BEHAVIORAL ECOLOGY - ORIGINAL PAPER

Does personality in small rodents vary depending on populationdensity?

Katri Korpela • Janne Sundell • Hannu Ylonen

Received: 2 June 2010 / Accepted: 28 September 2010 / Published online: 26 October 2010

� Springer-Verlag 2010

Abstract Personality means an individual’s unique way

of behaving and reacting to the environment. It is a stable

and heritable trait, which is expressed consistently in dif-

ferent situations. The aim of our study was to develop

novel tests to depict the personality structure of the bank

vole Myodes glareolus, and to determine if the phase of the

population cycle, i.e. population density, affects personality.

We focused on some central aspects of bank vole behav-

iour: mobility, risk taking, exploratory behaviour, domi-

nance, and aggressive behaviour towards pups. These

behaviours were chosen because they directly affect bank

vole survival or fitness or are classified as important factors

of personality in other species. In total, 192 males from

different populations went through four behavioural tests,

in which 20 variables were measured. The tests were

repeated after 3 weeks, which verified that all traits were

stable, i.e. repeatable between trials. Three personality

compounds emerged, named extroversion, novelty seeking

and infanticide. Extroversion included dominance and

mobility, while novelty seeking consisted of risk taking and

exploration. Infanticide encompassed all indices measuring

harmful behaviour towards pups. Mobility and dominance

were connected, possibly because both seem to depend on

condition. Time spent in captivity increased extroversion,

which may be explained by good food, stable conditions

and acclimation to strong social cues. Novelty seeking was

connected to repeatability which could mean that novelty

avoiding individuals adjust their behaviour to match new

environments. Population density affected the infanticide

trait but not novelty seeking or extroversion.

Keywords Myodes (Clethrionomys) � Dominance �Infanticide � Novelty seeking � Personality

Introduction

Personality can be defined as an individual way of

behaving which is stable and, to a great extent, heritable

(Loehlin et al. 1998; Bouchard and Loehlin 2001; van Oers

et al. 2005; Hampson and Goldberg 2006). It is a dynamic

psychophysical system, which results in the individual’s

unique adjustment to its environment (Alport 1937).

Behaviour is affected by both personality and the

environment.

In traditional ecology, individual variation in behaviour

has been treated as random and maladaptive noise around

the population optimum. During the last decade, it has

become increasingly evident that this individual variation

may in many cases be adaptive. The optimal behaviour

may not be the same for all individuals, but may instead

vary according to, e.g., the inherited and acquired physio-

logical traits as well as experiences and the life-history

Communicated by Roland Brandl.

K. Korpela

Department of Biological and Environmental Sciences,

University of Helsinki, P.O. Box 65, 00014 Helsinki, Finland

J. Sundell � H. Ylonen

Department of Biological and Environmental Science,

Konnevesi Research Station, University of Jyvaskyla,

P.O. Box 35, 40014 Jyvaskyla, Finland

J. Sundell

Lammi Biological Station, University of Helsinki,

Paajarventie 320, 16900 Lammi, Finland

K. Korpela (&)

Department of Biological and Environmental Science,

University of Jyvaskyla, P.O. Box 35, 40014 Jyvaskyla, Finland

e-mail: katri.korpela@jyu.fi

123

Oecologia (2011) 165:67–77

DOI 10.1007/s00442-010-1810-2

stage of the individual (Daly and Wilson 1999; Dall et al.

2004; Sih et al. 2004; Re’ale et al. 2007). Personality

affects the life-time reproductive success of an individual

and can be understood as a component of its life history

(Dingemanse and Re’ale 2005; Boon et al. 2007; Re’ale

et al. 2007, 2009; Quinn et al. 2009).

The existence of animal personality and the correlation

of different behaviours mean that an individual’s behaviour

is not infinitely flexible. An individual cannot adjust its

behaviour to perfectly match each situation, but behaves in

a similar manner in many different types of situations. This

is contrary to what is commonly assumed in ecological

research. For example, an active animal may benefit from

this type of behaviour when searching for food or mates in

a safe environment but may suffer from it when predation

risk is high. This also means that a single behaviour should

not be studied in isolation from others that constitute a

personality trait, because the total fitness will be affected

by all correlated behaviours and possible physiological

traits.

Animal behaviour, and even animal personality, is

normally studied using one or a few traits at a time.

Often animal personality is assumed to be represented by

the shy/bold or proactive/reactive typology, regardless of

the species in question. However, the structure of per-

sonality is an adaptation to the species-specific selection

pressures. Therefore, we take a different perspective. Not

assuming any preconceived personality structures, we

aim to characterize the structure of personality in our

study species in relation to the social environment

the individual comes from. In order to understand the

behavioural ecology of a species, one should understand

the underlying personality structure—how the different

behavioural and physiological traits are linked to each

other. This requires measuring many traits in the same

individuals.

