Download Effects of resource abundance on habitat selection and spatial

FACULTY OF SCIENCE
UNIVERSITY OF COPENHAGEN
Master’s thesis
Anne Eskildsen
Effects of resource abundance on habitat selection and
spatial behavior of the bank vole (Myodes glareolus)
Academic advisors:
Gösta Nachman, University of Copenhagen.
Peter Sunde, the National Environmental Research Institute.
Thomas Bjørneboe Berg, Naturama.
Submitted:
September 1 s t 2010
Contact
Anne Eskildsen. Institute of Biology, University of Copenhagen. Universitetsparken 15, DK-2100 København Ø.
[email protected]
Gösta Nachman. Department of Population Ecology, Institute of Biology, University of Copenhagen.
Universitetsparken 15, DK-2100 København Ø
Peter Sunde. The National Environmental Research Institute, University of Århus. Grenåvej 14, DK-8410 Rønde
Thomas Bjørneboe Berg. Naturama. Dronningemaen 30, DK-5700 Svendborg
Front page photos (clockwise from left):
Anne Eskildsen, Roger Butterfield, Countryside info, Sonny Munk Carlsen.
Master’s Thesis – Anne Eskildsen
Table of contents
Dansk resumé ...........................................................................................................................................................................3
Preface........................................................................................................................................................................................4
Acknowledgements ..................................................................................................................................................................5
Introduction ..............................................................................................................................................................................6
Manuscript: Resource abundance promotes risk-sensitive behavior in forest-dwelling, granivorous rodents – the
effects of mast fall on spatial behavior, habitat selection and barrier-crossing of the bank vole (Myodes glareolus) .......................14
Appendices ..............................................................................................................................................................................28
Appendix 1. Information on all tracked voles .........................................................................................................................29
Appendix 2. Photos of fieldwork locations ..............................................................................................................................30
Appendix 3. Description of barriers........................................................................................................................................31
Appendix 4. Map of fieldwork locations .................................................................................................................................32
Appendix 5: Home range maps..............................................................................................................................................33
Appendix 6. Individual preference ratios for cover and protection .............................................................................................35
Appendix 7. Capture rates.....................................................................................................................................................36
2
Master’s Thesis – Anne Eskildsen
Fødemængde havde et signifikant inverst forhold
til home range størrelse (m2), maksimal
bevægelsesafstand (m) og fangstrate (mus time-1).
Desuden sås et skift i habitatselektion, hvor rødmus
foretrak at blive i prædator-sikre mikrohabitater, så
som krat og grenbunker, nær deres home range
centrum så længe fødeudbudet var højt.
Udnyttelsesrater af bøgeolden var ligeledes
signifikant højere i prædator-sikre mikrohabitater,
selvom fødeudbudet var langt højere i åbne,
eksponerede områder.
En signifikant barriereeffekt af menneskeskabte
strukturer på rødmusens bevægelser blev fundet, og
det var således 15 gange mindre sandsynligt at finde
en mus på den modsatte side af en barriere, som på
den side, hvor den var blevet fanget. Enkelte
barriere-krydsninger blev dog registreret, hvilket
indikerer, at barrierer virker på den individuelle
niveau, og ikke på populationer som helhed.
De signifikante ændringer i arealbrug, aktivitet og
habitatselektion, som blev registreret indikerer, at
rødmusene, som respons på øget fødemængde,
implementerede mere lav-risiko adfærdsmønstre, der
inkluderede nedsat aktivitetsniveau og nedsat brug af
mikrohabitater med høj prædationsrisiko.
Under hele feltindsatsen blev der fanget
kønsaktive dyr (hanner med nedfaldne testes og
hunner med perforeret vagina), hvilket indikerede, at
der efter den normale ynglesæson, som løber fra
marts til oktober, forekom en forlænget yngleaktivitet
i oktober og november, hvilket er normalt i oldenår.
Blandt fældefangede mus sås der i løbet af efteråret
en signifikant vægtstigning hos hunner, men ikke hos
hanner, hvilket ud over en generel forbedring af
kropskondition, også indikerede, at der foregik
yngleaktivitet. Tidligere studier har vist, at kraftigt
øgede populationstætheder associeret med oldenfald
kan forårsage ændret rumlig adfærd, men da disse
populations-udbrud normalt først finder sted året
efter oldenfaldet, mener jeg ikke, at de observerede
ændringer i rumlig adfærd kan tilskrives
populationsdynamiske forhold.
I modstrid med tidligere undersøgelser blev der
ikke fundet nogen forskel i arealbrug eller
habitatselektion mellem de to køn, hvilket indikerer,
at den rumlige adfærd på undersøgelsestidspunktet
var mere påvirket af fødetilgængelighed end af
yngleaktivitet.
Dansk resumé
Byttedyr, så som småpattedyr, må konstant afveje
modstridende behov for, på den ene side set at
minimere eksponering overfor faktorer, der
nedsætter den individuelle fitness, og på den anden
side set at maksimere brugen af ressourcer, som er
nødvendige for reproduktion og overlevelse. Hos
småpattedyr sker denne afvejning typisk mellem
fourageringsaktivitet og den associerede eksponering
overfor rovdyr. Dog er mønstre i rumlig adfærd og
habitat selektion ofte svære at identificere på grund af
konstant temporal og rumlig variation i
ressourcetilgængelighed og prædationsrisiko.
Småpattedyr spiller desuden en økologisk
nøglerolle som frøspredere, for især eg og bøg, og
som en vigtig fødekilde for en række forskellige skovlevende rovdyr, så som ræve, mårdyr, ugler og andre
rovfugle, men de økologiske effekter af den løbende
reducering og fragmentering af skovhabitater på
småpattedyr er endnu uklare.
De ovenstående spørgsmål er tidligere søgt
besvaret især vha. studier af dyr i fangenskab eller
ved brug af fangst-genfangst. Den nylige udvikling af
letvægts-radiosendere har således kraftigt forbedret
mulighederne for at undersøge den rumlig adfærd
hos småpattedyr med baggrund i detaljerede
oplysninger
om
arealbrug,
aktivitet
og
habitatselektion.
I 2009 indtraf et oldenfald fra bøg (Fagus sylvaticus)
i de danske skove, hvilket forårsagede et midlertidigt
fødeoverskud for frøspisende organismer og gav en
god mulighed for at undersøge den associerede
adfærdsmæssige
respons
hos
skovlevende
småpattedyr. Rødmusen (Myodes glareolus) er en
velegnet modelorganisme til at undersøge effekterne
af ændrede økologiske forhold fordi den er udbredt
og afhængig af skovhabitater af høj kvalitet.
Ved at indsamle oplysninger om bevægelsen af 20
radiomærkede
rødmus,
der
levede
nær
menneskeskabte barrierer, og relatere disse
observationer til ændringer i oldenmængde, ønskede
jeg at forklare kausaliteten mellem fødetilgængelighed
og rumlige adfærdsmønstre så som arealbrug,
aktivitet, habitatselektion og barriere-krydsning.
Mine resultater viste, at den kraftige stigning i
fødemængde
som
oldenfaldet
forårsagede,
resulterede
i
en
hurtig
og
omfattende
omstrukturering af rødmusens rumlige adfærd.
3
Master’s Thesis – Anne Eskildsen
death cause. Importantly, physical harm to the animal
such as toe-clipping can be avoided, and testing has
shown that radio-collared animals are not inhibited in
their normal behavior while carrying the tag
(WEBSTER and BROOKS 1980).
In a recent study comparing the number of road
crossings by small mammals detected by use of
CMR, fluorescent powdering and telemetry, a
significantly greater proportion of animals were
detected crossing roads with telemetry than with the
two other methods (CLARK et al. 2001). This
demonstrates the higher information level that
telemetry studies provide, and underlines that it
should be the method of choice, when wishing to
conduct a comprehensive study of small mammal
behavior around barriers or spatial behavior in
general.
