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All content in this area was uploaded by Heiko G. Rödel on Dec 22, 2013
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Content uploaded by Heiko G. Rödel
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All content in this area was uploaded by Heiko G. Rödel on Dec 22, 2013
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ARTICLE
Lactation does not alter the long-term stability of individual
differences in behavior of laboratory mice on the elevated
plus maze
Heiko G. Ro
¨
del
•
Robyn Hudson
•
Lena Rammler
•
Nina Sa
¨
nger
•
Lisa Schwarz
•
Peter Machnik
Received: 14 October 2011 / Accepted: 22 November 2011 / Published online: 10 December 2011
Ó Japan Ethological Society and Springer 2011
Abstract Individual consistency over time in behavioral
responses to challenging situations is usually regarded as
an indication of the existence of animal personality types.
Although such consistency has been found in a variety of
species, information about long-term stability is scanty, in
particular across different life history stages, for example
reproductive and non-reproductive periods, which have the
potential to affect substantially the behavioral responses of
animals. In our study of adult female laboratory mice, we
explored the stability of behavioral responses across a
43-day period by successively testing the animals on an
elevated plus maze. We tested two groups, one group that
had offspring during the first two tests but not during the
last test, and another group that only had offspring during
the last test. We found clear evidence of individual con-
sistency over time by means of positive significant corre-
lations across the different tests: animals that spent more
time in the closed arms and those that entered the open
arms more often during the first test also tended to do so
during the second test—when still in the same reproductive
state, and also during the third test—when in a different
reproductive state. In addition, females of the two groups
did not differ overall in their responses, although we found
a significant increase in the frequency and duration of
presumed anxiety-related behavior during the course of the
experiment, contradicting the notion that habituation
effects should attenuate the challenge of the test situation.
In conclusion, our study strongly suggests the existence of
stable personality types in female laboratory mice, even
across different reproductive stages.
Keywords Animal personality Anxiety
Mus musculus Temperament Reproduction
Introduction
Interest has been growing recently in the study of consis-
tent individual differences in the behavior of animals, a
phenomenon that has been variously termed animal per-
sonality, temperament, behavioral style, behavioral syn-
drome, or coping style (Wilson et al. 1994; Koolhaas et al.
1999; Sih et al. 2004). An increasing number of studies of a
wide range of vertebrate and invertebrate species have
demonstrated the stability of such differences over long
time spans and in different contexts (Gosling and John
1999; Dingemanse et al. 2002; Bell 2007; Freeman and
Gosling 2010; Gracceva et al. 2011; Reyes-Meza et al.
2011;Ro
¨
del and Meyer 2011;Ro
¨
del and Monclu
´
s 2011;
Schuett et al. 2011), two factors that are generally regarded
as requirements for the existence of animal personality
(Bell 2007; Bergmu
¨
ller 2010; Uher 2011). Nevertheless, in
addition to the study of consistency across time and con-
text, there is also a need for information about temporal
H. G. Ro
¨
del (&)
Laboratoire d’Ethologie Expe
´
rimentale et Compare
´
e
E.A. 4443 (LEEC), Universite
´
Paris 13, Sorbonne Paris Cite
´
,
93430 Villetaneuse, France
e-mail: heiko.rodel@leec.univ-paris13.fr
H. G. Ro
¨
del L. Rammler N. Sa
¨
nger L. Schwarz
P. Machnik (&)
Department of Animal Physiology, University of Bayreuth,
Universita
¨
tsstraße 30, 95447 Bayreuth, Germany
e-mail: Peter.Machnik@uni-bayreuth.de
R. Hudson (&)
Instituto de Investigaciones Biome
´
dicas, Universidad Nacional
Auto
´
noma de Me
´
xico, Distrito Federal, Mexico
e-mail: rhudson@biomedicas.unam.mx
123
J Ethol (2012) 30:263–270
DOI 10.1007/s10164-011-0320-y
consistency in individual differences during different
stages in the life history of an individual. Without doubt,
reproduction is one of the most prominent aspects of the
life of an adult animal, accompanied by marked changes in
its physiological and emotional state. Importantly, it is
widely accepted that mammalian females are hypo-
responsive to stressors during lactation (Lightmann et al.
2001), leading to decreased fear and anxiety and to
increased maternal aggressiveness (Ostermeier 1983;Ha
˚
rd
and Hansen 1985; Maestripieri and D’Amato 1991).
Defense of offspring against infanticidal intruders is
thought to be the main function of this (Parmigiani et al.