Our study species, the bank vole Myodes glareolus, is a

granivorous species occupying a wide variety of habitats

from meadows to forests. Finnish populations exhibit

multiannual cyclicity, with a cycle length of 3–5 years. The

social organisation of bank voles is characterised by

exclusively defended female territories and large male

home ranges that overlap with other male home ranges and

several female territories (Bondrup-Nielsen and Karlsson

1985). Males sharing overlapping home ranges form a

dominance hierarchy. Infanticide, the killing of unrelated

conspecific young, can account for a significant proportion

of juvenile mortality in many microtine species including

the bank vole. It can limit population growth and be an

effective regulator of population dynamics (e.g. Andreassen

and Gundersen 2006), as well as shape the evolution of

social systems and reproductive strategies (reviewed in

Agrell et al. 1998; Ebernsperger 1998).

The bank vole is a common model organism in

ecological research. Thus, a comprehensive understanding

of its behaviour is needed, which was the aim of this study.

In order to find out the structure of bank vole personality,

we studied several behavioural traits and used principal

components analysis to examine if and how they are

connected to each other. The following set of behaviours

that cover many important aspects of bank vole behaviour

were chosen to be studied: mobility, risk taking, explor-

atory behaviour, dominance rank and infanticidal behav-

iour. These were selected on the basis of them being known

either to be connected to bank vole fitness or to comprise

central aspects of personality in other species (e.g. Kruczek

1997; Norrdahl and Korpimaki 1998; Banks et al. 2002;

van Oers et al. 2005; Boyer et al. 2010). Stability of the

traits was tested by determining the repeatability of each

behavioural characteristic over time, as this is a prerequisite

for the existence of personality.

Personality traits have been found to affect the fitness of

an individual through their effects on, e.g., survival,

reproductive success or growth (reviewed in Biro and

Stamps 2008; Smith and Blumstein 2008). The fitness

effects may change with environmental conditions and the

life-history stage of the individual (Boon et al. 2007).

Population density can be regarded as the most important

factor in the social environment of voles, also affecting

many other important aspects of the environment such as

predation and food abundance. Therefore, we expected

population density to influence at least some of the per-

sonality traits in the species. As we aimed to conduct the

study in a short time frame, we decided to use geograph-

ically distinct populations differing in the multiannual

cycle phase. One of the populations was, however, tested

during two cycle phases. As voles are very short-lived and

can never experience a whole continuum of a population

cycle, our method should be as valid as studying a single

population over a whole cycle. We expected the different

environments with differing selection pressures to be

reflected in individual personalities in a consistent manner.

Materials and methods

Experimental animals

The experiment was conducted in a laboratory at the

Konnevesi Research Station in May, June, July and October

2008. A total of 192 bank voles from five different popu-

lations were tested. The animals were either captured in

different locations in Finland or were born in the laboratory

(see Table 1 for details).The three wild populations were in

different phases of the population cycle; one of these was

captured during two cycle phases. In addition, we used a

68 Oecologia (2011) 165:67–77

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laboratory-born population (first and second generation)

and an enclosure population, which originated from the

same first and second generation laboratory-born animals.

The founding animals of the laboratory and enclosure

populations were captured in Konnevesi in 2007 during the

increase phase of the population cycle. The enclosure

population had spent the previous winter before the

experiments in 0.25-ha outdoor enclosures. Using two

laboratory-born populations differing in their degree of

confinement enabled us to take into account the possibility

of laboratory effects on bank vole behaviour and person-

ality profiles.

Prior to testing, the animals had spent anything from a

few days to several months in the laboratory where they

were housed in standard mouse cages (43 9 26 9 15 cm)

with sawdust and hay as bedding under a 16L:8D photo-

period. Lights were switched on at 0600 hours. Food and

water was available ad libitum.

Only male voles were chosen for the experiment to

avoid any effects that the sex of the animal or the oestrus

cycle phase of a female might have on its behaviour. Also,

males have been found to be more consistent in their

behavior than females (Bell et al. 2009; Shuett and Dall

2009). All animals were mature, their ages varying from

2 months to over a year. This made it possible to find out if

age affects personality and its stability.

Voles were weighed twice per testing period: immedi-

ately before the first test and after the last one. In the final

analyses, change in weight during the interval period was

used, and the highest weight recorded for an individual was

taken as a measure of body size.