It should be noted that frequent spatial
observations such as telemetry fixes in their nature
are neither temporally nor spatially independent, and
therefore datasets are often autocorrelated. This issue
has been of some concern to spatial ecologists, often
leading to undesirable solutions such as sub-sampling
(WORTON 1987), which reduces the size of the
dataset and thus the biological meaningfulness of the
study. However, a study examining whether home
range estimators based on kernel densities required
serial independence of observations, concluded that
autocorrelation did not harm home range estimation
and encouraged researchers to maximize the amount
of observations using constant time intervals
between fixes to increase accuracy and precision of
estimates (SOLLA et al. 1999).
In my thesis I will be working with radio-collared
bank voles in order to address some aspects of small
mammal biology, namely space use and habitat
selection as a response to varying environmental
conditions. During the fall of 2009 there was a mast
fall from European Beech (Fagus sylvaticus) in Danish
forests, causing an excess of food resources for
granivorous rodents, and providing an excellent
opportunity to study the associated behavioral
responses of small mammals. The bank vole is a
useful model organism for understanding the effects
of changing environmental conditions, being
widespread and dependent on high-quality forest
habitat (AMORI 2008).
Furthermore, I will address the increasingly urgent
matter of habitat fragmentation, which constitutes
Preface
Small mammals are in general well described,
numerous, have short generation times and are easily
trapped, making them ideal model organisms for
studying population dynamical and behavioral
responses to varying environmental conditions. A
large number of studies have been published over the
past years, based chiefly on experiments with captive
animals (JONSSON et al. 2002; KOSKELA et al. 1997) or
using various forms of the capture-mark-recapture
(CMR)
method
(ANDREZEJEWSKI
and
MAZURKIEWICZ 1976; BUJALSKA 1990; BUJALSKA
1992; BUJALSKA and GRUM 1989; KORN 1986;
MAZURKIEWICZ 1994; ZHIGAREV 2005) but also
rarer methods such as the spool-and-line technique
(CRAINE 1985) and fluorescent marking (CLARK et al.
2001; MCDONALD and ST CLAIR 2004) have been
used.
These studies have contributed significantly to the
understanding of small mammal biology, however
there are some important methodological drawbacks
that should be taken into consideration when using
these methods, and which leave room for
improvement.
CMR is a useful tool for determination of
population densities, sex ratios and age structure,
however the shortcomings associated with
determination of space use and habitat selection by
means of this method are well known. Trapping may
provide data from a large amount of animals
however the amount of information given by these
studies on the movement of individuals is usually
limited, often consisting of only a handful of recaptures. Furthermore, trap-attraction or -avoidance
is a serious bias in small mammals, causing
individuals
to
either
become
seriously
overrepresented
or
completely
overlooked,
respectively (STRADIOTTO 2008). Lastly, immigration
and emigration dynamics are difficult, if not
impossible, to account for in both CMR and captive
studies (STRADIOTTO 2008).
The recent development of lightweight VHF tags
has greatly improved the opportunity to study small
mammal behavior in detail. Radio-collared animals
can be studied at a distance at any time of day and
with any time-interval, providing detailed information
about space use, activity level, microhabitat elements
that are preferred or avoided and sometimes even
4
Master’s Thesis – Anne Eskildsen
one of the most serious and widespread threats to
biodiversity today (FAHRIG 2002). The effects of
habitat fragmentation on small mammals are not fully
understood, and have, like most other studies of
spatial behavior, been dominated by the use of CMR
(APELDOORN et al. 1992; CLARK et al. 2001; HUITU et
al. 2008; MCGREGOR et al. 2008; PAILLAT and BUTET
1996; RICO et al. 2007a; RICO et al. 2007b), but also
recently genetic studies (GERLACH and MUSOLF
2000; REDEKER et al. 2006).
Low dispersal ability and great ecological
importance as a seed disperser (JENSEN 1985;
JENSEN and NIELSEN 1986) and prey-item to an
array of forest-dwelling species (JĘDRZEJEWSKI et al.
1993) makes the bank vole a suitable model-species
for studying the ecological impacts of habitat
fragmentation.
By collecting telemetry data from animals living
near man-made barriers I hope to contribute with
new information that may help to better understand
the consequences of this grave ecological threat.
In the following introduction I will give a short
description of the biology of small mammals, using
the bank vole as the chief example. Furthermore, it
will provide a brief review of the ongoing scientific
discussion regarding population dynamics, behavioral
dynamics, habitat selection and barrier effects of
small mammals.
The introduction is followed by a manuscript,
based on my experimental work in the field during
the fall and winter of 2009, and designed for
submission in Journal of Mammalogy.
Acknowledgements
This thesis and the experimental studies
constituting the empirical basis for my reflections
and conclusions could not have been realized
without:
The estate of Holstenshuus and the Bikuben
Foundation for allowing me to do fieldwork on their
property.
NATURAMA Museum of Natural History for
funding radio transmitters and providing other
necessary fieldwork equipment.
My advisors Gösta Nachman, Peter Sunde and
Thomas Bjørneboe Berg for providing valuable
academic guidance and support.
Bjørn Hermansen from University of Copenhagen
for GIS assistance.
Claus Hermansen from the Danish Forest and
Nature Agency for personal communication about
mast fall.
Claus Eskildsen and Dietmar Herwig for pleasant
and competent assistance in the field.
My office-mates Rikke Guldborg Hansen, Rasmus
Stenbak Larsen and Luigi Ponteri for good company
and more or less relevant discussions.
My friends and family for much needed patience
and moral support.
Anne Eskildsen, September 1st 2010
5
Master’s Thesis – Anne Eskildsen
dominant in small mammal communities found in
temperate forests (MAZURKIEWICZ 1994), with
typical densities varying between approximately 6-12
individuals per hectare and 50-100 individuals per
hectare (AMORI 2008). Breeding takes place from
March to October, but in years of very favorable
feeding conditions breeding has been known to
continue throughout the winter (ERIKSSON 1984).
Ecosystem role. Studies of seed dispersal have
documented an important role of rodents in the
dispersal of e.g. Fagus, Quercus and Corylus species,
which have evolved heavy and nutrient-rich seeds
not suitable for wind dispersal. By removing seeds
from where they originally fall and spacing them
more evenly, rodent-mediated seed dispersal
decreases seedling competition and increases the
probability of seedling survival, thus greatly affecting
the succession and population biology of the plant
species in question (JENSEN 1985; JENSEN and
NIELSEN 1986).
Importantly, the bank vole is a favored prey of an
array of forest-dwelling carnivores, e.g. foxes,
mustelids and raptors. Studies of the diet
composition of predator species in temperate
habitats have shown that the bank vole comprises up
to 30% of the diet of the red fox (Vulpes vulpes)
(JEDRZEJEWSKI and JEDRZEJEWSKA 1992), 40% of
the diet of the tawny owl (Strix aluco)(JEDRZEJEWSKI
et al. 1996) and 60% of the diet of the pine marten
(Martes martes) (ZALEWSKI 2005).
Spatial behavior. The term ‘home range’ is
traditionally used to define the area traversed by an
individual during its normal activities of food
gathering, mating and caring for young (BURT 1943).
However, a home range may also be used to define
the amount of space used by an animal at a certain
age, in a certain season, or may simply be confined to
the period of a study (ZHIGAREV 2005).
The term ‘home range’ should not be confused
with territory, i.e. a core area within the home range
which is defended by the animal (BURT 1943). The
home range may be divided into a number of
territories, e.g. nest territory, feeding territory and
breeding territory (BURT 1943; ZHIGAREV 2005).
The possession of a home range is a vital need for
small mammals in order to obtain stable access to the
resources needed for survival and reproduction and
range size may be related to the energetic
requirements, resource availability or behavioral
Introduction
The bank vole (Myodes glareolus, formerly
Clethrionomys glareolus, Schreber 1780) is a small vole
of 8-12 cm length, typically weighing between 15-40
grams (GEBEZYNSKA 1983).
Distribution. The species has a wide range in the
Palaearctic, which stretches from the British Isles
through continental Europe and Russia to Lake
Baikal. In the north, its range extends beyond the
Arctic Circle, and in the south it reaches northern
Turkey and northern Kazakhstan. It is widespread in
Europe, although it is absent from southern Iberia
and the Mediterranean islands (fig. 1). It is found
from sea level to 2.400 meters (AMORI 2008).
