the voles out of the protective habitat to a
risky matrix area without protective vegetation (Haapa-
koski et al. 2012, 2013).
Two most common vole species in Fennoscandia and
much of Europe, the eld vole and the bank vole, inhab-
it different habitats; eld voles as herbivores are grass-
land specialists and granivorous bank voles inhabit the
forests (Sundell & Ylönen 2008). Bank voles have a 3-D
habitat and they use trees for foraging buds and lichens.
Do bank voles use trees to escape when chased by a
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H. Ylönen et al.
predator, and, if yes, how effective is climbing as an es-
cape strategy? We tested the escape reactions of grass-
land specialists, field voles, and forest species, bank
voles, when escaping weasels (Mäkeläinen et al. 2014).
Both species did not mind using the offered possibil-
ity to climb to a tree when there was no weasel pres-
ent. When chased by a weasel, 14 out of 51 tested bank
voles climbed the tree and only 2 out of 30 eld voles
climbed. Weasels followed the horizontal tube of es-
cape; that is, most eld voles would have been falling
prey to weasels as 25% of the bank voles escaped suc-
cessfully. Forest-dwelling, climbing bank voles survive
population decline better than ground-dwelling, clumsi-
er and non-climbing eld voles, which are suggested to
be preferred prey by weasels in the multi-species prey
vole guild.
The activity of voles is dependent on predator activ-
ity. If predators, like owls, are nocturnal only, the prey
animals adjust their activity to dusk and dawn to avoid
the peak activity of owls (Jacob & Brown 2000). In the
nocturnal predator–prey interaction, a full moon de-
creases prey activity as it exposes them more to avi-
an predation, which is documented in desert rodents,
with no grass cover allowing shelter during moonlight
(Brown et al. 2001; Kotler et al. 2010). Boreal bank
voles have polyphasic activity patterns throughout the
day and night (Ylönen 1988, however see Bleicher et al.
2019). In a eld study where we monitored boreal voles
and weasels with radio-tracking in large enclosures, the
voles carefully followed the resting times of weasels in
their activity and decreased their activity as the weasels
in the enclosure started to move again (Sundell et al.
2008). Seeking food and handling it after having found
a protable foraging patch are essential for animal ener-
gy gain, wellbeing and survival. In a simple and, for fu-
ture research, inuential optimality model, Brown (1988)
suggested animal foraging efciency and, thus, energy
gain to be determined by foraging costs, predation costs
and costs from other activities missed during foraging.
He developed a method called giving-up-density (GUD),
which provides the harvest rate of a food patch under
different risk (cost) of predation. He proposed that the
animals quit foraging as the protability of a patch de-
creases and time to nd food in the patch rises, increas-
ing the time exposed to predation (predation costs).
GUD measurements have become a standard in ani-
mal foraging ecology and decision-making under risk of
predation (Bedoya-Perez et al. 2013). Decreased forag-
ing under increased predation risk has been document-
ed in dozens of studies with different taxa from small
mammals to ibex, ungulates and porcupines (Brown &
Alkon 1990; Kotler et al. 1994; Altendorf et al. 2001;
Ylönen & Brown 2007). Optimality in foraging reects
fitness-related behaviors and survival strategies, and,
thus, provides a far broader picture of animals’ optimal
behavior than only gaining food and energy to survive
(Stephens et al. 2007).
Producing offspring under high risk of predation, es-
pecially targeted against the pups, is a strongly debated
issue. The least weasel as a predator provides an excel-
lent example in studying the effects of increased weasel
risk on breeding of prey voles. The weasel is so small
that it can enter almost any hole or nest of voles or oth-
er ground-dwelling or subterranean small mammals.
Thus, it is an effective nest predator as well. As the vole
populations decline, the numbers of adult and sub-adult
prey voles decrease and weasels may be forced to seek
the nests of last breeding females to find food. They
might even be forced to enter the nests of ground-nest-
ing or even hole-nesting passerine birds to exploit eggs
of edglings as food (Järvinen 1985).
What should a female vole in reproductive condi-
tion do under risk, where the probability of pups being
killed by a predator, the weasel, is high? Furthermore,
if the cues of the nest with pups lead weasels to the nest
site, or if reproductive and lactating weasels attract ol-
factory hunting weasels, the female may lose her own
life as well (Korpimäki et al. 1994; Ylönen & Ronka-
inen 1994). In a series of laboratory and semi-natural
field experiments, we demonstrated breeding suppres-
sive effects of weasel presence or weasel odors on re-
production of the bank vole and the eld vole (Ylönen
& Ronkainen 1994; Koskela & Ylönen 1995; Mappes
& Ylönen 1997). However, more extensive field stud-
ies often did not verify any effects in breeding of voles
during the best summer conditions, despite increased
or simulated risk of weasel predation (Trebaticka et al.
2012, but see Fuelling & Halle 2004). In an overwinter-
ing study under weasel odor-simulated risk of predation,
however, a signicant effect and a delay of rst repro-
duction of 1 month under weasel risk compared to start
of breeding in populations with supplemental food and
no weasel predation was again observed (Haapakoski
et al. 2012). The results raise 2 essential questions: how
the odor-based weasel cue persists in the breeding envi-
ronment and if the recognition of risk needs to be hap-
pening at the onset the of breeding season. For the rst
question we have the answer that an odor remains a re-
liable cue under the snow, with no wind or rain that may
dilute or fade the odor signal in summer. For the second
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Boreal voles and weasels under climate change
question, we consider that if breeding has already start-
ed, stopping the breeding cycle seems to be difcult if
not impossible. Running around in breeding condition
but not breeding would possibly not bring any survival
benet anymore.
The partly contradictory studies may provide a syn-
thesis in the form of variability of breeding strategies in
animals: whether to invest in own survival and decrease
breeding activity, suppressing or delaying reproduc-
tion (Ylönen 1994; Ylönen & Ronkainen 1994), along
with other activities like moving and foraging. Alterna-
tively, the second option is to invest in intensive repro-
duction, even with the risk of being the last one, with
the hope that at least one pup will survive over the peri-
od of high risk (Dufeld et al. 2017; Haapakoski et al.
2018; Sievert et al. 2019). The latter theoretical strategy,
bet-hedging or terminal investment, has been document-
ed in numerous taxa depending on either intrinsic fac-
tors like individuals’ age or extrinsic threat factors for
survival, like predation or parasitism (see tables 1 and 2
in the review by Dufeld et al. 2017).
WEASEL PERSPECTIVE: WEASEL AS
SPECIALIST PREDATOR AND PREY
Weasel behavior and survival adaptations along
the vole cycle
Weasels have large reproductive potential if the food
situation is good. This is true during the increase and
peak years of vole cycles. Rapid reproduction with large
litters is sustained by increasing population densities of
voles. Weasels are regarded to be the strongest single
factor in causing the vole numbers to turn from growth
to decline. As the vole numbers are decreasing, the nu-
merous weasels alone are sufficient to complete the
crash leading to very low numbers of voles. Especially
during autumns of high-density years preceding the de-
cline, weasels are known to kill more prey than required
for their daily energy needs. This phenomenon, called
surplus killing, is, according to current knowledge, an
adaptive behavior: hoarding food for future in the cold
seasons (Jędrzejewska & Jędrzejewski 1989) when the
caches do not rot rapidly. The same occurs in the small-
est owl species, the pygmy owl (Claucidium passerinum
Linnaeus, 1758), which hoards birds and small rodents
in holes or nest boxes just before the onset of winter
(Solheim 1984; Mappes et al. 1993).