Behavioural tests

In the experiment, each individual went through four

different behavioural tests during a 3-day testing period. To

find out how stable the voles’ behaviour was, all animals

were aimed to be tested twice. Between the two testing

periods, there was an interval of 18–21 days (due to

logistical reasons, 30 voles had a longer interval of

40 days). Tests were performed in random order, and

between tests all animals spent several hours in their cages,

so that their behaviour would not be affected by the pre-

vious test. Testing was conducted between 0900 and

2000 hours. The bank vole has several activity peaks dur-

ing the night, whereas daytime activity remains at a

somewhat lower but steady level (Ylonen 1988; Lopucki

2007). Hence, it was assumed that the time of day would

not affect the voles’ behaviour. All tests were conducted

under the same light conditions as in the housing labora-

tory. According to our long-term experience, bank voles as

polyphasically active animals are active during daylight,

both in the field and in the laboratory. Furthermore, for

reliable observations, adequate light conditions were

necessary.

Apart from the maze used in the exploration test, all

testing arenas were cleaned with water and 70% ethanol

after each test. The ethanol was given sufficient time to

evaporate before the arena was used again.

Quantitative traits, be they behavioural or physiological,

that are influenced by several genes together with the

environment are expressed at the population level as a

continuum. This is certainly true for a trait as complex as

personality. Hence, the full spectrum of behaviour cannot

be captured by treating it as a categorical variable. In

animal research, personality or behavioural traits are often

reduced to the extremes, while in reality the majority of

individuals lie somewhere in the middle of a given

dimension. For this reason, we measured and analysed all

behaviours as continuous variables.

Risk taking

A plastic testing arena (38 9 59 9 19 cm) in a small room

next to a one-way mirror was used to observe the male

voles’ risk taking behaviour. One end of the arena was

covered with a thin layer of bedding from several females’

cages. A Petri dish with sunflower seeds and pellets was

placed in the centre of this end. In the opposite end, there

was a cardboard tube for a hiding place. The smell of

Table 1 Number of male bank voles Myodes glareolus used in the study, their origin (time of capture, phase of population cycle), when tested

and how many times tested

Origin of population n Captured Tested Phase of cycle

Muhos 44 May 2008 Summer 9 2 Low/increase

Koli 31 May 2008 Summer 9 2 Peak

Konnevesi 1 19 Autumn 2007 Summer 9 2 Increase

Konnevesi 2 63 May 2008/September 2008 Summer 9 2/October 9 1 Peak

Laboratory 18 Lab-born Summer 9 2

Enclosure 17 Lab-born Summer 9 2

The laboratory and enclosure populations were 1st and 2nd generation laboratory-born animals kept in different environments. They originated

from the Konnevesi 2007 population

Oecologia (2011) 165:67–77 69

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females and food was meant to entice the vole to come out

of the hiding place. The arena was oriented so that the end

with the food was closest to the door.

At the beginning of the test, the vole was placed next to

the cardboard tube and left alone in the room. The vole

usually went inside the tube. Three behaviours were

recorded: the vole’s latency to come out of the tube, to

come to the opposite end of the arena with the bedding, and

to take a seed or pellet and start to eat. Even if the vole did

not show all of these behaviours within 10 min, the next

part of the test was started.

After the vole had started to eat (or 10 min had passed),

the observer opened the door suddenly and jumped in the

room. This usually startled the vole and made it run back to

the hiding place. Sometimes, it was necessary to make

more noise by clapping hands and step closer to the arena

to achieve this effect. When the vole was back in the hiding

place, its latency to come out again was recorded. Again,

the maximum observation time was 10 min.

Exploratory behaviour

A wooden maze (40 9 124 9 10 cm) with 24 compart-

ments and wheat flour sprinkled on the floor was used to

measure the voles’ exploratory behaviour. A vole was

placed in one corner of the maze, the lights were turned off

and the door closed. After 10 min, the vole was taken back

to its cage. The vole’s movements left tracks in the flour, so

it was easy see how many compartments the vole had

visited. Each individual got an exploration score between 1

and 24.

After each test, the flour was changed and, if necessary,

the maze was cleaned with a paper towel. As the maze was

made out of wood, it was not possible to clean it with

ethanol. The flour may have covered some of the smells the

previous voles had left in the maze, but it is more than

likely that the voles could smell that others had been there

and possibly followed their tracks. However, this was the

case for all individuals and the voles did not move in a

consistent manner. Each individual made a unique pattern

in the flour and did not seem to follow the tracks of the

previous vole.