1988;Ro
¨
del et al. 2008). Thus, changes in emotionality
associated with animals’ reproductive stage might have the
potential to alter the consistency of a female’s behavioral
responses over long time periods, including different
reproductive stages. Typically, such changes can affect the
temporal consistency of the average score of a behavior
expressed by a group of animals tested in a given context
(mean-level consistency; Stamps and Groothuis 2010), as
has been described for great tits (Parus major) across age
or across different life history stages (Dingemanse et al.
2002; Carere et al. 2005).
Considering that the laboratory mouse (Mus musculus)
is now one of the most commonly used mammals in
behavioral and biomedical research, it was our objective in
this study to investigate the stability of individual differ-
ences in behavioral responses of females of this species
tested over an appreciable time span and when in different
reproductive states. Generally, it has recently been reported
that laboratory mice are also consistent over time in their
responses in standardized test situations, pointing towards
the existence of distinct personality types (Lewejohann
et al. 2011). We chose RjHan:NMRI mice, because these
are frequently used in behavioral studies in biomedicine
and psychopharmacology, and we chose to investigate
animals’ responses when tested on the elevated plus maze,
a standardized and commonly used test of anxiety in
laboratory rats and mice (Archer 1973; Pellow et al. 1985;
Komada et al. 2008).
We asked whether stable individual differences in
response would be observed for females on the elevated
plus maze across an appreciable time span, and also across
different reproductive states. For this, we first evaluated
the temporal consistency of lactating and non-lactating
females’ behavioral responses over a short time period of
2 days, and in particular whether these two groups of
females would be distinguishable in their overall responses.
We then tested for temporal consistencies over a longer
time period of more than 40 days, and which included
changes in the females’ reproductive state.
Methods
Animals and housing conditions
We used 23 female RjHan:NMRI mice (on average
91.5 ± 0.9 SD days old at the start of the study) obtained
from Janvier Laboratories (Le Genest-Saint-Isle, France).
Females were kept individually in standard polycarbonate
cages (26 cm 9 42 cm 9 15 cm; Macro 2808 type III;
Ehret, Germany) containing wood shavings as bedding. For
mating, only, they were housed with a stud male of the
same strain (for 7 days). Animals had ad libitum access to
mouse standard diet (Rat & Mouse Pro; Versele-Laga,
Belgium) and water, and were kept on a 12:12-h light/dark
cycle (lights off at 19:00 hours). Temperature was main-
tained at 21°C(±0.5 SD) and relative humidity at
approximately 50%. Animals were transferred to clean
cages once a week. Cages were checked daily for the
presence of litters, and the day of birth was regarded as
postnatal day 0. Mothers and litters were left undisturbed
until the mothers’ first test trial on postpartum day 6
(Fig. 1). Mean litter size was 15.9 ± 1.8 SD, and litters
were euthanized shortly after the trials on postnatal day 8.
without offspring without offspring with offspring
with offspring with offspring without offspring
time
T
1
n = 14 n = 14 n = 14
n = 7
n = 9n = 9
b
a
T
2
T
3
Fig. 1 Experimental design. Repeated measurements conducted with
two groups (a, b) of same-age adult female laboratory mice. Subjects
underwent three consecutive tests on an elevated plus maze during
different reproductive states. Females with offspring were tested on
postpartum day 6 (T
1
, T
3
) and on postpartum day 8 (T
2
); note that
days after the onset of the experiment are given in the figure. Females
were not pregnant when tested
264 J Ethol (2012) 30:263–270
123
Experimental design, sample sizes and behavioral
testing
At the start of the study we randomly divided the females
into two treatment groups, those mated and first tested as
mothers of young litters and later as non-mothers, and
those housed alone and first tested as non-mothers and then
mated and tested as mothers of young litters (Fig. 1).
Fourteen females formed the first group, and nine formed
the second group, although, because of failure to become
pregnant, only seven of these completed all three trials
(Fig. 1). Except for these two females, animals were given
three trials spread over 43 days (Fig. 1) on an elevated plus
maze. During the first two trials, which were conducted
within 2 days, the animals of the two groups were in the
same reproductive state, whereas the reproductive state of
the individual females changed between the first/second
trial and the third trial, representing a change in repro-
ductive history. These changes were reversed for the two
groups (Fig. 1a, b).
The elevated plus maze was made of PVC for easy
cleaning with isopropyl alcohol and water between trials. It
consisted of four arms 10 cm wide and 50 cm long,
arranged at 90° angles, and mounted 80 cm above the floor.