Fig. 1. Geographic range of the bank vole. Source: IUCN.
In Denmark, recolonization took place after the
last glaciation in the preboreal period from 95508250 B.C. (AARIS-SØRENSEN 2007). Today, the bank
vole is a common and widespread species throughout
most of Denmark, except for Northwestern Jutland
and most islands (JENSEN 2007).
Food and habitat preferences. Bank voles are
herbivorous-granivorous, but will to a lesser extent
also feed on fungi and animal foods. The species is
considered a habitat generalist and is known for its
high trophic plasticity with no deep specialization on
any particular plant species (GEBEZYNSKA 1983).
Bank voles are known to inhabit all kinds of
woodland, preferring densely vegetated clearings,
woodland edges, and river - and stream banks in
forests (MAZURKIEWICZ 1986; MAZURKIEWICZ 1994;
MIKLOS and ZIAK 2002). The species is numerically
6
Master’s Thesis – Anne Eskildsen
aspects of the species in question (KORN 1986;
MCNAB 1963). In mammal species with short life
spans and high reproductive rates, changes in food
abundance can lead to rapid fluctuations in
population density and space use (JENSEN 1982;
OSTFELD et al. 1996; STRADIOTTO 2009). Many
experiments conducted through the past decades
have investigated the link between these three factors
(BERGSTED 1966; BUJALSKA and GRUM 1989;
JONSSON et al. 2002; KORN 1986; KOSKELA et al.
1997; ZHIGAREV 2005), however, understanding
their causality is intrinsically difficult and still widely
discussed. For instance, individuals are expected to
range over smaller areas whenever food is abundant,
because they are able to move shorter distances to
cover their energetic needs (MCNAB 1963). This has
previously been demonstrated in food manipulation
studies where population sizes have been kept
constant (JONSSON et al. 2002). Meanwhile, an
alternative argument is that small mammals with
short generation times quickly will respond to high
food abundance by increasing population density,
causing a density-dependent decrease in range sizes
(BUJALSKA 1990). However, high population
densities may also be the direct consequence of
animals decreasing their range size in response to
favorable food conditions (MCNAB 1963; QUIRICI et
al. 2010)!
linkage between population density and spatial
behavior has been studied at great detail though the
past decades, with captive animals as well as in the
field. However, the mechanisms behind are still
widely discussed and centered around three basic
explanatory hypotheses:
The bottom-up hypothesis argues that food supplies
are the driving force behind population fluctuations
and hence space use. Seeds play an important role in
the diet of forest rodents and population densities in
temperate forest habitats are greatly affected by the
magnitude of seed production in e.g. European
beech (Fagus sylvatica) and oak (Quercus sp.) (HANSSON
1979; JENSEN 1982). The local synchronization of
large seed production which is seen in these species is
a strategy developed to maximize the probability of
seeds escaping predation, also known as the ‘seed
predator satiation strategy’ (JANZEN 1971). In winters
following these large seed productions bank voles are
able to maintain a high average weight, thus
prolonging their reproductive period throughout the
winter. This results in elevated population densities
the following year, also known as population
‘outbreaks’ (JENSEN 1982).
The responses of small mammal populations to
changes in food availability can either be investigated
by setting up direct feeding experiments with captive
animals or by measuring the abundance of food
resources actually available to the species in its
natural habitat and then correlating changes in
abundance of these food items to changes in
population density. While the former approach is
constrained by the use of unnatural food items and
controlled population dynamics, the latter approach
has been used successfully in a number of studies
(KREBS et al. 2010; OSTFELD et al. 1996; STRADIOTTO
2009) and is also the approach I have chosen to use
for my empirical work.
In years of large mast production, as was the case
in 2009, quantifying the amount of e.g. beech seeds
scattered on the forest floor is a simple way of
investigating the quality and quantity of food
resources available to granivorous forest rodents at
any given time.
The top-down hypothesis argues that predation,
parasites and diseases are the controlling
demographic factors. Population dynamics may be
very different for populations living at different
latitudes and thus, the top-down effect is especially
Fig. 2. Radiocollared bank vole. Photo: Sonny Munk Carlsen.
Population fluctuations. Small mammals population
densities are known to fluctuate greatly, and the
7
Master’s Thesis – Anne Eskildsen
pronounced in Northern European and Arctic
habitats, where food shortage is common and
predation pressure is high (HANSKI et al. 2001). This
results in large cyclic variation in small mammal
population densities, with peaks occurring every 3-5
years (GUSTAFSSON et al. 1983; HANSKI et al. 2001;
HANSSON 1969; KORPIMAKI et al. 2002; NORRDAHL
and KORPIMAKI 1995). Meanwhile, vole populations
residing at Southern latitudes are subjects to more
stable resource availability and modest predation
pressure, which is reflected by more stable
population densities with smaller and more irregular
fluctuations (HANSKI et al. 2001; JENSEN 1982;
NYHOLM and MEURLING 1979).
The social behavior hypothesis argues that social
interactions, including territoriality and infanticide
control population densities, thereby affecting spatial
behavior. In small mammals, it is well documented
that female space use is driven by territoriality, while
male space use is driven by access to females
(BUJALSKA 1992; KOSKELA et al. 1997; OSTFELD
1990; STRADIOTTO 2009; WOLFF 1993; ZHIGAREV
2005). Overall population density is therefore
believed to be driven mostly by the spatial behavior
of females.
Although territoriality among females is well
documented, the underlying behavioral mechanisms
are still somewhat unclear (JONSSON et al. 2002;
KOSKELA et al. 1997; WOLFF 1993). Infanticide
among females is a mechanism for territory
competition and females who have lost their pups by
infanticide will often surrender their nest site or
territory to the other female (WOLFF 1993). This
indicates that females with small territories to defend
will have higher reproductive success. Meanwhile,
reproductive females have an excess energy
requirement during pregnancy and lactation
(KACZMARSKI 1966), suggesting that reproductively
active females should have larger home ranges than
immature females due to their higher energetic needs.
Studies of captive females showed that home range
sizes were decreased during pregnancy and lactation,
and that supplementary feeding also decreased home
range size and home range overlap, while increasing
the reproductive success of female voles (JONSSON et
al. 2002; KOSKELA et al. 1997). These results suggest
that females with smaller territories to defend have
higher reproductive success because their offspring
are less vulnerable to infanticide by other females,
and indicate that an important function of female
territoriality is defense of offspring rather than
defense of food resources.
As described in the following manuscript, this
study shows that a rise in resource abundance
triggered significant behavioral responses among
bank voles, indicating a clear bottom-up effect.
Because a population outbreak related to this
elevated resource abundance would not occur before
the following spring (JENSEN 1982), population
dynamics are not thought to have played a key role in
the observed behavioral changes at the time of the
study. In stead, a combination of reduced activity,
due to high resource abundance (as discussed above),
and a change in resource exploitation - and habitat
selection strategy, (as discussed below), are thought
to have been the main drivers of the observed spatial
patterns.
Habitat selection. When a resource is used
disproportionately to its availability, use is said to be
selective (MANLY 2002). Habitat selection can be
seen as a trade-off process, where animals attempt to
minimize exposure to factors limiting individual
fitness at different spatial and temporal scales while
at the same time obtaining resources needed for
survival and reproduction (MASSÉ and CÔTÉ 2009).
In prey species such as small mammals, the most
common trade-off occurs between access to foraging
sites and exposure to predation risk and habitat
selection is therefore determined not only by
abundance and quality of food, but also by cover
(BROWN 1999; MASSÉ and CÔTÉ 2009; OKSANEN
and LUNDBERG 1995).