Dominance

Urine marking during dyadic interaction has been estab-

lished as a reliable measure of social rank in male voles

(Myodes glareolus: Horne and Ylonen 1996; Microtus

oeconomus: Sun et al. 2007). The males’ marking behav-

iour in the presence of another male was tested using an

arena (40 9 67 9 40 cm) divided into two longitudinal

halves. Two focal males of approximately the same size

were placed in the arena, each in one half. They could

communicate through a 5-cm-high wire mesh window in

the dividing wall. The test was conducted overnight in

darkness lasting 12 h. Each vole got a piece of potato and a

laboratory pellet (Labfor�) at the beginning of the test.

Underneath the arena was brown packing paper which

absorbed the voles’ markings so that they could be checked

later with UV light. After the test, each half of the arena

was divided into 48 squares of 5 9 52 cm each. The

dominance score of the vole was determined by how many

of these squares had been marked, yielding a score (urine-

marking-value, UMV; Horne and Ylonen 1996) between 1

and 48. All individuals marked at least one square.

Aggressive behaviour towards pups

This test was conducted in the same arena and observing

room as the risk taking test. A one-way mirror was used to

observe the male voles’ behaviour in the presence of pups.

Two pups, a male and a female, were placed in one end of the

arena in opposite corners with some bedding from their cage

to increase the smell of the nest. The pups were from the

same litter, and were not related to the male. All pups were

3–5 days old. One pup was normally used in three consec-

utive tests, after which it was returned to its mother. Bank

vole mothers accept their pups even after the pups have been

handled by humans. Pups were not kept away from their

mother for more than 1 h, and during the tests they were

inside protective tubes made of wire mesh (diameter 1.5 cm,

length 5 cm), so that they could not get hurt by the male

voles. The tube was small and light and did not hinder the

adult voles from sniffing, moving or attacking the pup.

The male was placed in the other end of the arena and

left alone in the room. The male’s behaviour was observed

behind the one-way mirror for 10 min. In a few cases, the

male became so aggressive that the test was ended before

the 10 min had passed. Aggressive behaviour towards pups

is usually treated as a discontinuous trait, individuals being

classified as either infanticidal or not (e.g. Poikonen et al.

2007). However, Labov et al. (1985) propose that a third

category, ‘‘partially infanticidal’’, be included until it is

established that partially infanticidal and infanticidal ani-

mals have the same fitness, which has not been addressed

in studies on voles. Therefore, we measured aggressive

behaviour on continuous scales.

Five different behaviours (staying still, moving, sniffing

a pup, nibbling on the wire mesh tube or attacking a pup)

were recorded as well as how the individual divided its

time between these behaviours.

Data analysis

The repeatability (stability) of the behaviours was tested as

Spearman rank order correlations between scores from the

70 Oecologia (2011) 165:67–77

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two consecutive tests. Behaviours with significant corre-

lation coefficients were taken as indicators of personality

and were included in the analyses. Rank order correlation

was used, as it is insensitive to trends that are common to

the whole population, thus avoiding the problem of mean-

level change (Hayes and Jenkins 1997).

For each behavior, we calculated an individual repeat-

ability score (adapted from Assendorpf 1990):

Repeatability score

¼ 1� score 1 - score 2ð Þ=maximum difference½ �2n o1=2

Repeatability scores ranged from 0 to 1, with 1

indicating no change in behaviour. A mean repeatability

score for each individual was calculated as the average of

repeatability scores for different behaviours. In a similar

manner, an average repeatability score was calculated for

each behaviour over all individuals.

Animals were divided into three groups based on their

age: 1–2 months, n = 16; 2–4 months, n = 50; over

6 months, n = 128). One-way ANOVA was used to exam-

ine the effect of age on repeatability of each behavioural trait.

Mating is suggested to inhibit infanticidal behaviour at

the time of parturition, preventing a male from killing his

own pups (e.g. vom Saal 1985). Not all voles had spent

enough time in the laboratory to be sure that they were not

influenced by this inhibition. Because of this, instead of

taking the average score, the more aggressive result was

used in the analyses. Infanticide in the bank vole has been

found to be a repeatable trait (Poikonen et al. 2007), and in

spite of the confounding effects of inhibition, correlations

between the two consecutive tests were significant.

Although the sex of the pup was recorded for the purpose

of another study (Korpela et al. 2010), the sexes were not

treated separately in this study.

Principal components analysis was used as the data

reduction method to find the underlying personality

dimensions. Most variables had positive skewness and

some were normally distributed. Transformations of

skewed variables resulted in a lower factorability and more

difficult interpretation of the components, so untrans-

formed variables were used. As PCA was used descrip-

tively to summarise relationships in the variables, violation

of normality should not be a problem (Tabachnik and

Fidell 2007). As PCA searches for linear correlations

between variables, multivariate linearity is assumed. It was

impractical to check all bivariate combinations of 20

variables for linearity, but several of them were spot-

checked. No implication of nonlinearity was found.