Two opposite arms enclosed by 40-cm high walls and two
open arms without walls were connected by a 10 9 10 cm
central platform. We tested in the light phase (between
08:00 and 10:00 hours). The luminance measured on the
surface of the plus maze was 20 cd/m
2
in the closed arms
and 70 cd/m
2
in the open arms of the plus maze. Each
female was placed on the central platform facing an open
arm and its behavior was recorded for 5 min by use of a
video camera mounted 120 cm above the center of the
maze. We scored two types of behavior: the percentage of
time an animal spent in the closed arms and the number of
times it entered the open arms, both defined as crossing the
respective thresholds with all four feet. Animals were kept
and treated according to the institutional guidelines of the
University of Bayreuth, Germany, where the experiments
were conducted.
Statistical analysis
Each video was analyzed by one of three persons unaware
of the experimental design. Videos from the different
experimental stages and from the different animals were
analyzed in a random order.
We used multivariate statistical models for analyzing
the data; the software R version 2.13.0 (R Development
Core Team 2011) was used for all statistical analysis. The
principal objective was to test for correlations of the two
different behavioral variables (% time in closed arms;
N entries to open arms) across time. Therefore, we first
correlated the behavioral responses measured during
experimental stages T
1
(predictor variable) and T
2
(response variable), and then tested for correlations between
the behavior measured at T
1
(predictor variable) and T
3
(response variable). We always included the reproductive
state/history of the animals (Fig. 3) in the statistical models
as an additional factor. In the case of correlations between
T
1
and T
2
, the females of the two groups were in different
reproductive stages, i.e. they either had offspring or did not
(factor with 2 levels). In the case of correlations between T
1
and T
3
, the two groups of females had a different repro-
ductive history, i.e. females either had offspring during the
first test and then no longer during the second or vice versa
(factor with 2 levels). We also checked for the interactions
of T
1
and the females’ reproductive state (Table 1a, c) or
reproductive history (Table 1b, d), in order to determine
whether the correlations between the different experimental
stages differed or specifically occurred in one group of
females only. However, these interactions were never sig-
nificant (Table 1), and thus the statistical models were
recalculated after omitting the interaction term. As a con-
sequence, and because the main effects of reproductive state
or history were also never significant (Table 1), the data for
the two groups of females were pooled and only one
regression line was calculated for each statistical model
(Fig. 3).
The data presented in Fig. 2 were analyzed with mixed
effects models including the individuality of the animals as
a random factor and thus allowing for repeated measure-
ments. Also here, we calculated the interactions between
the experimental stages (factor with three levels) and the
reproductive stage/history of the females. As the interac-
tions were again never significant, they were omitted from
the models and these were re-calculated. Mixed effects
models were calculated using the R-package lme4 (Bates
et al. 2011), and P values were extracted by likelihood ratio
tests (Faraway 2006).
The percentage time that the two groups of animals
spent in the closed arms was analyzed with linear mixed
models (data plotted in Fig. 2a, b) or linear models (data
plotted in Fig. 3a, b). We ensured the model residuals
approximated a normal distribution by checking normal
probability plots and by using the Shapiro–Wilk test. The
number of entries into the open arms was analyzed with
generalized linear models (data plotted in Fig. 2c, d) or
general linear mixed models (data plotted in Fig. 3c, d) for
Poisson-distributed data using a log-link function. For
all models, we checked for homogeneity of variances
by plotting the model residuals versus fitted values
(Faraway 2006). For the Poisson regressions (as shown in
Fig. 3c, d) we calculated Nagelkerke’s pseudo-R
2
to assess
the explained variance of the significant correlations
(Nagelkerke 1991).
J Ethol (2012) 30:263–270 265
123
Results
Anxiety-related behavior of females during successive
tests
The percentage time that the animals spent in the closed
arms of the elevated plus maze increased (within subjects:
v
2
2
= 40.57, P \0.001; Fig. 2a, b) and the number of
entries into the open arms decreased (within subjects:
v
2
2
= 45.37, P \ 0.001; Fig. 2c, d) across the three con-
secutive experimental stages. Post-hoc comparisons with
regard to both response variables indicated significant
differences (increase: Fig. 2a, b; decrease: Fig. 2c, d)
between T
1
and T
2
and between T
1
and T
3
; P \0.001 in all
cases), but not between T
2
and T
3
(P [ 0.10). There were,
however, no general differences among individual females
in different reproductive states (P [ 0.10), and also no
specific differences between the two groups of females
during the different stages of the experiment—as indicated
by the non-significant interaction terms (group 9 experi-
mental stage: P [ 0.10), either with regard to the per-
centage time spent in the closed arms or to the number of
entries into the open arms.