During the milder season, the least weasel needs on
average a bit more than one 25-g vole per day. The en-
ergy needs of female and male voles are equal despite
their body size differences; during pregnancy, the fe-
male needs 3 times the amount of food that a non-breed-
ing female needs (Macdonald 1995). During autumn
and towards the winter, the energy needs and hunting
efforts of weasels double (Haapakoski et al. 2013). The
mortality effect of weasels from the population peak to
decline and population low is dramatic. It is illustrated
by the fact that during the peak phase of both prey voles
and weasels, the number of weasels is estimated to be
a maximum of 5–10 individuals per km2. At the same
time, the number of eld or sibling voles can reach up
to 10 000 voles per km2 (Macdonald 1995).
After the vole population crashes, weasels are in trou-
ble. As small vole specialists, they are not able to nd
alternative prey in the same manner as larger carnivores.
If the vole populations start to decline during autumn
and remain low until spring, the weasels need to put
more effort and energy into hunting the decreasing and
rare voles left. This also means more hunting trips, and
more movement out of the sheltering ground vegetation
or on the snow. Here come the top predators, raptors,
owls and larger mammalian predators, as actors into the
evolutionary play where the weasel partly changes from
predator to prey.
Fatal coat color dilemma along climate change
Predicted climate change scenarios suggest fun-
damental changes, especially in the winters of north-
ern boreal areas. The environment is changing, but day
length remains the same. The weasel changes its white
winter coat in autumn based on a physiological mecha-
nism of melatonin synthesis. The most important factor
driving molting in mammals is a hormonal cascade in-
duced by photoperiod (Zimova et al. 2018), which stays
the same regardless of onset of snow cover. Plasticity of
winter fur molt in weasels is very limited (Atmeh et al.
2018). For thousands of years, shortening of day length
and onset of winter have been in strict correlation but
not necessarily anymore. This makes weasels vulnera-
ble to climate change-caused mismatch in color molting
so that they are no longer camouaging with the back-
ground color due unpredictable snow cover. Recently it
has been found that climate change is affecting weasel
mortality in Poland due to camouage mismatch (Atmeh
et al. 2018). In the Polish study area, both weasel sub-
species were present, the northern least weasel, which
changes coat color in winter, and the southerly common
weasel (Mustela nivalis vulgaris), which remains brown
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H. Ylönen et al.
during the winter. The relative proportion of white-coat-
ed least weasels is decreasing in the 2-weasel communi-
ty (Atmeh et al. 2018). This means that climate change
will strongly inuence the mortality of the weasel due to
prolonged camouage mismatch at both ends of winter.
How will climate change impact weasels? Both on-
set and end of winters are predicted to be more often
snow-free and the number of snow-coved days is de-
creasing (Atmeh et al. 2018). The key question is the
extent of exibility or polymorphism in the response of
weasels to day length trigger, Zeitgeber, for starting the
melatonin synthesis leading to coat change (Mills et al.
2018). Through polymorphism, natural selection can
operate in favor of individuals which change their win-
ter coat later, or which use cues other than day length
as a trigger for the change. Mills et al. (2018) found in
a global survey of 8 coat changing species polymor-
phic zones which could represent the material for evo-
lutionary rescue for these species under climate change.
However, the Fennoscandian least weasel, the key spe-
cies impacting cyclic dynamics of several vole species,
seems to have a very limited plasticity in the timing of
coat color change (Atmeh et al. 2018).
Thus, least weasel survival, population numbers and
dynamics on population dynamics of voles is an import-
ant issue. Through Central Sweden and the Baltic states
there is an overlapping zone of 2 weasel subspecies, the
more northern and eastern least weasel and the Cen-
tral European common weasel. The former changes coat
color and the latter does not. Thus, one scenario is the
spread of the common weasel more to the north if en-
vironmental change favors brown remaining predators
and least weasel plasticity or degree of polymorphism is
limited (Atmeh et al. 2018). Spread of new species to-
wards the north along the milder climate conditions is
occurring. However, the main groups of immigrants,
birds and insects have wings and can rapidly respond to
environmental change. Mammals are slower and hin-
dered by physical barriers like the Baltic Sea in invad-
ing Fennoscandia.
CONCLUSIONS: WEASEL FAITH,
VOLE COMMUNITIES AND FOREST
LANDSCAPES
There exists a general picture that something weird is
going on in vole cycles around Europe (e.g. Hörnfeldt
et al. 2005; Millon et al. 2014) and that these changes
reflect habitat changes, predator fluctuations and food
webs in general (Penszykowski et al. 2017). The gen-
eral assumption is the impact of climate change, for in-
stance change in the North Atlantic Oscillation and its
effects on winter properties, is a strong factor behind the
general dampening of cycles. Korpela et al. (2014), ex-
amined the role of specialist and generalist predators,
especially that of weasels in summer and winter dynam-
ics of northern boreal voles in Finland. Their assump-
tion was that there would be a strong climate driven ef-
fect on vole populations, especially during the winter.
However, the extensive analyses showed a reverse pic-
ture: that weasel impact was strong during summer, and
that winter conditions were not driving population col-
lapses during the following summer.
The Europe-wide dampening of population cycles
in mainly grassland species, Microtus voles and Micro-
tus-like Myodes voles, the grey-sided vole (Myodes ru-
focanus Sundevall, 1846) (Hörnfeldt et al. 2005; Cor-
nulier et al. 2013). Evidence on the interaction between
climate predation and forest dwelling species like the
bank vole is scarce. There are 2 Fennoscandian exam-
ples of drastic changes in vole dynamics, the temporal
disappearance and return of vole cycles in Finnish Lap-
land (Henttonen et al. 1987; Cornulier et al. 2013) and
the low densities of grey-sided voles in Sweden (Hörn-
feldt et al. 2005) (Fig. 1.). Both seem to have as a com-
mon factor: the changes in land use and forestry, and,
therefore, in landscape structures. However, the process-
es leading to vole cycle dampening and the magnitude
seem to be different.
In Lapland, the change in the forest age structure
was followed by disappearance of synchrony between
the species in population peaks and crashes and espe-
cially the drastic decline of eld voles. Along with the
eld vole decline, numbers of weasels declined and the
stoat (Mustela erminea) became the major “regulator”
of vole dynamics, however concentrating on eld voles
and field vole-type tundra voles and grey-sided voles.
This allowed the competitor bank vole populations to
grow and bank vole numbers remained high and stable
over long periods (Henttonen 2000). As the field vole
returned to the system, weasels and cycles returned as
well.
Dampening of the Swedish grey-sided vole cycle is
more clearly attributed to climate change (Hörnfeldt
et al. 2004) and change in forest structures, like chang-
es in the stony structures of forest oor and forest frag-
mentation (Ecke et al. 2006; Magnusson et al. 2013),
without a direct link to small mustelid predation or Mi-
crotus–Mustela interaction.