Kaiser’s criterion, Scree plot and Monte Carlo PCA

parallel analysis were referred to when determining the

number of components to extract. Significance of

component loadings was estimated with the aid of a table

of critical values provided by Stevens (2002). Only

significant loadings were used in the interpretation and

naming of the components.

Component scores were calculated with the regression

method, and ANOVA was performed with the component

scores as dependent variables and population, age, weight

and time spent in the laboratory as explanatory variables.

The wild populations were regarded as indicators of the

different cycle phases, while the laboratory and the enclo-

sure populations were included in order to study the effects

of the respective artificial environments on behaviour. The

voles were divided into four groups based on how many

weeks they had spent in the laboratory: \1 week, n = 50;

3–4 weeks, n = 44; 5–6 weeks, n = 8; over 8 weeks,

n = 25. A Bonferroni adjusted alpha level of 0.017 was

used as the critical value. All analyses were carried out with

SPSS 16.

Results

Stability of behavioural traits

Correlations between the two consecutive tests were highly

significant for most variables (Table 2). Mean repeatability

scores for the stable variables ranged from 0.63 to 0.99,

their distribution being negatively skewed (i.e. most indi-

viduals had high repeatability scores). Repeatability was

not affected by age (F2,129 = 0.244; P = 0.784).

Structure of bank vole personality

Twenty variables were included in the PCA (Table 2). The

Kaiser–Meyer–Oklin value was 0.856 ([0.6 indicates

adequate factorability) and Bartlett’s test of sphericity was

significant (P \ 0.0001), supporting factorability of the

data. Eigenvalues of the first three components were larger

than the critical value obtained from the parallel analysis.

The Scree plot suggested two to four components to be

retained. Three components resulted in the most mean-

ingful solution with several high loadings on all of them,

and it explained 64% of total variation (Table 2). The

components were named according to the individual

behaviours that they encompassed: infanticide, novelty

seeking and extroversion.

Oblimin rotation showed that there was a relatively high

correlation between infanticide and novelty seeking

(r = 0.451), which would be in favour of an oblique

rotation. However, there were no structural differences

between the Oblimin and Varimax solutions, Varimax

having only slightly more complex variables, so the

orthogonal rotation was chosen for the sake of simplicity

Oecologia (2011) 165:67–77 71

123

and because it is the commonly used rotation in personality

studies. Loadings above 0.450 were considered when

naming the components.

Factors affecting personality

A separate two-way ANOVA for each personality dimen-

sion was conducted to find out which factors affect them

(Fig. 1; Table 3). Weight and age did not significantly

affect any of the personality traits, and interaction effects

were not found.

Infanticide was affected by population density. The high

density populations (Konnevesi mean = 2.31, SE = 0.127

and Koli mean = 2.36, SE = 0.191) were significantly

more aggressive than the low density one (Muhos

mean = 1.58, SE = 0.213).

Novelty seeking was not affected by population density

or time spent in captivity. The only significant difference

was between the increase phase (mean = 1.45; SE =

0.051) and the laboratory population (mean = 1.15; SE =

0.039).

Table 2 Varimax rotated loadings of the individual traits on the three personality dimensions, Spearman correlation between two consecutive

tests, its P value and the average repeatability score

Individual traits Personality dimensions Extroversion rs P Repeatability

Infanticide Novelty seeking

Number of attacks 0.897 -0.175 0.042 0.318 0.001 0.992

Time spent attacking 0.889 -0.053 -0.039 0.266 0.013 0.939

Aggression rate 0.878 -0.336 0.130 0.325 0.001 0.640

Time spent in contact with pup 0.850 -0.132 0.246 0.39 0.000 0.975

Number of pups attacked 0.816 -0.264 0.147 0.226 0.026 0.639

Latency to attack pup 20.784 0.355 -0.118 0.252 0.012 0.902

Latency to move -0.241 0.802 -0.083 0.365 0.000 0.975

Latency to come out -0.094 0.796 0.028 0.448 0.000 0.925

Latency to reach sawdust -0.093 0.790 -0.172 0.545 0.000 0.824

Latency to eat -0.283 0.655 -0.198 0.501 0.000 0.767

Latency to come out after startle -0.224 0.634 -0.020 0.61 0.000 0.852

Latency to sniff pup 20.478 0.621 -0.219 0.423 0.000 0.959

Repeatability 0.082 20.564 0.036

Time spent still 20.502 0.558 20.479 0.383 0.000 0.760

Exploration 0.118 20.501 0.048 0.505 0.000 0.759

Dominance 0.020 -0.131 0.683 0.43 0.000 0.889

Weight change 0.029 -0.163 20.629

Time spent sniffing pups 0.438 -0.250 0.608 0.234 0.027 0.994

Time spent moving 0.351 20.490 0.588 0.487 0.000 0.722

Number of sniffs 0.475 -0.422 0.516 0.29 0.016 0.918

Percentage of variance explained 28.092 24.417 11.587

Significant loadings are in bold. Negative loadings mean a negative correlation between the trait and the personality dimension