Consistency across time
The time that individual females spent in the closed arms
and the number of entries into the open arms were signif-
icantly correlated across time (Fig. 3). There were signifi-
cant positive correlations between the responses during the
first and second tests, when individual females of the two
groups were in the same reproductive state (Table 1a, c;
Fig. 3a, c), and there were also positive, although weaker,
correlations between the first and the third period of the
experiment, i.e. across two periods when the reproductive
state within the two groups of females had changed
(Table 1b, d; Fig. 3b, d).
As shown above, the results indicate that there were no
general differences in this anxiety-related behavior
between the females of the two groups; that is, the corre-
lations of the two groups did not differ in the intercepts, as
indicated by the non-significant effects of reproductive
state (Table 1). In addition, there were no differences in
slopes, as indicated by the non-significant interaction terms
(Table 1a, b), and thus the four correlations were best
explained by single regression lines for the two groups of
females (Fig. 3a–d).
Discussion
Overall, individual behavioral responses of female mice in
a standardized test considered to test fearfulness were
markedly different. We found correlational evidence for
short-term temporal consistency across individuals (dif-
ferential consistency: Stamps and Groothuis 2010) for
animals in the same reproductive state. The repeatability
was quite high, with explained variances of 33 and 50%
(values of R
2
in Fig. 3a, c, respectively). In addition, the
two measures of anxiety-related behavior used here were
also indicative of high long-term temporal consistency over
the 43-day experimental period, an appreciable time span
in the life of an adult mouse. Here, the repeatability was
moderate with explained variances of 22 and 43% (Fig. 3b, d).
Table 1 Consistency across time
Response variable Predictor variables F/v
2
df P
(a) T
2
time spent in closed arms T
1
time spent in closed arms 10.31 1,21 0.004
Reproductive state 1.32 1,20 0.26
Interaction 0.83 1,19 0.37
(b) T
3
time spent in closed arms T
1
time spent in closed arms 5.43 1,19 0.031
Reproductive history 3.50 1,18 0.078
Interaction 0.95 1,17 0.34
(c) T
2
entries into open arms T
1
entries into open arms 15.89 1,21 \0.001
Reproductive state \0.01 1,20 0.98
Interaction 1.53 1,19 0.22
(d) T
3
entries into open arms T
1
entries into open arms 12.72 1,19 \0.001
Reproductive history 0.35 1,18 0.56
Interaction 0.05 1,17 0.82
Multivariate models on the correlations between the percentage time that female laboratory mice spent in the closed arms of an elevated plus
maze (a, b: calculated with linear models) and between the numbers of entries into the open arms (c, d: calculated with generalized linear models
for Poisson-distributed data) during three consecutive tests. In addition, the effects of the animals’ reproductive state/history were tested (Fig. 1).
Statistics were calculated using a backward elimination of non-significant predictor variables and interaction terms
266 J Ethol (2012) 30:263–270
123
Most importantly, the changes in reproductive state (from
non-lactating to lactating in one group and vice versa in the
other) did not nullify this consistency.
Our results are therefore, on the one hand, consistent
with the proposition that mice show stable individual dif-
ferences in anxiety-related behavior, commonly used as
indicators of animal personality (Lewejohann et al. 2011).
On the other hand, our failure to find a general effect on
fearfulness of the females’ reproductive state or of their
reproductive history was surprising. Overall, females were
no less fearful when they had young, and, irrespective of
their reproductive state, in relation to the sequence of
conditions in which they were tested. This was the case
even though we tested mothers early postpartum when
changes in the physiological and emotional state of a
female are thought to be particularly strong (Ostermeier
1983). Although this finding contrasts with a number of
reports of reduced fearfulness of lactating rats and mice
(Fleming and Luebke 1981;Ha
˚
rd and Hansen 1985;
Ferreira et al. 1989; Maestripieri and D’Amato 1991), it is
consistent with other reports failing to find such an effect
(Lonstein 2005). Various explanations for this inconsis-
tency have been suggested: possible bias because of
elimination of ‘‘non-responders’’ from study samples
(Maestripieri and D’Amato 1991); that different behavioral
tests measure different aspects of anxiety; that females’
levels of fearfulness vary during different stages of lacta-
tion; strain differences; and whether or not mothers had
recently had contact with their young before testing
(Lonstein 2005).