Identifying patterns of habitat selection is often
difficult due to the inherent plasticity that lies in its
nature. The distribution of resources, foraging costs,
population density, species interactions and predation
risk may vary both temporally and spatially, thereby
influencing patterns of habitat selection over space
and time (MANLY 2002; MASSÉ and CÔTÉ 2009;
RODHOUSE et al. 2010). Prey species’ response to
habitat-specific resource availability and predation
risk is also known as the risk allocation hypothesis
(LIMA and BEDNEKOFF 1999) or risk-sensitive
foraging (CARACO et al. 1980), demonstrating that
prey species are prone to take greater risks when
predation level is low (LIMA and BEDNEKOFF
1999)or energy expenditure is high (CARACO et al.
1980).
8
Master’s Thesis – Anne Eskildsen
Studies of bank vole habitat selection show a
preference towards older forest stands with dense
ground cover in the form of undergrowth and dead
woody material, providing food and antipredatory
refuges (MAZURKIEWICZ 1986; MAZURKIEWICZ
1994; MIKLOS and ZIAK 2002).
In a number of studies Mazurkiewicz showed
positive correlations between under storey vegetation
cover and home range size, intensity of space use,
rate of colonization, number of sexually active
individuals and survival rates of spring recruits, thus
demonstrating the great importance of undergrowth
density on the species’ spatial behavior and
demographics
(MAZURKIEWICZ
1986;
MAZURKIEWICZ 1991; MAZURKIEWICZ 1994).
A different habitat selection study showed that
preference for undergrowth plant species changed
throughout the year, but always so that plant species
that were the most important component of the
undergrowth during a particular season were
preferred (MIKLOS and ZIAK 2002). This indicates
that seasonality in microhabitat preference is
associated more with structural changes of the
undergrowth than with the plant species themselves
(MAZURKIEWICZ 1994; MIKLOS and ZIAK 2002),
suggesting that microhabitat preference is primarily
motivated by anti-predatory behavior.
Barrier effects. Habitat reduction and fragmentation are two of the most serious threats to
biodiversity and rank among the major causes of
species extinction (FAHRIG 2002). Harmful effects of
fragmentation include increased edge-effects, causing
increased predation risk and increased vulnerability to
spread of diseases and parasites, and isolation of
subpopulations, leading to inbreeding and a general
destruction of metapopulation dynamics, ultimately
causing an increased risk of extinction (YANES et al.
1995).
Understanding the effects of fragmentation on
small forest-dwelling mammals is of particular
interest given their relatively limited dispersal abilities
combined with the ongoing, worldwide extent of
anthropogenic habitat fragmentation inflicted upon
forest ecosystems (MOORE and SWIHART 2005;
PATTERSON and MALCOLM 2010). Denmark is no
exception, with many deciduous woodland localities
having been forced to give way to intense agricultural
practice (SCHNEEKLOTH 2005). Today only few large
continuous forests remain, and bank vole habitats are
therefore mostly found in isolated woodlots.
Traditionally it has been argued that small
mammal populations would be less affected by
fragmentation and landscape barriers because
populations living in or near them are large enough
to maintain long-term survival (MOORE and
SWIHART 2005; NUPP and SWIHART 1996). However,
recent studies show that habitat fragmentation is
linked to restricted movement and patch
colonization, reduced population growth rates and
reduced adult body weights, home range compaction,
reduced foraging opportunities, increased parasitism,
and elevated levels of inbreeding depression and
genetic drift (PATTERSON and MALCOLM 2010).
Today, infrastructural elements such as roads,
highways, and railroads have an especially widespread
effect on landscape structure, causing extensive
ecological impact on habitats and the species residing
in them (SPELLERBERG 1998). The harmful impacts
of roads on wildlife may either be direct, in the form
of casualties, or indirect by dividing the landscape
into many small, isolated patches (CLARK et al. 2001;
SPELLERBERG 1998). The barrier effect of roads has
been shown to be a non-linear function of traffic
intensity, road width, roadside characteristics, the
behavior of the species in question as well as their
sensitivity to disturbance (SEILER 2001).
Studies have shown that roads and highways
either inhibit small mammal crossing completely or
act as partial barriers, depending on road width
(CLARK et al. 2001; RICO et al. 2007a; RICO et al.
2007b). Rico et al (2007a) demonstrated that the
number of spontaneous road crossings by bank voles
was significantly lower than expected if roads had not
been barriers. By translocating animals to the
opposite side of the road where they had been
captured it was demonstrated that narrow roads were
partial barriers, acting at an individual level, while
wide roads were complete barriers, acting at
population level (CLARK et al. 2001; RICO et al.
2007b).
In recent years molecular methods have
increasingly been utilized to investigate the genetic
impacts on bank vole populations subjected to
landscape fragmentation (GERLACH and MUSOLF
2000; REDEKER et al. 2006). Gerlach & Musolf (2000)
showed that significant genetic subdivision arose
when a bank vole population was separated by a
9
Master’s Thesis – Anne Eskildsen
highway. However, neither study found significant
barrier effects of narrower country - or forest roads.
Hypotheses. Based on the theoretical background
described above, I have chosen to base my thesis on
five main hypotheses, and supporting predictions.
Predictions: Perceptual abilities will to some degree
enable voles to assess barrier-width, and with narrow
barriers posing a lesser potential threat than wide
barriers, cross these more willingly.
Hypothesis 1. Spatial behavior of small mammals is
affected by resource availability by means of risk-sensitive
foraging behavior.
Predictions: With increased food availability, small
mammals are able to invest less time, move shorter
distances and lessen exposure-risks to obtain the
needed amount of resources. This will result in
decreased movement distances, decreased home
range sizes and decreased capture rates for both
sexes.
Hypothesis 2. Habitat selection is affected by resource
availability by means of risk-sensitive foraging behavior.
Predictions: Due to risk-sensitive foraging behavior,
small mammals will adopt a more careful foraging
strategy in times of resource abundance, resulting in
microhabitats providing the best protection against
predator attacks being used more than expected, and
microhabitats providing poor protection against
predator attacks being used less than expected.
Hypothesis 3. Resource exploitation strategy is a
result of risk sensitive foraging behavior.
Predictions: Due to risk-sensitive foraging behavior,
small mammals will adopt a more careful foraging
strategy in times of resource abundance, and resource
exploitation will be greatest in the most secure
microhabitats, even though the availability of food is
higher in less secure microhabitats.
Fig. 3. Mast collection. Photo: Anne Eskildsen.
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Master’s Thesis – Anne Eskildsen
Manuscript:
Resource abundance promotes risk-sensitive behavior in forest-dwelling, granivorous rodents
– the effects of mast fall on spatial behavior, habitat selection and barrier-crossing of the bank vole (Myodes
glareolus)
ABSTRACT
Small mammals must constantly balance conflicting demands for resource intake and safety from predation,
however due to temporal and spatial variation in resource availability and predation risk, patterns of space use
and habitat selection are inherently difficult to identify. Furthermore, small mammals perform key ecological
functions in forest ecosystems, working as seed dispersers and serving as highly favored prey-items for many
forest-dwelling carnivores. However, the ecological effects of the ongoing reduction and fragmentation of forest
habitats on small mammals are still unclear. To address these questions, the spatial behavior of small mammals
has been widely studied using captive animals or capture-recapture methods, however these studies lack the level
of information that radio telemetry can provide. For this study, high-quality spatial data was collected from 20
radio-collared bank voles living near anthropogenic barriers. These data were subsequently related to changes in
habitat specific resource availability, in the form of beech mast, elucidating the causality between food abundance
and behavioral patterns with regard to space use, activity, habitat selection and barrier-crossing activities.
A temporary elevation in food abundance, caused by mast fall, resulted in a rapid and significant
destructuralization of the behavioral patterns of the bank vole. Food abundance had a significant inverse
relationship with home range size, maximum movement distance and capture rate. Furthermore, a shift in
microhabitat selection was seen, with bank voles preferring to stay in predator-safe microhabitats near their home
range center during times of high food abundance. Exploitation rates of beech mast were also shown to be
significantly greater in high-protection microhabitats, even though food was more abundant in open, predatorexposed areas. These significant changes in space use and habitat selection indicate that bank voles, as a response
to increased food abundance, adopted a risk-sensitive foraging strategy which included a significant decrease in
activity level and decreased use of high predation-risk microhabitats.