Origin of population

Mea

n sc

ore

(+/-

SE

)

0

1

2

3

4 Infanticide Novelty seeking Extroversion

Lab-born Enclosure Muhos Konnevesi Konnevesi Koli 2007 2008

14 16 18 18 35 26

Fig. 1 Personality profiles of the different populations of bank voles

Myodes glareolus. Error bars represent ±1 SE. Muhos captured 2008,

low phase; Konnevesi 2007 increase phase; Konnevesi 2008 peak

phase; Koli captured 2008, peak phase. The laboratory and enclosure

populations were 1st and 2nd generation laboratory-born animals kept

in different environments. They originated from the Konnevesi 2007

population

72 Oecologia (2011) 165:67–77

123

Time spent in captivity (Fig. 2) had a significant effect

on extroversion. According to Tukey HSD, the peak den-

sity populations Koli (mean = 1.45; SE = 0.13) and

Konnevesi 2008 (mean = 1.50; SE = 0.11) did not differ

from the low density population Muhos (mean = 1.88;

SE = 0.17). The increase phase population, Konnevesi

2007 (mean = 2.93; SE = 0.19), had significantly higher

extroversion values, due to the fact that this population had

spent the longest time in captivity. The laboratory popu-

lation had the highest extroversion values (mean = 3.16;

SE = 0.28).

Discussion

Personality dimensions in the bank vole

The aim of this study was to measure the stability of some

central aspects of bank vole behaviour, to study how they

relate to each other, and to find out how population density

and the laboratory environment affect personality. The

results fit well with what is currently known on animal

personality. Three separate personality traits were found to

comprise male personality: novelty seeking, extroversion

and infanticide, which together explained 64% of the

observed variation in behaviour. Both extroversion and

novelty seeking encompassed behaviours measured in

different situations, suggesting that these traits are stable

not only over time but also across situations. Infanticide

was unrelated to the other behavioural traits. risk taking

behaviour was linked to exploration and behavioural sta-

bility, and mobility correlated with dominance. Age and

weight did not affect behaviour or its repeatability, con-

sistent with a meta-analysis by Bell et al. (2009). Time

spent in captivity affected the males’ extroversion. This

may be explained by the long-term exposure to strong

social cues and crowdedness on the one hand, but by good

food and stable laboratory conditions on the other.

All behaviours were repeatable over a 3-week period,

which, considering the average life span is only a few

months, is a long time. Some of the rs values, especially the

ones measured in the infanticide test, seem modest. This

was expected, not only because of the relatively long

interval but also because of the possible inhibitory effects

of mating on infanticidal behaviour. There is some dis-

crepancy between the repeatability scores and the rs values,

due to mean level change in some variables, to which the

repeatability score is sensitive. Nevertheless, the overall

image is that of consistent individual differences in

behaviour in the species.

Novelty seeking

Novelty seeking comprised behaviours measured in several

different situations, implying that it is a stable not situa-

tion-specific trait. Animals that visited many compartments

of the maze (in the dark, in the exploration test) also started

moving and exploring soon after they were placed in a

novel area (in the light, in the infanticide and risk taking

tests). They were also quick to take a sunflower seed

(a novel food item) and start eating, and preferred not to

stay long in a hiding place even after they had been star-

tled, indicating a high tolerance for possibly dangerous

situations.

Novelty seeking does not seem to be greatly affected by

environmental conditions, as neither population density nor

Table 3 Effects of population, weight, time in captivity and age on personality traits

Explanatory variable Novelty seeking (n = 121) Extroversion (n = 121) Infanticide (n = 122)

Population, df = 4 (Konnevesi 2007 and 2008 combined) F = 2.75; P = 0.31 F = 9.87; P \ 0.0001 F = 3.2; P = 0.016

Population, df = 5 (Konnevesi 2007 and 2008 separated) F = 3.02; P = 0.013 F = 19.73; P \ 0.0001 F = 2.52; P = 0.033

Weight, df = 1 F = 1.19; P = 0.276 F = 0.65; P = 0.799 F = 4.19; P = 0.043

Time in captivity, df = 3 F = 0.75; P = 0.392 F = 8.106; P \ 0.0001 F = 0.001; P = 0.977

Age, df = 1 F = 0.16; P = 0.687 F = 1.00; P = 0.319 F = 0.08; P = 0.778

Significant results are in bold

Fig. 2 Mean scores (±SE) of extroversion of bank vole males in

relation to time spent in captivity

Oecologia (2011) 165:67–77 73

123

time spent in captivity showed a significant effect on this

trait. It can be regarded as an individually determined

strategy, most likely dependent on the specific character-

istics of the individual.