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Boreal voles and weasels under climate change
Figure 1 Schematic presentation of 2 types of dampening of the Fennoscandian cyclic vole uctuations. The grey-sided vole de-
clines and stable low numbers are suggested to be due to habitat changes, especially in old pine forests (Hörnfeldt et al. 2005). The
disappearance of synchronous cycles in Lapland (Henttonen 2000) is more clearly predator-driven. The disappearance of eld voles
(red line) had a cascading effect in releasing growth of competing bank vole populations, that stabilized at a high level not seen be-
fore (black line). The lower panels describe examples of winter change at Konnevesi, Central Finland: on the left the “old stable and
snow-rich” winter and on the right the “current unstable wet winter,” with late onset and early melting of snow cover. If this type of
winter affects weasel survival as suggested, this could lead to similar dynamics disturbance in vole populations as observed in Lap-
land after weasel disappearance (indicated with the arrow).
Here we would like to add the direct link of winter
change and its possible effects on small mustelid num-
bers to the abovementioned factors affecting the popula-
tion dynamics of voles. Both weasels and stoats change
their camouage, providing protection from other pred-
ators during the snowy season. The white coat chang-
es more or less at the same time in autumn, regardless
of the timing of the onset of the snowy season. In ad-
dition, the brown coat appears back in spring, regard-
less of when the snow melts. If the degree of polymor-
phic exibility in the coat change is small, both weasels
and stoats are exposed to predation at both ends of win-
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ter. These are times that all animals, resident avian and
mammalian predators included, in a strongly seasonal
environment need more energy, for winter survival and
for reproduction and feeding the spring-born young.
If small mustelids, and particularly the least weasel,
decline or even disappear, this can cause drastic chang-
es in vole dynamics, as indicated by the Lapland case
(Henttonen 2000) but in a far larger geographical scale.
If the type of dynamics change is driven by release of
predation pressure by vole specialists, the populations
may be stabilized to a permanently higher level than
with a strong small mustelid predation. As alone the age
structure change and fragmentation in forest structures
cause disturbance in vole population dynamics, the ef-
fect of increasing seedling pest numbers may change
forestry in a way not seen before. The disappearance of
the world’s smallest carnivore, the least weasel, from
the northern boreal small mammal community could
have dramatic effects on the mammal community and
the landscape.
REFERENCES
Altendorf KB, Laundré JW, López González CA et al.
(2001). Assessing effects of predation risk on forag-
ing behavior of mule deer. Journal of Mammalogy
82, 430–9.
Andersson M, Erlinge S (1977). Inuence of predation
on rodent populations. Oikos 29, 591–7.
Angelstam P, Lindström E, Widén P (1984). Role of pre-
dation in short-term population uctuations of some
birds and mammals in Fennoscandia. Oecologia 62,
199–208.
Apfelbach R, Blanchard CD, Blanchard RJ et al. (2005).
The effects of predator odors in mammalian prey spe-
cies: A review of eld and laboratory studies. Neuro-
science & Biobehavioral Reviews 29, 1123–44.
Apfelbach R, Parsons MH, Soini HA et al. (2015). Are
single odorous components of a predator sufcient to
elicit defensive behaviors in prey species? Frontiers
in Neuroscience 9, 263.
Apps PJ, Weldon PJ, Kramer M (2015). Chemical sig-
nals in terrestrial vertebrates: Search for design fea-
tures. Natural Product Reports 32, 1131–53.
Atmeh K, Andruszkiewicz A, Zub K (2018). Climate
change is affecting mortality of weasels due to cam-
ouflage mismatch. Scientific Reports 8, 7648. doi:
10.1038/s41598-018-26057-5.
Beale MH, Birkett MA, Bruce TJA et al. (2006). Aphid
alarm pheromone produced by transgenic plants af-
fects aphid and parasitoid behavior. Proceedings of
the National Academy of Sciences. National Acade-
my of Sciences 103, 10509–13.
Bedoya-Perez MA, Carthey AJR, Mella VSA et al.
(2013). A practical guide to avoid giving up on giv-
ing-up densities. Behavioral Ecology and Sociobiolo-
gy 67, 1541–53.
Bleicher SS, Marko H, Morin DJ et al. (2019). Balanc-
ing food, activity and the dangers of sunlit nights.
Behavioral Ecology and Sociobiology 73, 95. https://
doi.org/10.1007/s00265-019-2703-y
Boissy A, Terlouw C, Le Neindre P (1998). Presence of
cues from stressed conspecics increases reactivity to
aversive events in cattle: Evidence for the existence
of alarm substances in urine. Physiology and Behav-
ior 63, 489–95.
Bowers W, Nault L, Webb R (1972). Aphid alarm pher-
omone: Isolation, identification, synthesis. Science
177, 1–2.
Brechbühl J, Moine F, Klaey M et al (2013). Mouse
alarm pheromone shares structural similarity with
predator scents. Proceedings of the National Acade-
my of Sciences 110, 4762–7.
Breed MD, Guzmán-Novoa E, Hunt GJ (2004). Defen-
sive behavior of honey bees: Organization, genetics,
and comparisons with other bees. Annual Review of
Entomology. Annual Reviews 49, 271–98.
Brinck C, Erlinge S, Sandell M (1983). Anal sac secre-
tion in mustelids a comparison. Journal of Chemical
Ecology 9, 727–45.
Brown JS (1988). Patch use as an indicator of habitat
preference, predation risk, and competition. Behav-
ioral Ecology and Sociobiology 22, 37–47.
Brown JS, Alkon PU (1990). Testing values of crest-
ed porcupine habitats by experimental food patches.
Oecologia 83, 512–8.
Brown JS, Kotler BP, Bouskila A (2001). Ecology of
fear: Foraging games between predators and prey
with pulsed resources. Annales Zoologici Fennici 38,
71–87.
Bytheway JP, Carthey AJR, Banks PB (2013). Risk vs.
reward: How predators and prey respond to aging ol-
factory cues. Behavioral Ecology and Sociobiology
67, 715–25.
Cornulier T, Yoccoz NG, Bretagnolle V et al. (2013).
Europe-wide dampening of population cycles in key-
stone herbivores. Science 340, 63–6.
337
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
© 2019 The Authors. Integrative Zoology published by International Society of Zoological Sciences,
Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd
Boreal voles and weasels under climate change
Dufeld KR, Bowers EK, Sakaluk SK et al. (2017). A
dynamic threshold model for terminal investment.
Behavioral Ecology and Sociobiology 71, 185.
Ecke F, Christensen P, Sandström P et al. (2006). Iden-
tification of landscape elements related to local de-
clines of a boreal grey-sided vole population. Land-
scape Ecology 21, 485–97.
Erlinge S, Sandell M (1986). Seasonal changes in the
social organization of male stoats, Mustela erminea:
An Effect of shifts between two decisive resources.
Oikos 47, 57–62.
Erlinge S, Sandell M, Brinck C (1982). Scent-marking
and its territorial significance in stoats, Mustela er-
minea. Animal Behaviour 30, 811–8.
Forbes KM, Henttonen H, Hirvelä-Koski V et al (2015).
Food provisioning alters infection dynamics in popu-
lations of a wild rodent. Proceedings of the Royal So-
ciety B 282, 20151939.
Fuelling O, Halle S (2004). Breeding suppression in
free-ranging grey-sided voles under the inuence of
predator odour. Oecologia 138, 151–9.
Gehring TM, Swihart RK (2004). Home range and
movements of long-tailed weasels in a landscape
fragmented by agriculture. Journal of Mammalogy
85, 79–86.
Gillingham BJ (1984). Meal size and feeding rate in the
least weasel (Mustela nivalis). Journal of Mammalo-
gy 65, 517–9.