A significant barrier effect of anthropogenic structures on bank vole movement was found, with voles being 15
times less likely to be found on the opposite side of a barrier. However, a few rare barrier-crossing events
demonstrated that barriers worked at an individual level but not on the population as a whole, supporting
previous findings.
No difference was found in spatial behavior or habitat selection of males and females, suggesting that spatial
decision-making at the time of study was more heavily influenced by food availability than by breeding activity.
Key words: Myodes glareolus, telemetry, resource availability, spatial behavior, habitat selection, barrier effect, risksensitivity.
14
Master’s Thesis – Anne Eskildsen
(APELDOORN et al. 1992; CLARK et al. 2001; HUITU et
al. 2008; MCGREGOR et al. 2008; PAILLAT and BUTET
1996; RICO et al. 2007a; RICO et al. 2007b), but also
recently genetic studies (GERLACH and MUSOLF 2000;
REDEKER et al. 2006).
Traditionally it has been argued that small mammal
populations would be less affected by fragmentation
and landscape barriers because populations living in
or near them are large enough to maintain long-term
survival (MOORE and SWIHART 2005; NUPP and
SWIHART 1996). However, recent studies show that
habitat fragmentation is linked to restricted
movement and patch colonization, reduced
population growth rates and adult body weights,
home range compaction, reduced foraging
opportunities, increased parasitism, and elevated
levels of inbreeding depression and genetic drift
(PATTERSON and MALCOLM 2010).
Low dispersal ability and a huge ecological
importance as seed disperser (JENSEN 1985; JENSEN
and NIELSEN 1986) and prey-item to an array of
forest-dwelling species (JĘDRZEJEWSKI et al. 1993)
makes the bank vole a highly suitable model-species
for studies of the ecological impacts of habitat
fragmentation. By collecting telemetry data from
animals living near man-made barriers I hope to
contribute with new information that may help to
further understand the consequences of landscape
fragmentation on small mammals.
Crossing a barrier is associated with total exposure,
posing a high potential predation risk and I therefore
hypothesize that tracked animals will be highly
reluctant to barrier-crossing. However, perceptual
ability should to some degree enable voles to assess
barrier-width, and with narrow barriers posing a lesser
potential threat than wide barriers, cross these more
willingly (MECH and ZOLLNER 2002).
Furthermore, I will test the hypotheses that space
use, habitat selection, resource exploitation strategy,
capture rate and willingness to cross barriers are all
directly associated with a risk-sensitive foraging
strategy (BROWN 1999; CARACO et al. 1980; LIMA and
BEDNEKOFF 1999). I predict that elevated resource
abundance will allow small mammals to seek towards
an optimal trade-off between resource intake and
exposure to predation, resulting in decreased space
use and increased use of predator-safe microhabitats
(BROWN 1999; OKSANEN and LUNDBERG 1995).
INTRODUCTION
Small mammals are in general well described,
numerous, have short generation times, and are easily
trapped, making them ideal model organisms for
studying population dynamical and behavioral
responses to varying environmental conditions.
Furthermore, the recent development of lightweight
VHF tags has greatly improved the opportunity to
study small mammal behavior, providing detailed
information about space use, activity level and habitat
selection. In 2009 a mast fall from European Beech
(Fagus sylvaticus) occurred in Danish forests, causing an
excess of food resources for granivorous rodents, and
providing an excellent opportunity to study the
associated behavioral responses of small mammals.
The bank vole is a good model organism for
understanding the effects of changing environmental
conditions, being widespread and extremely
dependent on high quality forest habitat (AMORI
2008). By collecting spatial observations through
radio-telemetry and relating these observations to
changes in resource availability, e.g. beech mast, I
hope to elucidate the causality between a temporary
elevation in food abundance and small mammal
behavioral patterns with regards to space use, activity
and habitat selection.
In addition, this study will address the increasingly
urgent matter of habitat fragmentation, which
constitutes one of the most serious and widespread
threats to biodiversity today, ranking among the
major causes of species extinction (FAHRIG 2002).
Understanding the effects of fragmentation on
small forest-dwelling mammals is of particular interest
given their relatively limited dispersal abilities
combined with the ongoing, worldwide extent of
anthropogenic habitat fragmentation inflicted upon
forest ecosystems (MOORE and SWIHART 2005;
PATTERSON and MALCOLM 2010). Denmark is no
exception, with many deciduous woodland localities
having been forced to give way to intense agricultural
practice. Today only few large continuous forests
remain, and small mammal habitats are therefore
mostly found in isolated woodlots (SCHNEEKLOTH
2005).
The effects of habitat fragmentation on small
mammals are not yet fully understood, and have, like
most other studies of spatial behavior, been
dominated by the use of capture-recapture methods
15
Master’s Thesis – Anne Eskildsen
Tracking took place throughout the day from 7 am to
22 pm. Each animal was tracked on average for 2
weeks and as recommended by Seaman et al. (1999),
no less than 30 positions were obtained for each
animal (SEAMAN et al. 1999).
If an animal was predated or lost its collar before a
sufficient amount of fixes had been obtained, it was
replaced by a new animal and tracking was restarted.
When possible, radio-collared animals were recaptured, re-weighed and freed from their collar.
Habitat selection. In order to investigate which
habitat elements bank voles prefer or avoid, a simple
score system was developed which distinguishes
between two habitat categories, cover (under storey
vegetation such as herbs, bramble and ferns providing
hiding places, but with little or no physical protection
against predator attacks) and protection (branch piles,
thickets or fallen trees, where the animal may be
visible to predators, but is partially or fully protected
from attacks). Each category was subsequently
divided into four sub-categories that characterize the
degree of cover and protection (table 1).
MATERIALS AND METHODS
Fieldwork
Study area. Field data were collected from mid
September to late November 2009 in a 4x4 km
forested area on the Danish island of Funen
(Northing: 6107625; Easting: 582524). Part of the area
was in 2007 turned into a nature monument, owned
by the Bikuben Foundation, while the rest is owned
and driven as conventional forestry by the estate of
Holstenshuus.
Trapping and marking of animals. In order to
investigate spatial behavior and barrier sensitivity 10
plots of mature beech forest (Fagus sylvaticus) were
chosen within the area, each traversed by a road or a
path ranging in width from 5 meters to 40
centimeters. Along both sides of each barrier 10
multiple-capture live traps (Ugglan Special No. 2,
Grahnab, Sweden) were set along a linear transect at a
distance of 5-10 m from the road surface, spaced with
5 m. Traps were bedded with hay and baited with
sunflower seeds and carrot pieces and were checked
twice daily, once in the morning and once in the
evening.
All captured animals were sexed and weighed using
a 100 g Samson Super Salter spring weight (to nearest
0.5 g). One adult bank vole of each sex was
subsequently selected for radio tracking and was fitted
on location with a small mammal cable tie VHF
transmitter (BioTrack, Wareham, Dorset) weighing
approximately 1 gram. On one location, no males
were captured, and in stead, an extra female was
tagged. Only adult individuals weighing over 17 grams
were selected for collaring due to the size and weight
of the transmitters. After a short monitoring period in
a transportable cage, radio-collared animals were
released in the same place they had been caught.
Radiotracking. Due to logistical constraints and
short battery life of the transmitters, animals were
caught and tracked over several rounds, with 6-8
voles being tracked at a time. Tracking was performed
using a Sika radiotracking receiver (Biotrack,
Wareham, Dorset) and a Yagi antenna. Animal
positions were determined by triangulation with
consecutive fixes spaced by regular 50-minute
intervals as recommended by (SOLLA et al. 1999).
After each fix, information about the time, place and
activity level of the animal was recorded.
Table 1. Description of cover (a) and protection (b) sub-categories.
a)
b)
The microhabitat structure of each individual
home range with respect to cover - and protection
scores was registered by making meticulous handdrawn maps that were digitized in GIS.