Fig. 2 Differences in the
responses over time.
Comparison of the percentage
time that female laboratory
mice spent in the closed arms of
an elevated plus maze (a, b) and
between the numbers of entries
into the open arms (c, d) during
three consecutive tests. Data
(repeated measurements) are
shown separately for the two
sets of females with different
consecutive reproductive stages:
grey boxes indicate that the
females had offspring whereas
white boxes indicate that
females did not have offspring
during the respective trials. See
text for statistics; sample sizes
are given in the graph
J Ethol (2012) 30:263–270 267
123
For animals of both groups an increase in fearfulness
was actually observed from the first compared with the
subsequent two trials, expressed as an increase in the time
spent on the closed arms and a decrease in the number of
entries into the open arms (Fig. 2). This is in contrast with
the assumption that the animals might habituate to the
maze, i.e. show an overall reduction in fearfulness as a
result of increasing familiarity with the test situation across
the three trials (Calvo-Torrent et al. 1999). However, such
an increase in anxiety-related behavior in successive plus-
maze tests seems to be not unusual and similar results have
been reported previously (File et al. 1993; McIlwain et al.
2001;Vo
˜
ikar et al. 2003; Lewejohann et al. 2011). Possi-
bly, in the first trial, motivation to explore the novel situ-
ation presented by the maze counteracted to some extent
the more fearful response (or reduced curiosity) seen in
later trials after the animals had learned the configuration
of the maze and their various response options. Alterna-
tively, it might be assumed that the better illumination of
the surface of the open arms (70 cd/m
2
) than of the closed
arms (20 cd/m
2
) might have led to an increased aversion to
the former parts of the elevated plus maze across the dif-
ferent trials (Miller et al. 2011). Nevertheless, important for
the purpose of our study, these changes in the absolute
levels in the animals’ behavioral responses over time tested
on an individual basis were again decoupled from the
females’ initial reproductive stage along T
1
and T
2
, and
from the changes in the females’ reproductive state along
T
2
and T
3
(Figs. 1, 2).
Overall, the findings of this study add to the growing
evidence of individual differences among conspecifics in
behavior that can be considered to reflect an animal’s
personality by demonstrating that individual differences in
the fearfulness (or curiosity) of female mice persist across
time and physiological (reproductive) state. This then rai-
ses questions about the origin of such differences, partic-
ularly during development (Stamps and Groothuis 2010;
Trillmich and Groothuis 2011; Trillmich and Hudson
2011). This is important, given the efforts made in
behavioral and biomedical research to reduce or ideally to
eliminate such differences by using inbred stains or clones,
and by raising and maintaining animals under highly con-
trolled, standardized conditions. These results (although
conducted with an outbred strain) provide support for a
growing understanding that eliminating such variance is
not possible, and for the proposition that stable individual
Fig. 3 Consistency across time.
Significant correlations between
the time spent in the closed
arms and between the number of
entries into the open arms of the
elevated plus maze during the
first test T
1
and (a, c) the second
test T
2
, conducted 2 days later
and (b, d) the third test T
3
,
conducted 43 days later. Data
from the females of
experimental group A are given
by filled circles, and data from
females of group B are given by
open circles (Fig. 1). The
explained variations (R
2
for
linear regressions and R
Nagelkerke
2
for Poisson regressions) are
given in the graphs; details of
the statistics are given in
Table 1. Note the differences in
the scaling of the y-axes
268 J Ethol (2012) 30:263–270
123
differences in behavior (and so in underlying physiology)
are an inherent part of animal populations (Wu
¨
rbel 2000;
Macrı
`
and Wu
¨
rbel 2006; Hudson et al. 2011; Lewejohann
et al. 2011; Schuett et al. 2011). It is now widely accepted
that variation in animal personality and the maintenance of
this within populations is because of fitness trade-offs (Dall
et al. 2004;Re
´
ale 2007; Wolf et al. 2007). Accordingly, it
would be useful to investigate the consequences for
reproductive fitness in maternal mice with indicators of
different personality types of the kind found here (Biro and
Stamps 2008; Boon et al. 2008; Smith and Blumstein
2008).
Acknowledgments We thank Stefan Schuster, Wolfram Schulze,
and Hans Distel for stimulating discussions, Carolina Rojas for bib-
liographical assistance, and Karl-Heinz Po
¨
hner and Achim Schmidt
for excellent animal care. Financial support to RH was provided by
the Mexican funding agencies CONACYT (48692-Q) and PAPIIT
(IN223910).
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