Gomes LAP, Salgado PMP, Barata EN et al. (2013).
Alarm scent-marking during predatory attempts in
the Cabrera vole (Microtus cabrerae Thomas, 1906).
Ecological Research 28, 335–43.
Haapakoski M, Sundell J, Ylönen H (2012). Predation
risk and food: Opposite effects on overwintering sur-
vival and onset of breeding in a boreal rodent: Preda-
tion risk, food and overwintering. Journal of Animal
Ecology 81, 1183–92.
Haapakoski M, Sundell J, Ylönen H (2013). Mamma-
lian predator–prey interaction in a fragmented land-
scape: Weasels and voles. Oecologia 173, 1227–35.
Haapakoski M, Sundell J, Ylönen H (2015). Conserva-
tion implications of change in antipredator behavior
in fragmented habitat: Boreal rodent, the bank vole,
as an experimental model. Biological Conservation
184, 11–7.
Haapakoski M, Hardenbol AA, Matson KD (2018). Ex-
posure to chemical cues from predator-exposed con-
specics increases reproduction in a wild rodent. Sci-
entic Reports 8, 17214.
Hanski I, Hansson L, Henttonen H (1991). Specialist
predators, generalist predators, and the microtine ro-
dent cycle. The Journal of Animal Ecology 60, 353–
67.
Hanski I, Henttonen H, Korpimäki E, Oksanen L,
Turchin P (2001). Small-rodent dynamics and preda-
tion. Ecology 82, 1505–20.
Hanski I, Turchin P, Korpimäki E et al. (1993). Popu-
lation oscillations of boreal rodents: Regulation by
mustelid predators leads to chaos. Nature 364, 232–
5.
Hansson L, Henttonen H (1985). Gradients in density
variations of small rodents: The importance of lati-
tude and snow cover. Oecologia 67, 394–402.
Hartman EJ, Abrahams MV (2000). Sensory compen-
sation and the detection of predators: The interaction
between chemical and visual information. Proceed-
ings of the Royal Society B: Biological Sciences 267,
571–5.
Hegab IM, Jin Y, Ye M et al (2014). Defensive respons-
es of Brandt’s voles (Lasiopodomys brandtii) to
stored cat feces. Physiology & Behavior 123, 193–9.
Henttonen H (2000). Long-term dynamics of the bank
vole Clethrionomys glareolus at Pallasjärvi, Northern
Finnish taiga. Polish Journal of Ecology 48, 87–96.
Henttonen H, Oksanen T, Jortikka A et al. (1987).
How much do weasels shape microtine cycles in the
Northern Fennoscandian taiga? Oikos 50, 353–65.
Hörnfeldt B, Hipkiss T, Eklund U (2005). Fading out of
vole and predator cycles? Proceedings of the Royal
Society B 272, 2045–9.
Howe N, Sheikh Y (1975). Anthopleurine: A sea anemo-
ne alarm pheromone. Science 189, 386–8.
Huitu O, Koivula M, Korpimäki E et al. (2003). Winter
food supply limits growth of northern vole popula-
tions in the absence of predation. Ecology 84, 2108–
18.
Hutchison VH, Marvin GA (1995). Avoidance response
by adult newts (Cynops Pyrrhogaster and Notoph-
thalmus Viridescens) to chemical alarm cues. Be-
haviour 132, 95–105.
Jacob J, Brown JS (2000). Microhabitat use, giving-up
densities and temporal activity as short- and long-
term anti-predator behaviors in common voles. Oikos
91, 131–8.
Järvinen A (1985). Predation causing extended low den-
sities in microtine cycles: Implications from preda-
tion on hole-nesting passerines. Oikos 45, 157–8.
338
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
© 2019 The Authors. Integrative Zoology published by International Society of Zoological Sciences,
Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd
H. Ylönen et al.
Jędrzejewska B, Jędrzejewski W (1989). Seasonal sur-
plus killing as hunting strategy of the weasel Mustela
nivalis – Test of a hypothesis. Acta Theriologica 34,
347–59.
Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y (2004).
Alarm pheromones with different functions are re-
leased from different regions of the body surface of
male rats. Chemical Senses 29, 35–40.
Korpela K, Helle P, Henttonen H et al. (2014). Preda-
tor–vole interactions in northern Europe: The role of
small mustelids revised. Proceedings of the Royal So-
ciety B 281, 20142119.
Korpimäki E, Norrdahl K (1989). Avian predation on
mustelids in Europe 1: Occurrence and effects on
body size variation and life traits. Oikos 55, 205–15.
Korpimäki E, Norrdahl K, Rinta-Jaskari T (1991). Re-
sponses of stoats and least weasels to uctuating food
abundances: Is the low phase of the vole cycle due to
mustelid predation? Oecologia 88, 552–61.
Korpimäki E, Norrdahl K, Valkama J (1994). Reproduc-
tive investment under uctuating predation risk: Mi-
crotine rodents and small mustelids. Evolutionary
Ecology 8, 357–68.
Koskela E, Ylönen H (1995). Suppressed breeding in
the field vole (Microtus agrestis): An adaptation to
cyclically uctuating predation risk. Behavioral Ecol-
ogy 6, 311–5.
Kotler BP, Gross JE, Mitchell WA (1994). Applying
patch use to assess aspects of foraging behavior in
Nubian ibex. The Journal of Wildlife Management
58, 299–307.
Kotler BP, Brown J, Mukherjee S, Berger-Tal O, Bous-
kila A (2010). Moonlight avoidance in gerbils reveals
a sophisticated interplay among time allocation, vig-
ilance and state-dependent foraging. Proceedings of
the Royal Society B 277, 1469–74.
Kuwahara Y, Leal WS, Nakano Y et al. (1989). Pher-
mone study on astigmait mites: XXIII. Identication
of the alarm pheromone on the acarid mite, Tyroph-
agus neiswanderi and species specificities of alarm
pheromones among four species of the same genus.
Applied Entomology and Zoology 24, 424–9.
Lemke P, Ren J, Alley RB et al. (2007). Observations:
Changes in snow, ice and frozen ground. In: Solomon
S. et al., eds. Climate Change 2007: The Physical
Science Basis. Contribution of Working Group I to
the Fourth Assessment Report of the Intergovernmen-
tal Panel on Climate Change. Cambridge University
Press, Cambridge, UK, pp. 337–83.
Lima SL, Dill LM (1990). Behavioral decisions made
under the risk of predation: A review and prospectus.
Canadian Journal of Zoology 68, 619–40.
Macdonald D (1995). European Mammals. Evolution
and Behaviour. HarperCollins Publishers, London.
Magnusson M, Bergsten A, Ecke F et al. (2013). Pre-
dicting grey-sided vole occurrence in northern Swe-
den at multiple spatial scales. Ecology and Evolution
3, 4365–76.
Magurran AE, Irving PW, Henderson PA (1996). Is there
a fish alarm pheromone? A wild study and critique.
Proceedings of the Royal Society of London B 263,
1551–6.
Mäkeläinen S, Trebatická L, Sundell J et al. (2014). Dif-
ferent escape tactics of two vole species affect the
success of the hunting predator, the least weasel. Be-
havioral Ecology and Sociobiology 68, 31–40.
Mappes T, Ylönen H (1997). Reproductive effort of fe-
male bank voles in a risky environment. Evolutionary
Ecology 11, 591–8.