It has been suggested that behavioural repeatability

could be part of an individual’s personality, with some

individuals characterised by highly stable behaviours

across time and situations, and some having more vari-

ability in their behaviour (Sih et al. 2004). For this reason,

repeatability was treated as a trait among others. Interest-

ingly, individuals scoring high on novelty seeking exhib-

ited high overall test–retest repeatability, whereas the low

scoring ones had lower repeatability scores. This seems to

be a consistent pattern among different animal species, as

similar findings have been reported before (e.g. Benus et al.

1990, 1991; Marchetti and Drent 2000). It may be that the

tests were perceived as highly stressful by novelty avoiding

individuals, which has been found to decrease the corre-

spondence between personality and behaviour and to

increase the influence of random environmental factors on

behaviour (Zuckerman 2005; Cockrem 2007).

On the other hand, it is possible that novelty avoiding

individuals are more reactive and attentive to environ-

mental cues, and thus better able to adjust their behaviour

according to the current situation. Both poles of this

dimension would then have their pros and cons: novelty

seeking individuals most likely find and claim the best food

sources, mates and territories, but probably bear the cost of

low survival because of their risk taking behaviour and

poor adjustment to changing conditions. Additionally,

highly active and exploratory animals may experience a

higher parasitic load (Boyer et al. 2010). A meta-analysis

on animal personality studies revealed a survival cost of

boldness, counterbalanced by higher reproductive success

(Smith and Blumstein 2008). Hence, it is feasible to think

of novelty seeking and avoiding in the bank vole as dif-

ferent strategies maintained by equal total fitnesses in a

changing environment, as suggested by Sih et al. (2004),

Dingemanse and Re’ale (2005), Boon et al. (2007), Re’ale

et al. (2007) and Quinn et al. (2009).

Extroversion

Like novelty seeking, extroversion comprised behaviours

measured in different situations, indicating cross-situa-

tional stability. Highly dominant animals spent a lot of time

sniffing the pups and moving in the infanticide arena. The

relationship between dominance and mobility is a common

pattern in many different species, including humans

(reviewed in Gosling 2001), which indicates that this

relationship may have a deep evolutionary basis—whether

it is a constraint or an adaptation is still an open question.

In a study with mountain chickadees, Fox et al. (2009)

found that dominance was related to exploration of a novel

environment but not to novel object exploration. Explora-

tion of the environment may represent mobility, which

would also be evidence for a similar dominance–mobility

relationship in this species. Interestingly, the correlation in

the mountain chickadees was negative.

There has been some controversy as to whether domi-

nance can be considered a trait of an individual, or whether

it is merely a product of a specific relationship between two

individuals. In voles, dominance is related to physiological

traits of an individual (Kruczek 1997; Lopuch and Matula

2008) and is heritable (Horne and Ylonen 1998)—a clear

implication of a genetic basis for this trait. In addition,

dominance in this study was among the most repeatable

behaviours, although the opponent was changed between

tests. This strongly suggests that dominance is indeed a

stable trait of an individual and is not determined solely on

the basis of each new individual encountered. McGhee and

Travis (2010) recently came to the same conclusion in a

study on killifish.

The fitness consequences of both mobility and domi-

nance have been studied in voles, but only separately. Both

mobility and dominance increase the fitness of a male vole

(Horne and Ylonen 1996; Banks et al. 2002; Sundell et al.

2008). Dominance seems to be an honest signal of male

quality and condition in the bank vole (Horne and Ylonen

1998; Lopuch and Matula 2008). Maintaining dominance

status—the behaviours and the physiology it requires—is

energetically costly. A male has to be in prime condition to

reach high dominance rank and to maintain it (Gosling

et al. 2000; Lopuch and Radwan 2009). This was con-

firmed by the lower weight gain of dominant animals

compared to more submissive ones, a result also found by

Gosling et al. (2000) in male mice. As male dominance-

related traits are highly heritable in the bank vole (Horne

and Ylonen 1998) and indicate good condition, and as

females have been found to prefer good quality males

(Klemme et al. 2007; Lopuch and Radwan 2009), it seems

that females are attracted to good genetic quality reflected

in dominance status and the traits related to it. One can also

assume good physical condition as a prerequisite for high

mobility.