Resource abundance and - exploitation. Resource
abundance and - exploitation was investigated by
quantifying changes in the amount of beech mast on
16
Master’s Thesis – Anne Eskildsen
the forest floor from November to April. Samples
were collected from three locations on three different
occasions, mid November, late December and early
April. In order to distinguish resource exploitation in
habitats with different degrees of cover and
protection, samples were collected using the habitat
score system described above. Four replicates were
sampled from each habitat sub-category on each
sampling occasion, resulting in a grand total of 288
samples. The litter samples were collected using a
small metal cylinder with a 20.3 cm diameter.
Sampling was carried out by identifying specific spots
with the wished habitat score, placing the cylinder on
the forest floor in that position and then collecting
the entire content of the ring into a paper bag, making
sure that no seeds were overlooked. The respective
cover- and protection score of each sample was noted
on the bag. Later, the content of each paper bag was
carefully sorted, and the number of beech seeds was
counted and entered into an Excel spreadsheet. Only
viable seeds that were not rotten or attacked by
insects were counted.
linear distances between consecutive fix points. All fix
points with low precision (>10 m) were discarded.
For both MMD and MDD, a GLIMMIX was used to
examine the relationship between movement and the
variables sex and time, with a log-link function and
vole id taken in as a random effect.
For MDD, movement was divided into three
periods: morning (until two hours after sunrise), day,
and evening (from two hours before sunset), using an
almanac, and a GLIMMIX was used to examine the
relationship between movement distances and the
variables time of day and home range size.
Weight. To examine the relationship between
weight and the variables sex and time for all captured
voles, a GLIMMIX was applied, with a log-link
function and vole id taken in as a random effect.
Furthermore, a GLM was used to examine the
relationship between weight and home range size for
radio-collared animals.
Capture rate and age structure. Capture rates were
calculated as the number of voles caught per trapping
hour for each of the 10 locations. A GLM was used
to examine the relationship between capture rate and
the variables sex and time. Also, animals were divided
into two age groups, juveniles (<15 g) and adults, and
the capture rates for these different groups for each
location were also calculated.
Habitat selection. To examine the habitat selection of
radio-collared animals, a circular buffer zone covering
exactly all fix points was created around each home
range center, using ArcGIS. This was done to define
the area that was realistically accessible to each
individual animal. Each buffer was divided into two
zones: 0-10 m, which was the core area of activity and
roughly 75 % of all fixes, and 10-20 m, which
included only peripheral activity and roughly 25 % of
all fixes. Separate selection analyses were performed
for these two zones.
Habitat selection was quantified by calculating
individual preference ratios (PR) for each animal with
respect to each cover- and protection sub-category.
This was done by generating evenly spaced random
points within the buffer zone of each animal in
ArcGIS and subsequently calculating the PR for each
habitat subcategory using a simple formula:
Data analysis
All statistical analyses were performed in SAS 9.2.
The relationship between response and predictor
variables was examined using a generalized linear
model (GLM) or a generalized linear mixed model
(GLIMMIX). When calculating GLMs, best models
were selected based on the Akaike information
criterion (AIC). When appropriate, response variables
were log transformed.
All spatial analyses were carried out with ArcGIS
9.3 (ESRI, Redlands, California).
Home range size. For each animal its home range size
was determined using the 95% fixed kernel method,
applying least squares cross-validation to select the
smoothing parameter (NILSEN et al. 2008). Home
range center points were subsequently calculated
using Hawth’s Analysis Tools 3.27. A GLM was used
to examine the relationship between home range size,
sex and time.
Movement patterns. The movement of each animal
was quantified in two ways. Firstly, the maximum
linear movement distance (MMD) in meters from the
home range center was calculated. Secondly,
minimum displacement distances (MDD) in meters
per hour were calculated for each animal by using
PR=ln(Nused/Navailable) – ln(Ntotal used/Ntotal available)
17
Master’s Thesis – Anne Eskildsen
PR > 0 indicated that a habitat was used more than
expected (use > availability), and PR < 0 indicated
that a habitat was used less than expected (use <
availability). In some cases one or several habitat
category had been completely ignored by an
individual, ie. use = 0, and a PR could not be
calculated. In order to calculate a PR in these cases a
very small, positive value was transferred to the
category, as recommended by Elston et al. (ELSTON et
al. 1996).
A one-sample t-test was used to examine whether
PR differed from 0, and a Student’s t-test was used to
test differences in PR between different habitat subcategories. Finally a GLIMMIX was used to examine
the relationship between PR and the variables sex,
habitat sub-category and time, with a log-link function
and vole id taken in as a random effect.
To model the overall probability of use and
availability of different habitat sub-categories for all
tracked animals a GLIMMIX was applied, using a
logit-link function and with vole id taken in as a
random effect. For simplicity, only protection was
considered in the analysis. Voles were never observed
to use sub-category 0 (open road), and it was
therefore omitted when modeling use.
Resource exploitation. A GLIMMIX was used to
examine the relationship between mast count and the
variables habitat sub-category and month, with a loglink function and location taken in as a random effect.
Barrier effect. To calculate barrier effect, buffer
zones and random points were generated using the
method described above and distance from the home
range center to each random point was calculated
using Hawth’s Analysis Tools in GIS. Using
GLIMMIX the barrier effect was calculated using the
relative use and availability of points on the same side
and opposite side of the barrier. Effects of distance to
the home range center, barrier width, sex, and time
were tested. To correct for over-dispersion in the
dataset, residuals were taken in as a random effect.
Furthermore, vole id was taken in as a random effect
and a logit-link function was used.
difference in home range size between the two sexes
and hence, they were pooled for further analyses. A
significant relationship with Day of Year (DOY) was
found for home range size (p<0.003), with area
decreasing throughout the study period for both sexes
(fig. 1a).
Movement patterns. The average MMD was 23 m (±2
SE) and no difference was found between the two
sexes. A highly significant relationship was found
between MMD and DOY (p<0.001) with distances
declining through the fall period (fig. 1b).
The average MDD was 8 m h-1 (± 1 SE). There
was no difference in MDD between the two sexes or
between morning, day and night. A noticeable
declining trend between MDD per hour (m h-1) and
DOY was seen, however the relationship was found
to be marginally insignificant (p<0.06) (fig. 1c).
a)
b)
c)
RESULTS
Fig. 1. a) Home range size (p<0.003), b) MMD (p<0.001) and
c) MDD (ns) as a function of time. Modeled trends with 95%
confidence limits are shown.
Telemetry data were obtained from 20 adult bank
voles, 9 males and 11 females.
Home range. The average home range size for all
voles was 628 m2 (± 134 SE). There was no significant
18
Master’s Thesis – Anne Eskildsen
A highly significant relationship was found
between home range size and MDD (p<0.0002) (fig.
2).
Capture rate. During the field study, a total of 148
bank voles (81%), 29 yellow-necked mice (Apodemus
flavicollis) (16%) and 6 shrews (Sorex sp.) (3%) were
caught. No difference was found in the capture rate
of male and female bank voles, and the two sexes
were pooled for further analysis (see data on capture
rates in app. 7).
DOY had a significant effect on the number of
voles captured pr. hour (p<0.005), with capture rates
decreasing markedly in September and October, but
increasing again in November. When differentiating
between juveniles and adults, it was found that
capture rate of juveniles was highest in late September
and late November (trend not significant, p<0.3),
while the capture rate of adults decreased steadily
throughout the study period with only a small
increase in late November (p<0.004) (fig. 4).
Fig. 2. MDD as a function of time (p<0.0002). Modeled trend
with 95% confidence limits is shown.
Weight. The average weight for males was 16.6 g
(±0.8 SE) and 20.0 g (±0.7 SE) for females. Testing
showed a significant relationship between weight and
DOY for females (p<0.02), with weight initially
increasing and then decreasing during the late fall (fig.
3). There was no relationship between weight and
DOY for males.
Fig. 4. Modeled trends for capture rate of all voles (p<0.005),
adults (p<0.004) and juveniles (ns) as a function of time. 95%
confidence limits are not shown, but can be found in app. 7.
Habitat selection. Testing of the relationship between
sex and preference ratio showed no difference in
habitat preference between the sexes and they were
pooled for further analysis. Furthermore, no
difference was found in preference for sub-categories
representing absent, low and high cover/protection
(i.e. C1 vs. P1, C2 vs. P2 and C3 vs. P3) and
consequently these classes were also pooled for
further analyses (in the following named CP1, CP2
and CP3).