Mappes T, Halonen M, Suhonen J et al. (1993). Selec-
tive avian predation on a population of the eld vole,
Microtus agrestis: Greater vulnerability of males and
subordinates. Ethology Ecology & Evolution 5, 519–
27.
May RM (1973). Complexity and Stability in Model
Ecosystems. Princeton University Press, Princeton,
New Jersey, USA.
Millon A, Petty SJ, Little B et al. (2014). Dampening
prey cycle overrides the impact of climate change on
predator population dynamics: A long-term demo-
graphic study on tawny owls. Global Change Biology
20, 1770–81.
Mills LS, Bragina EV, Kumar AV et al. (2018). Win-
ter color polymorphisms identify global hot spots for
evolutionary rescue from climate change. Science
359, 1033–6.
Nevo O, Orts Garri R, Hernandez Salazar LT et al.
(2015). Chemical recognition of fruit ripeness in spi-
der monkeys (Ateles geoffroyi). Scientic Reports 5,
14895.
Norrdahl K, Korpimäki E (1995). Mortality factors in a
cyclic vole population. Proceedings of the Royal So-
ciety B: Biological Sciences 261, 49–53.
Oksanen T, Oksanen L, Fretwell SD (1985). Surplus
killing in the hunting strategy of small predators. The
American Naturalist 126, 328–46.
339
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
© 2019 The Authors. Integrative Zoology published by International Society of Zoological Sciences,
Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd
Boreal voles and weasels under climate change
Penczykowski RM, Conolly BM, Barteon BT (2017).
Winter is changing: Trophic interactions under al-
tered snow regimes. Food Webs 13, 80–91.
Sánchez-González B, Planillo A, Navarro-Castilla Á
et al. (2018). The concentration of fear: Mice’s be-
havioural and physiological stress responses to dif-
ferent degrees of predation risk. The Science of Na-
ture 105, 16.
Sievert T, Laska M (2016). Behavioral responses of
CD-1 Mice to six predator odor components. Chemi-
cal Senses 41, 399–406.
Sievert T, Haapakoski M, Palme R, Voipio H (2019).
Secondhand horror: effects of direct and indirect
predator cues on behavior and reproduction of the
bank vole. Ecosphere 10, e02765.
Solheim R (1984). Caching behaviour, prey choice and
surplus killing by pymy owls Glaucidiumpasserinum
during winter, a functional response of a generalist
predator. Annales Zoologici Fennici 21, 301–8.
Stenseth NC (1999). Population cycles in voles and lem-
mings: Density dependence and phase dependence in
a stochastic world. Oikos 87, 427–61.
Stephens DW, Brown JS, Ydenberg RC, eds (2007).
Foraging: Behavior and Ecology. University of Chi-
cago Press, Chicago, IL.
Sundell J (2003). Reproduction of the least weasel in
captivity: Basic observations and the influence of
food availability. Acta Theriologica 48, 59–72.
Sundell J, Ylönen H (2004). Behaviour and choice of
refuge by voles under predation risk. Behavioral
Ecology and Sociobiology 56, 263–69.
Sundell J, Ylönen H (2008). Specialist predator in a
multi-species prey community: Boreal voles and
weasels. Integrative Zoology 3, 51–63.
Sundell J, Norrdahl K, Korpimaki E et al. (2000). Func-
tional response of the least weasel, Mustela nivalis
nivalis. Oikos 90, 501–8.
Sundell J, Trebatická L, Oksanen T et al. (2008). Preda-
tion on two vole species by a shared predator: anti-
predatory response and prey preference. Population
Ecology 50, 257–66.
Sundell J, O’Hara RB, Helle P et al. (2013). Numerical
response of small mustelids to vole abundance: de-
layed or not? Oikos 122, 1112–20.
Terraube J, Villers A, Ruffino L et al. (2015). Cop-
ing with fast climate change in northern ecosystems:
mechanisms underlying the population-level response
of a specialist avian predator. Ecography 38, 690–9.
Trebatická L, Suortti P, Sundell J et al. (2012). Preda-
tion risk and reproduction in the bank vole. Wildlife
Research 39, 463–8.
Turchin P, Batzli GO (2001). Availability of food and
the population dynamics of arvicoline rodents. Ecol-
ogy 82, 1521–34.
Viney ME, Franks NR (2004). Is dauer pheromone of
Caenorhabditis elegans really a pheromone? Natur-
wissenschaften 91, 123–4.
von Frisch K (1938). Zur Psychologie des Fisch-
Schwarmes. Naturwissenschaften 26, 601–6.
Wedekind C, Bettens F, Chapuisat M et al. (2000). Ex-
amples of MHC-correlated sexual selection in mice
and humans. In: Espmark Y, Amundsen T, Rosenqvist
G, eds. Animal Signals: Signalling and Signal Design
in Animal Communication. Tapir Academic Press,
Trondheim, Norway, pp. 437–44.
Weiß BM, Marcillo A, Manser M et al. (2018). A
non-invasive method for sampling the body odour of
mammals. Methods in Ecology and Evolution 9, 420–
9.
Ylönen H (1988). Diel activity and demography in an
enclosed population of the vole Clethrionomys glare-
olus (Schreb.). Annales Zoologici Fennici 25, 221–8.
Ylönen H (1994). Vole cycles and antipredatory be-
haviour. Trends in Ecology & Evolution 9, 426–30.
Ylönen H (2001). Predator odours and behavioural re-
sponses of small rodents: An evolutionary perspec-
tive. In: Pelz HJ, Cowan PD, Feare CJ, eds. Advances
in Vertebrate Pest Management II. Filander, Fuerth,
pp. 123–38.
Ylönen H, Brown JS (2007). Fear and the foraging,
breeding, and sociality of rodents, in Wolff JO, Sher-
man PW, eds. Rodent Societies: An Ecological &
Evolutionary Perspective. University of Chicago
Press, Chicago, IL, USA, p. 610.
Ylönen H, Ronkainen H (1994). Breeding suppression
in the bank vole as antipredatory adaptation in a pre-
dictable environment. Evolutionary Ecology 8, 658–
66.
Ylönen H, Sundell J, Tiilikainen R et al. (2003). Wea-
sels’ (Mustela nivalis nivalis) preference for olfacto-
ry cues of the vole (Clethrionomys glareolus). Ecolo-
gy 84, 1447–52.
Ylönen H, Eccard JA, Jokinen I, Sundell J (2006). Is the
antipredatory response in behaviour reected in stress
measured in faecal corticosteroids in a small rodent?
Behavioral Ecology and Sociobiology 60, 350–8.
340
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
© 2019 The Authors. Integrative Zoology published by International Society of Zoological Sciences,
Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd
H. Ylönen et al.
Zimova M, Hackländer K, Good JM et al. (2018). Func-
tion and underlying mechanisms of seasonal col-
or moulting in mammals and birds: what keeps them
changing in a warming world? Biological Reviews
93, 1478–98.
Zimova M, Mills LS, Nowak JJ (2016). High fitness
costs of climate change-induced camouflage mis-
match. Ecology Letters 19, 299–307.
Ylönen H, Haapakoski M, Sievert T, Sundell J (2019). Voles and weasels in the boreal Fennoscandian small mam-
mal community: what happens if the least weasel disappears due to climate change? Integrative Zoology 14,
327–40.