The correlation between dominance and mobility and

their condition-dependence means that the better survival

reported for mobile voles could be due to dominance or

better condition and not mobility per se. It is possible that

submissive voles are forced by the dominant ones to use

areas where predation risk is higher, or quite simply that

voles in good physical condition survive better than those

in poorer condition. This reflects the need to consider all

related behaviours when studying fitness consequences.

More research is warranted to find out how universal the

dominance–mobility relationship is, and whether the

74 Oecologia (2011) 165:67–77

123

common factor behind this correlation is indeed the phys-

ical condition of the individual.

While time spent in captivity increased extroversion,

population density had no clear effects on this trait. The

increase phase population did exhibit higher extroversion

values than both the peak and low phase populations, but

this can be explained by the longer captivity time of the

increase phase population.

The possible dependence of extroversion on condition

could explain why time spent in captivity correlates posi-

tively with it and why the laboratory colony and animals

from Konnevesi 2007 were the most extrovert groups. We

suggest high quality food, probably a lower parasitic load,

stable conditions and acclimation to strong social cues in

the laboratory environment as possible explanations for the

higher dominance and mobility of laboratory animals. This

implies a laboratory artefact on rodent behaviour, which

may confound the generality and ecological relevance of

experiments with laboratory animals. This needs to be

taken into consideration when discussing such results, as

suggested, e.g., by Ylonen (2001).

It has been suggested that mating with a dominant male

could be a defence against infanticide (Horne and Ylonen

1996), as dominant males have previously been found to be

more infanticidal than submissive ones, and infanticidal

behaviour is supposed to be inhibited in males at the time

of parturition (Vihervaara et al. 2010). However, contrary

to this theory, in our study dominance was not found to

correlate with infanticidal behaviour and had a very low

loading on the infanticide component. The extroversion

component was somewhat correlated with the infanticide

component, but this was because sniffing the pups loaded

highly on both. Nevertheless, this does not weaken the anti-

infanticide theory, because more dominant males are likely

to be better at defending their home range against intruding

infanticidal males and thus keeping their pups safe.

Infanticide

Aggressiveness towards pups is not usually tested as part of

personality research, but it has previously been found to be

a stable and heritable individual trait of rodents (Perrigo

et al. 1993). The infanticide component in this study cov-

ered all aspects of aggressive behaviour towards the pups

but nothing else, which made it a very straightforward

component to interpret and name. This means that infan-

ticidal behaviour can legitimately be studied as a separate

trait, independent of other behaviours. Infanticide was the

only personality trait clearly affected by population

density: high density populations were more infanticidal

than low density ones, suggesting infanticide as a means to

reduce competition. This result is investigated in greater

detail in Korpela et al. (2010).

Pooling the data from different populations could

potentially be problematic if different populations exhib-

ited different underlying personality structures, i.e. if dif-

ferent behaviours were correlated or altogether different

personality dimension existed in different populations. This

is unlikely, as personality structures have been shown to be

identical in different populations of various species ranging

from insects to mammals (e.g. McCrae et al. 2004; Lloyd

et al. 2008; Pruitt et al. 2010). It seems, then, that per-

sonality is a species-specific trait that only has quantitative

variation at the population level. Sufficient variation in

scores is necessary for a factor analytic method to produce

reliable results; with too small variation the correlations

may be deflated. As sample size in this study was not very

large, pooling data from different populations was con-

sidered beneficial as it is likely to increase variation

(Tabachnik and Fidell 2007).

Conclusions

Many aspects of bank vole behaviour are repeatable and

linked to other behavioural traits. A high proportion of

behavioural variation in this species can be explained by

three separate personality dimensions: novelty seeking,

extroversion and infanticide. Extroversion seems to reflect

general condition of the male vole, good condition

allowing for high mobility, dominance status, survival and

reproductive success. These behaviours should not be

treated separately as they share a common background.

The same is true for the behaviours that together form

novelty seeking: risk taking, exploration and consistency

in behaviour. This dimension has not previously been

studied in voles, but this study shows that it is an

important cause of individual behavioural variation, may

represent alternative life-history strategies in the bank

vole, and may have confounding effects if ignored. Pop-

ulation density influences infantidical behaviour, and

time spent in the laboratory increases extroversion.

Novelty seeking may represent an individually determined

strategy.

Acknowledgments We thank technicians of the Konnevesi

Research Station for help in maintenance and care of the experimental

animals. The experiment was conducted under permission by the

Board for Animal Experimentation at the University of Jyvaskyla, No.

25/20.6.2006.

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