0-10 meters from the home range center. Preference
ratios for CP1 vs. CP2 and CP1 vs. CP3 were
significantly different (p<0.002 and p<0.001
respectively), whereas there was no difference in
preference for CP2 vs. CP3. CP1 was used
significantly less than expected (p<0.01), while CP3
Fig. 3. Modeled weight of all captured females (red, p<0.02) and
males (blue, ns) as a function of time. Dotted lines indicate 95%
confidence limits.
The average weight for voles fitted with a radiocollar at time of capture was 20.6 g (± 1.0 SE) for
males and 23.0 (±1.2 SE) for females. Out of 20
radio-collared voles, five males and five females were
recaptured. Recaptured males had on average gained
0.6 g (±1.0 SE), while females on average had gained
1.2 g (± 1.7 SE).
19
Master’s Thesis – Anne Eskildsen
was used significantly more than expected (p<0.02).
The use of CP2 did not differ from the expected (fig.
5).
far away. Contrastingly, sub-categories 2 (moderate
protection) and 3 (high protection) showed an
opposite trend, with high probabilities of use near the
home range center and probabilities subsequently
falling as the distance to the home range center
increased (p<0.0001 for all).
The modeled availability of protection subcategories 0-3 is shown in fig. 8. Results indicate that
roads (sub-category 0) and open forest floor (subcategory 1) were unlikely to occur near the home
range center, while moderate and high protection
areas (sub-categories 2 and 3) were more likely to
occur the closer the home range center (p<0.0001 for
all). Note that probabilities across sub-categories do
not always add up to 1 due to standard errors
associated with the modeled estimates.
Fig. 5. Average preference ratios for 0-10 meters from the home range
center. The x-axis indicates the relation when there is no selection, i.e.
use = availability.
10-20 meters from the home range center. Preference
ratios for the three categories did not differ
significantly. The use of all three categories was
significantly less than expected (p<0,05) (fig. 6).
a)
Fig. 6. Average preference ratios for 10-20 meters from the home
range center. The x-axis indicates the relation when there is no
selection, i.e. use = availability.
b)
A comparison of the preference ratios for the 0-10
m and 10-20 m zones showed a significant difference
in the use of all three categories. Category CP1 was
used significantly less in the core-area zone than in
the peripheral zone (p<0,05), while the use of CP2
and CP3 was significantly higher in the core-area zone
than in the peripheral zone (p<0,01 and p<0,02,
respectively). Statistical testing showed no relationship
between preference ratio and DOY.
Modeled probability of use and availability. The modeled
use of protection sub-categories 1-3 are shown in fig.
7. Modeling showed that voles were less likely to use
sub-category 1 (open forest floor) when they were
close to their home range center than when they were
c)
Fig. 7. Modeled use of a) P1, b) P2 and c) P3. Females are
indicated with solid red lines and males with solid blue lines. Dotted
lines indicate 95% confidence intervals for each sex.
20
Master’s Thesis – Anne Eskildsen
Resource availability and exploitation. Mast fall in 2009
began during the last week of September,
approximately DOY 270, and ended in the middle of
November, approximately DOY 310 (personal
communication, Claus Simonsen, The Danish Forestand Nature Agency).
It was found that cover- and protection score had
a highly significant effect on mast count (p<0.001),
with large numbers of mast being found in open
habitat sub-categories, e.g. 0 and 1, and small
numbers being found in closed habitat sub-categories,
e.g. 2 and 3 (fig. 8 and 9). Furthermore, month had a
highly significant effect on mast count for both cover
and protection (p<0.001), with decreasing amounts of
mast being found from November to April (fig. 9 and
10).
a)
b)
c)
Fig. 9. Mast count for protection sub-categories. Standard errors are
shown.
d)
Fig. 8. Modeled availability of a) P0, b) P1, c) P2 and d) P3.
Females are indicated with solid red lines and males with solid blue
lines. Dotted lines indicate 95% confidence intervals for each sex.
Fig. 10. Mast count for cover sub-categories. Standard errors are
shown.
21
Master’s Thesis – Anne Eskildsen
Modeling of mast count data showed that in
November and December, beech mast exploitation
was significantly higher in areas with a high protection
score (p<0,001), while in April exploitation was
greatest in habitats with a high cover score (p<0,001).
Barrier effect. Barrier effect is defined as the
probability of an animal being found on the opposite
side of the barrier, assuming that both sides of the
barrier are equally accessible to it. During the study
period only two barrier-crossings were observed. The
crossings were performed by one single female vole,
which on two separate occasions crossed the same 3.5
m wide asphalt road. The crossings took place in early
October with one day’s separation.
A highly significant barrier effect was found
(p<0.0001) with voles being roughly 15 times less
likely to be found on the opposite side of the barrier
where they were caught. Furthermore, there was a
significant relationship between the distance of the
barrier from the home range center and barrier effect,
which it exerted (p<0.001).
Barriers affected the two sexes equally and no
change in barrier effect as a function of DOY or
barrier width was found.
necked mouse (ANDREZEJEWSKI and MAZURKIEWICZ
1976; JONSSON et al. 2002; STRADIOTTO 2009).
Movement patterns. Inverse trends were seen for both
MMD and MMD over time (DOY), however the
trend for MMD was marginally insignificant (fig. 1b
and 1c). There may be several explanations for this,
including large standard errors, assumed linear
movement between data points and long time
intervals between measurements, leading to an
unknown amount of the actual movement being
neglected. Still, a highly significant relationship was
found between MMD and home range size (fig. 2),
indirectly confirming the hypothesis that increased
resource availability should lead to decreased activity.
No difference was found in activity during
mornings, daytime and evenings, contradicting
previous findings showing that voles are crepuscular,
with peak activity-periods during the early and late
hours of the day (GREENWOOD 1978). Again, this is
likely related to decreased space use associated with
high food abundance, allowing animals to take fewer
and shorter foraging trips throughout the day, or
utilize food caches already within the den (MILLER
and ELTON 1955).
Intersexual differences in space use. Surprisingly, there
was no difference in home range size between the two
sexes. This contrasts with many previous findings that
have shown male ranges to be significantly larger than
females’ (BERGSTED 1966; BUJALSKA 1990; KORN
1986; ZHIGAREV 2005) and suggests the possibility
that ranges were more heavily influenced by food
availability than by breeding activity at the time of
study. Sexually active animals (males with scrotal
testes and females with perforated vaginae) were
captured throughout the study period, making it
unlikely that male ranges contracted due to lesser
breeding activity during the fall.
Capture rates. As expected, the increase in food
abundance was reflected by a decrease in capture rates
during trapping sessions, with large numbers of voles
being caught during trapping sessions in the early fall,
while food availability was still low, and low numbers
being caught in the late fall when food abundance was
very high (fig. 4). This pattern suggests a decrease in
exploratory and risky behavior among small
mammals, thus making them less likely to be captured
and is supported by previous findings (CURRYLINDAHL 1956).
DISCUSSION
In this study I have investigated the space use and
habitat selection of a forest-dwelling granivorous
rodent, which benefits from a temporarily unstable
food resource, e.g. beech mast. Consistently with my
expectations, a heavy mast fall lasting from September
to November of 2009, leading to a dramatic
temporary elevation in food abundance, caused a
rapid and significant destructuralization of the
behavioral pattern of the bank vole with regard to
space use, activity and habitat selection.
Home range. Results showed a strong inverse
relationship between resource availability and space
use, with home range sizes of both sexes decreasing
significantly as food abundance grew during the late
fall (fig. 1). These changes are believed to be
associated with temporary resource saturation and
support the hypothesis that an increase in resource
availability should allow animals to move shorter
distances to obtain necessary resources, resulting in
decreased space use. Identical patterns have
previously been found in other studies of granivorous
rodents, including the bank vole and the yellow-
22
Master’s Thesis – Anne Eskildsen
Habitat selection. Against expectation, telemetry data
showed no overall changes in bank vole habitat
selection as a function of time, indicating no response
to improved feeding conditions (BROWN 1999;
MAZURKIEWICZ 1986; MAZURKIEWICZ 1994; MIKLOS
and ZIAK 2002; OKSANEN and LUNDBERG 1995).