Cite this article as:
... The crash itself also has most often been connected to specialist predators, especially to small mustelids that can enter the holes and cavities of small mammals, their nests and the subnivean space in winter (Norrdahl and Korpimäki 1995;Boonstra et al. 2016;Ylönen et al. 2019). The predator hypothesis is supported by mathematical models (e.g. ...
... Late and unpredictable onset of snow cover and its earlier melting could increase the vulnerability of individuals with a mismatched white coat colour due to intra-guild predation by larger mammalian predators and resident owls. This, in turn, may have dramatic effects on vole dynamics (Ylönen et al. 2019) and further cascading trophic effects at the ecosystem level (Terraube et al. 2015). ...
... Dampening of the Swedish grey-sided vole cycle is more clearly attributed to changes in forest landscape structure (Hörnfeldt 2004;Ecke et al. 2006;Magnusson et al. 2013Magnusson et al. , 2015, while dampening of the cycles of the field vole along with their recent recovery, are more likely related to a climatic driver (Magnusson et al. 2015). In contrast, the disappearance and subsequent return of vole cycles in Finnish Lapland seem to be due to a more complex network of changing seasonality and predator-prey interactions in a whole rodent community (Henttonen 2000;Ylönen et al. 2019). Several arctic lemming populations showed perhaps the most compelling examples of collapsing cycles in recent years (Ims et al. 2008), e.g. in North-Eastern Greenland (Schmidt et al. 2012). ...
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Prey animals can assess the risks predators present in different ways. For example, direct cues produced by predators can be used, but also signals produced by prey conspecifics that have engaged in non-lethal predator-prey interactions. These non-lethal interactions can thereby affect the physiology, behavior, and survival of prey individuals, and may affect offspring performance through maternal effects. We investigated how timing of exposure to predation-related cues during early development affects offspring behavior after weaning. Females in the laboratory were exposed during pregnancy or lactation to one of three odor treatments: (1) predator odor (PO) originating from their most common predator, the least weasel, (2) odor produced by predator-exposed conspecifics, which we call conspecific alarm cue (CAC), or (3) control odor (C). We monitored postnatal pup growth, and we quantified foraging and exploratory behaviors of 4-week-old pups following exposure of their mothers to each of the three odour treatments. Exposure to odors associated with predation risk during development affected the offspring behavior, but the timing of exposure, i.e., pre-vs. postnatally, had only a weak effect. The two non-control odors led to different behavioral changes: an attraction to CAC and an avoidance of PO. Additionally, pup growth was affected by an interaction between litter size and maternal treatment, again regardless of timing. Pups from the CAC maternal treatment grew faster in larger litters; pups from the PO maternal treatment tended to grow faster in smaller litters. Thus, in rodents, offspring growth and behavior are seemingly influenced differently by the type of predation risk perceived by their mothers.
... First, similar to the negative predicted impact of a warming climate and associated elevation shifts in forest communities on American marten (Martes americana [55,56]), weasels could be negatively impacted by climate-induced shifts in habitat conditions and associated prey communities. Second, some weasel populations that turn white in the winter may be particularly vulnerable to climate change given the potential for coat color-habitat mismatch and associated elevated risk of predation [57,58]. Finally, given the relatively high levels of historical harvest, historical overharvest cannot be ruled out as a cause of decline in portions of their range where harvest rates were particularly high. ...
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Small carnivores are of increasing conservation concern globally, including those formerly thought to be widespread and abundant. Three weasel species (Mustela nivalis, M. frenata, and M. erminea) are distributed across most of North America, yet several recent studies have reported difficulty detecting weasels within their historical range and several states have revised the status of weasels to that of species of conservation concern. To investigate the status and trends of weasels across the United States (US) and Canada, we analyzed four separate datasets: historical harvests, museum collections, citizen scientist observations (iNaturalist), and a recent US-wide trail camera survey. We observed 87-94% declines in weasel harvest across North America over the past 60 years. Declining trapper numbers and shifts in trapping practices likely partially explain the decline in harvest. Nonetheless, after accounting for trapper effort and pelt price, we still detected a significant decline in weasel harvest for 15 of 22 evaluated states and provinces. Comparisons of recent and historical museum and observational records suggest relatively consistent distributions for M. erminea, but a current range gap of >1000 km between two distinct populations of M. nivalis. We observed a dramatic drop-off in M. frenata records since 2000 in portions of its central, Great Lakes, and southern distribution, despite extensive sampling effort. In 2019, systematic trail camera surveys at 1509 sites in 50 US states detected weasels at 14 sites, all of which were above 40o latitude. While none of these datasets are individually conclusive, they collectively support the hypothesis that weasel populations have declined in North America and highlight the need for improved methods for detecting and monitoring weasels. By identifying population declines for small carnivores that were formerly abundant across North America, our findings echo recent calls to expand investigations into the conservation need of small carnivores globally.
... In predator-prey interactions between mammals, olfactory cues (and the associated sensory abilities) are more important. These cues and senses are critical to predators and prey in locating and avoiding each other in the covered or enclosed habitats that they share, including tunnels and cavities where the animals live or nest Ylönen et al. 2019). ...
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Predator-prey interactions are a major evolutionary driver, affecting not only the direct mortality of prey species, but also their behaviours and reproduction. Prey species behavioural adaptations aim to mitigate the effects of predation and to maximise survival and individual fitness. These adaptations include the ability to signal a threat to conspecifics, e.g. via alarm calls or alarm secretions, or to detect predator presence via odours. In this thesis, I studied the effects of predator odours and conspecific alarm secretions on behaviour and reproduction bank voles (Myodes glareolus), a small mammal species inhabiting boreal forests. My work focused on three major points in comparing the direct predator cue and indirect conspecific cue: first, how the reproductive behaviour is affected by the predator odour or alarm pheromone, second, whether there are transgenerational effects and how they are exhibited in offspring, and third, what the chemical nature of these alarm secretions is. I conducted four experiments, which included both trials in semi-natural enclosures and under controlled laboratory conditions. I found evidence that exposure to conspecific alarm secretions causes a shift in voles’ reproductive behaviour, switching towards terminal investment. This became apparent with an increase in parturitions and an increased growth rate in larger litters, which did not occur when exposed to predator odour. I also found evidence of transgenerational effects, which affect aspects of the offspring’s exploratory and foraging behaviour. Additionally, I discovered that these behavioural effects are context-dependent and do not occur in every environment. Lastly, I identified a group of chemicals from voles’ alarm secretion, which are likely to be responsible for the observed effects. The results of my thesis fill a knowledge gap concerning chemical communication in mammals, and help to further understand the implications of predator presence on prey behaviour and reproduction.
... Predation is a process in which an organism consumes all or part of the body of another living organism and directly obtains nutrients to maintain its nutritional homeostasis (Ge, 2008). Studies of predation can contribute greatly to understanding predator-prey relationships and can also provide integral knowledge regarding food webs and multi-trophic levels interactions, which in turn influence ecological processes such as niche partitioning and interspecific competition (Burgar et al., 2014;Steele, Yi, & Zhang, 2018;Ylönen, Haapakoski, Sievert, & Sundell, 2019). In addition, studies of predation can screen for the main predators of target insect pest species as potential biological agents Yang, Liu, Yuan, Zhang, Peng, et al., 2017). ...
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Studies of predation can contribute greatly to understanding predator–prey relationships and can also provide integral knowledge concerning food webs and multi‐trophic level interactions. Both conventional polymerase chain reaction (cPCR) and quantitative PCR (qPCR) have been employed to detect predation in the field because of their sensitivity and reproducibility. However, to date, few studies have been used to comprehensively demonstrate which method is more sensitive and reproducible in studies of predation. We used a Drosophila melanogaster‐ specific DNA fragment (99 bp) to construct a tenfold gradient dilution of standards. Additionally, we obtained DNA samples from Pardosa pseudoannulata individuals that fed on D. melanogaster at various time since feeding. Finally, we compared the sensitivity and reproducibility between cPCR and qPCR assays for detecting DNA samples from feeding trials and standards. The results showed that the cPCR and qPCR assays could detect as few as 1.62 × 10³ and 1.62 × 10¹ copies of the target DNA fragment, respectively. The cPCR assay could detect as few as 48 hr post‐feeding of the target DNA fragment. But the qPCR assay showed that all spiders were positive after consuming prey at various time intervals (0, 24, 48, 72, and 96 hr). A smaller proportion of the technical replicates were positive using cPCR, and some bands on the agarose gel were absent or gray, while some were white and bright for the same DNA samples after amplification by cPCR. By contrast, a larger proportion of the technical replicates were positive using qPCR and the coefficients of variation of the Ct value for the three technical replicates of each DNA sample were less than 5%. These data showed that qPCR was more sensitive and highly reproducible in detecting such degraded DNA from predator's gut. The present study provides an example of the use of cPCR and qPCR to detect the target DNA fragment of prey remains in predator's gut.
... In predator-prey interactions between mammals, olfactory cues (and the associated sensory abilities) are more important. These cues and senses are critical to predators and prey in locating and avoiding each other in the covered or enclosed habitats that they share, including tunnels and cavities where the animals live or nest Ylönen et al. 2019). ...
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In the predator–prey arms race, survival-enhancing adaptive behaviors are essential. Prey can perceive predator presence directly from visual, auditory, or chemical cues. Non-lethal encounters with a predator may trigger prey to produce special body odors, alarm pheromones, informing conspecifics about predation risks. Recent studies suggest that parental exposure to predation risk during reproduction affects offspring behavior cross-generationally. We compared behaviors of bank vole (Myodes glareolus) pups produced by parents exposed to one of three treatments: predator scent from the least weasel (Mustela nivalis nivalis); scent from weasel-exposed voles, i.e., alarm pheromones; or a control treatment without added scents. Parents were treated in semi-natural field enclosures, but pups were born in the lab and assayed in an open-field arena. Before each behavioral test, one of the three scent treatments was spread throughout the test arena. The tests followed a full factorial design (3 parental treatments × 3 area treatments). Regardless of the parents’ treatment, pups exposed to predator odor in the arena moved more. Additionally, pups spend more time in the center of the arena when presented with predator odor or alarm pheromone compared with the control. Pups from predator odor–exposed parents avoided the center of the arena under control conditions, but they spent more time in the center when either predator odor or alarm pheromone was present. Our experiment shows that cross-generational effects are context-sensitive, depending on the perceived risk. Future studies should examine cross-generational behavioral effects in ecologically meaningful environments instead of only neutral ones. Significance statement We exposed bank voles to odors signaling predation risk to assess the effects parental predation exposure on the behavior of their offspring. Besides predator odor, we also assessed the role of a conspecific alarm cue as a novel way of spreading the predation risk information. Pup behaviors were assessed in the open-field arena, a standard way of assessing animal behavior in a wide range of contexts. We found that also alarm pheromone increased the time pups spend in the center of the arena similarly to predator odor. While previous studies suggested that offspring would be more fearful, our results indicate that the cross-generational effects are very context-dependent; i.e., they differ significantly depending on which scent cue is presented in the open-field arena. This shows the need for better tools or measurements to translate laboratory results into ecologically meaningful frameworks.
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Background During the past three decades, sustained population decline or disappearance of cycles in small rodents have been observed. Both anthropogenic disturbance and climate warming are likely to be potential drivers of population decline, but quantitative analysis on their distinct effects is still lacking. Results Using time series monitoring of 115 populations (80 populations from 18 known rodent species, 35 mixed populations from unknown species) from 1980 in China (spanning 20–33 yrs), we analyzed association of human disturbances and climate warming with population dynamics of these rodent species. We found 54 of 115 populations showed a decreasing trend since 1980, and 16 of 115 showed an increasing trend. Human disturbances and climate warming showed significant positive associations with the population declines of most rodent species, and the population declines were more pronounced in habitats with more intensified human disturbance such as cities and farmlands or in high-latitude regions which experienced more increase of temperature. Conclusions Our results indicate that the large-scale sustained population decline of small mammals in various ecosystems driven by the rapid increase of both climate warming and human disturbance is likely a signal of ecosystem dysfunction or transition. There is an urgent need to assess the risks of accelerated climate warming and human disturbance imposes on our ecosystems.
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SUMMARY The least weasel Mustela nivalis is known to have two subspecies in Scandinavia, where M. n. vulgaris is know from Denmark, Southern Sweden and South-eastern Norway. The subspecies M. n. nivalis is known to inhabit the northern regions of Norway and Sweden (and Finland). The distribution line between the two species in Scandinavia is described to be around the east-west line between Stockholm and Oslo, but only with a few documented reports of the southern distributed subspecies M. n. vulgaris in Norway This article describes some recent reports on the southern subspecies, and gives a short literature review on the least weasel in Norway and Fennoscandia. It discusses the possibility that the southern subspecies might become more abundant as less and more unstable snow cover in its distribution area through the period 1960 – 2010 are documented. This suggests a spreading northward according to climate change in the future. Maybe also along the coastline areas to the south west of Oslo fjord. Today the limits between the two subspecies is at about the 60th degrees latitude, but the last observation in Norway is now just north of the 61th degree latitude.
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Living in northern latitudes poses challenges to the animals that live in those habitats. The harsh environment provides a short breeding season where the sunlit summer nights provide little reprieve from visibility to predators and increased risk. In this paper, we tested the activity and food choice patterns of bank voles Myodes glareolus in early spring season, categorized by 18 h of daylight and 6 h of dusk in every day cycle. We found that territorial females showed a less predictable pattern of activity than males that were most active during the hours of dusk. The voles also showed preference to forage on high carbohydrate foods at sunset, while switching over to a more protein and fat-based diet towards sunrise. This shift is suggestive of a diet that is a direct adaptation to day-long fasts. Our results suggest a sensitive mechanism between food choice and predator avoidance in a system where light summer nights increase the predation risk considerably. Significance statement Bank voles, Myodes glareolus, are considered a model organism in ecological studies and have been used for studies of population cycles, predator-prey interactions and studies of territoriality with over a century of published records. In this study, we challenge two major preconceptions about these animals using behavioral bio-assays in a controlled environment. (1) We challenge the diurnal activity patterns of these rodents currently accepted to have a bi-modal distribution in summer months and show a unimodular activity pattern. And (2) we show that these animals are not opportunistic foragers but vary their diet to compensate for the stress of an extended daytime fast further supporting a nocturnal pattern of activity even in extreme sunlit nights where night lasts under an hour.