However, preference ratios did show that voles used
high-protection habitat types such as thickets,
bramble and branch piles significantly more when
they were closer to their home range center, while
unsafe habitat types such as open forest floor were
used significantly less. Knowing that voles spent a
greater amount of time close their home range center
as a response to increased food availability, it
therefore seems reasonable to indirectly confirm the
hypothesis that increased food availability should lead
to increased risk-sensitive behavior, allowing animals
to shift their habitat preference towards more secure
habitats. This conclusion was further underpinned by
both preference ratios and modeled probabilities of
use, showing that voles used low-protection habitats
significantly less while close to their home range
center than when they ventured out on trips far away
from their core-area. These results demonstrate that
voles strategically choose to place their core areas of
activity in microhabitats that offer high levels of
protection from predators. Also, they show that
unsafe habitat types were mostly encountered on trips
far away from the home range center, which may be
associated with high-risk activities such as territorial
behavior, foraging or search for mates.
It is important to realize that other factors than
resource availability might have played a role in the
observed changes in activity patterns of bank voles.
For instance, a general reduction of under storey
vegetation cover associated with leaf-fall, increasing
visibility to predators, may have been an important
factor inducing risk-sensitive behavior among bank
voles (MAZURKIEWICZ 1994; MIKLOS and ZIAK
2002).
It is unclear why modeling of the telemetry data
did not show a relationship between habitat selection
and time, thereby not directly supporting the
hypothesis that habitat selection would shift towards
preference of more secure habitats as a response to
increased food availability. However I find it highly
plausible that even slight imprecisions in the tracking
and digitalization process may have played a large role
when working with such small home ranges and
movement distances.
Resource availability and - exploitation. Bank voles were
found to be numerically dominant in the small
mammal community of the study area, comprising
81% of the catch. Assuming equal trap ability among
the small rodent species present in the area the bank
vole is therefore assumed to be chiefly responsible for
mast consumption. The yellow-necked mouse was the
only other granivorous rodent species caught during
the study, comprising 16% of the captures.
Modeling showed that protection score was the
most contributing factor to mast exploitation during
November and December, while cover-score was
more contributing in April, indicating that voles
preferred to forage in areas with high protection
compared to areas with high cover. The shift that was
observed in April may be explained by the fact that
resource levels in high-protection areas were
approaching near-total depletion, subsequently
forcing rodents to seek less secure foraging areas,
where mast supplies were still high. Furthermore, a
thick snow cover lasting from late December to mid
April may have facilitated foraging in areas otherwise
unattractive, due to the extra cover provided by the
snow (KARLSSON and POTAPOV 1998), and is
underlined by a large removal of mast from the open
forest floor in this period (fig. 8 and 9).
Unfortunately, due to limited battery life of
transmitters and time constraints on fieldwork effort,
this could not be supported by telemetry data.
Interestingly, a rise in both overall capture rate (fig
4) and MMD (fig 1b) was seen among tracked animals
in late November, indicating that bank voles already
at this point were increasing their activity level,
perhaps due to a beginning depletion of mast supplies
in their nearest, most secure surroundings.
Small mammals were never observed to forage on
open roads, and removal of mast from this habitat
type is thought to have been chiefly undertaken by
granivorous forest birds, eg. wood pidgeon (Columba
palumbus), brambling (Fringilla montifringilla) and
chaffinch (Fringilla coelebs) or simply by wind removal.
Weight and reproduction. Improved feeding
conditions resulted in a periodical increase in body
weight of trapped animals, however the trend was
only significant for females (fig. 3). This indicated
that, apart from a general improvement of body
condition, the normal breeding season was followed
23
Master’s Thesis – Anne Eskildsen
by another peak in breeding activity in the late fall,
which was also confirmed by the capture of
reproductively active animals throughout the study
period.
Also, a general trend of decreasing average weight
in captured individuals of both sexes during
November indicated that a recruitment of juveniles
took place after mast fall, which was further
confirmed by trapping data, that showed the highest
capture rates of juveniles during the end of the
normal breeding season and then again during late
November, after mast fall had taken place, although
this trend was not significant (fig. 4).
Collared voles that were recaptured, had on
average gained weight, which, consistently with the
findings of previous studies, confirms that normal
behavior was not altered or inhibited by radiocollaring (WEBSTER and BROOKS 1980). Radiocollared females had on average gained a little more
weight than males, which was likely due to breeding
activity. As uncollared bank voles were not
individually marked, no control data on body weight
over the season could be attained.
No relationship was found between weight and
home range size of radio-collared voles, which is in
accordance with previous findings (KOSKELA et al.
1997).
Population dynamics and space use. Although evidence
exists supporting that prolonged breeding activity
took place during the late fall, previous studies have
shown that actual population boosts due to mast fall
do not occur before the following spring (JENSEN
1982). I therefore find it unlikely that any changes in
spatial behavior at this early stage could be ascribed to
changed demographics within the population.
Barrier effects. Roads were shown to exert a highly
significant barrier-effect on bank vole movement,
confirming the hypothesis that anthropogenic
structures have an obstructive effect on small
mammal movement. However, during the study two
spontaneous
road-crossings
were
observed,
demonstrating that roads do not act as impenetrable
barriers, but that crossing events are rare. This
supports previous findings showing that roads act as
barriers on the individual level, but do not affect small
mammal populations as a whole (CLARK et al. 2001)
and confirms the hypothesis that anthropogenic
structures have an obstructive effect on small
mammal movement (CLARK et al. 2001; RICO et al.
2007a; RICO et al. 2007b). It is likely that a spring
population boost may have resulted in an increased
number of road-crossing due to a demographically
driven increase in social stress and hence, territorial
conflicts, however this could not be confirmed within
the frame of this study.
It was hypothesized that perceptual ability to some
degree would enable voles to assess barrier-width, and
with narrow barriers posing a lesser potential threat
than wide barriers, cross these more willingly.
However, results showed that road width per se was
not influential on barrier effect, and it is interesting
that, when inside the forest, animals were able to
traverse distances much larger than the width of the
road. Instead, the observed reluctance to cross
barriers may be linked to risk-sensitive behavior, with
animals preferring to stay in habitats with a high
degree of vegetation cover, as it has already been
demonstrated. It is therefore also probable, as
hypothesized, that the very high resource abundance
that was present during the study period could lessen
dispersal and road-crossing incentives among small
mammals. Still, care must be taken when deducting
barrier effects only from short-term observations
such as the ones at hand and a larger sample size of
animals, tracked over a longer period of time and
under varying environmental conditions, ideally
supplemented by genetic studies, would be necessary
to fully understand the effect of man-made barriers
on small mammals such as the bank vole.
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Appendices
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Appendix 1. Information on all tracked voles
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Appendix 2. Photos of fieldwork locations
Examples of five barriers of varying type and width used for the study a) Grusvej 2, 3.0 m b) Dyrehavevej, 3.5 m c) Ridesti 2, 0.6
m d) Bjerregårdsvej, 4.5 m and e) Hjulsporet, 2.0 m
a)
d)
b)
e)
c)
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Master’s Thesis – Anne Eskildsen
Appendix 3. Description of barriers
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Appendix 4. Map of fieldwork locations
Names of field work locations are indicated in white.
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Appendix 5: Home range maps
Each home range is indicated by 95%, 75% and 50% kernel contours. Red lines indicates female home ranges and blue lines
indicates male home ranges.
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Appendix 6. Individual preference ratios for cover and protection
‘-‘ indicates that the habitat type was not available.
Preference ratios for the 0-10 m zone.
Preference ratios for the 10-20 m zone.
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Master’s Thesis – Anne Eskildsen
Appendix 7. Capture rates
Capture rates (voles h-1) for all voles, adults, juveniles, females and males with 95% confidence limits.
36