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Risk recognition by prey is of paramount importance within the evolutionary arms race between predator and prey. Prey species are able to detect direct predator cues like odors and adjust their behavior appropriately. The question arises whether an indirect predation cue, such as the odor of scared individuals, can be detected by conspecifics and subsequently affects recipient behavior. Parents may also transfer their experience with predators to their offspring. In two experiments, we assessed how direct and indirect predation cues affect bank vole (Myodes glareolus) foraging behavior, reproduction, and pup fitness. Weasel (Mustela nivalis) odor served as the direct cue, whereas the odor of weasel‐scared conspecifics, alarm pheromones, was used as an indirect cue and both of those were compared to a control odor, clean wood shavings. Alarm pheromones attracted female voles, measured as time in proximity to the treatment and foraging. Both predator odor and alarm pheromones enhanced reproduction compared to the control odor. Females treated with alarm pheromone had significantly higher pregnancy rates, and pups from predator‐treated mothers were significantly heavier at birth. Our study provides two novel ideas. First, the impact of a predator can be socially transmitted. Second, predation risk likely triggers terminal investment in reproduction.
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Prey strategically respond to the risk of predation by varying their behavior while balancing the tradeoffs of food and safety. We present here an experiment that tests the way the same indirect cues of predation risk are interpreted by bank voles, Myodes glareolus, as the game changes through exposure to a caged weasel. Using optimal patch use, we asked wild-caught voles to rank the risk they perceived. We measured their response to olfactory cues in the form of weasel bedding, a sham control in the form of rabbit bedding, and an odor-free control. We repeated the interviews in a chronological order to test the change in response, i.e., the changes in the value of the information. We found that the voles did not differentiate strongly between treatments pre-exposure to the weasel. During the exposure, vole foraging activity was reduced in all treatments, but proportionally increased in the vicinity to the rabbit odor. Post-exposure, the voles focused their foraging in the control, while the value of exposure to the predator explained the majority of variation in response. Our data also suggested a sex bias in interpretation of the cues. Given how the foragers changed their interpretation of the same cues based on external information, we suggest that applying predator olfactory cues as a simulation of predation risk needs further testing. For instance, what are the possible effective compounds and how they change “fear” response over time. The major conclusion is that however effective olfactory cues may be, the presence of live predators overwhelmingly affects the information voles gained from these cues. Significance statement In ecology, “fear” is the strategic response to cues of risk an animal senses in its environment. The cues suggesting the existence of a predator in the vicinity are weighed by an individual against the probability of encounter with the predator and the perceived lethality of an encounter with the predator. The best documented such response is variation in foraging tenacity as measured by a giving-up density. In this paper, we show that an olfactory predator cue and the smell of an interspecific competitor result in different responses based on experience with a live-caged predator. This work provides a cautionary example of the risk in making assumptions regarding olfactory cues devoid of environmental context.
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Abstract Predation involves more than just predators consuming prey. Indirect effects, such as fear responses caused by predator presence, can have consequences for prey life history. Laboratory experiments have shown that some rodents can recognize fear in conspecifics via alarm pheromones. Individuals exposed to alarm pheromones can exhibit behavioural alterations that are similar to those displayed by predator-exposed individuals. Yet the ecological and evolutionary significance of alarm pheromones in wild mammals remains unclear. We investigated how alarm pheromones affect the behaviour and fitness of wild bank voles (Myodes glareolus) in outdoor enclosures. Specifically, we compared the effects of exposure of voles living in a natural environment to a second-hand fear cue, bedding material used by predator-exposed voles. Control animals were exposed to bedding used by voles with no predator experience. We found a ca. 50% increase in litter size in the group exposed to the predator cue. Furthermore, female voles were attracted to and males were repelled by trap-associated bedding that had been used by predator-exposed voles. Movement and foraging were not significantly affected by the treatment. Our results suggest that predation risk can exert population-level effects through alarm pheromones on prey individuals that did not encounter a direct predator cue.
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Direct phenological mismatch caused by climate change can occur in mammals that moult seasonally. Two colour morphs of the weasel Mustela nivalis (M. n.) occur sympatrically in Białowieża Forest (NE Poland) and differ in their winter pelage colour: white in M. n. nivalis and brown in M. n. vulgaris. Due to their small body size, weasels are vulnerable to attacks by a range of different predators; thus cryptic coat colour may increase their winter survival. By analysing trapping data, we found that the share of white subspecies in the weasel population inhabiting Białowieża Forest decreases with decreasing numbers of days with snow cover. This led us to hypothesise that selective predation pressure should favour one of the two phenotypes, according to the prevailing weather conditions in winter. A simple field experiment with weasel models (white and brown), exposed against different background colours, revealed that contrasting models faced significantly higher detection by predators. Our observations also confirmed earlier findings that the plasticity of moult in M. n. nivalis is very limited. This means that climate change will strongly influence the mortality of the nivalis-type due to prolonged camouflage mismatch, which will directly affect the abundance and geographical distribution of this subspecies.
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Animals that occupy temperate and polar regions have specialized traits that help them survive in harsh, highly seasonal environments. One particularly important adaptation is seasonal coat colour (SCC) moulting. Over 20 species of birds and mammals distributed across the northern hemisphere undergo complete, biannual colour change from brown in the summer to completely white in the winter. But as climate change decreases duration of snow cover, seasonally winter white species (including the snowshoe hare Lepus americanus, Arctic fox Vulpes lagopus and willow ptarmigan Lagopus lagopus) become highly contrasted against dark snowless backgrounds. The negative consequences of camouflage mismatch and adaptive potential is of high interest for conservation. Here we provide the first comprehensive review across birds and mammals of the adaptive value and mechanisms underpinning SCC moulting. We found that across species, the main function of SCC moults is seasonal camouflage against snow, and photoperiod is the main driver of the moult phenology. Next, although many underlying mechanisms remain unclear, mammalian species share similarities in some aspects of hair growth, neuroendocrine control, and the effects of intrinsic and extrinsic factors on moult phenology. The underlying basis of SCC moults in birds is less understood and differs from mammals in several aspects. Lastly, our synthesis suggests that due to limited plasticity in SCC moulting, evolutionary adaptation will be necessary to mediate future camouflage mismatch and a detailed understanding of the SCC moulting will be needed to manage populations effectively under climate change.
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Changing coats with the season Many species of mammals and birds molt from summer brown to winter white coats to facilitate camouflage. Mills et al. mapped global patterns of seasonal coat color change across eight species including hares, weasels, and foxes. They found regions where individuals molt to white, brown, and both white and brown winter coats. Greater proportions of the populations molted to white in higher latitudes. Regions where seasonal coat changes are the most variable (molting to both brown and white) may provide resilience against the warming climate. Science , this issue p. 1033
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Excluded from the pursuit predator niche by better-adapted early felids and canids, the musteloids exploited other hunting strategies as grasslands proliferated in the Oligocene. Unconstrained by specialised running limbs, lineages evolved to excavate prey (badgers) and enter burrows (polecats). Others took to tree-climbing (martens, procynoids) and even swimming (otters). While some species specialised in rodent hunting (weasels) others became more generalist omnivores. In-turn the dispersion of these food types dictated socio-spatial geometries, allowing insectivorous, piscivorous and frugivorous species to congregate with varying degrees of social cohesion, often unified within subterranean burrows – a basis to group-living distinct from the pack-hunting felids and canids. Induced ovulation and delayed implantation feature in the mating systems of several species, evolved to ensure breeding success amongst low-density, solitary ancestors. Group-living musteloids exhibit degrees of reproductive suppression, allo-parental care and other cooperative behaviours, thus this contrarian superfamily provides unique insights into the basis of carnivore societies.