Behavioral Ecology
doi:10.1093/beheco/ars175
Advance Access publication 5 November 2012
Original Article
Insect personality depends on environmental
conditions
Martin Tremmel and Caroline Müller
Department of Chemical Ecology, Bielefeld University, Universitätsstraße 25, D-33615 Bielefeld,
Germany
Increasing evidence has accumulated within the last decade that individuals of different animal species show consistent behavior both across various contexts and through time, that is, they do have personality. However, little is known in how far the
environment an individual is facing may influence the personality of insects, whereas it is well established that the environment
can have profound influences on performance parameters. The development of personality may be closely linked to different
expectations in future fitness leading to contrasting life-history strategies. We investigated in how far the environmental food
conditions experienced during lifetime influence the life-history and shape the personality of the mustard leaf beetle, Phaedon
cochleariae, a pest of crucifers. Beetles reared on low-quality food developed slower and gained lower body masses than insects
reared on high-quality food. By performing behavioral tests analogous to vertebrate assays repeatedly during adult life, we identified 3 personality dimensions, boldness, activity, and nontargeted explorativeness. Comparing food-dependent differences of
the personality dimensions with state-dependent differences of the expected future prospects, we found that beetles feeding
low-quality food were bolder, thereby potentially increasing their capabilities to succeed in foraging. In contrast, animals feeding high-quality food were more active. Changes in boldness may be highly adaptive to increase future reproductive output,
whereas activity is likely constrained by the energy uptake. Our results demonstrate that the environment does not only affect
life-history traits but has also a consistent impact on an individual’s behavior, which is likely highly adaptive. Key words: animal
personality, behavioral phenotype, life-history, mustard leaf beetle, performance.[Behav Ecol]
Introduction
T
he particular environment of an animal can have profound influences on its life-history traits, such as body
size, generation time, and fertility (Lindström 1999; Awmack
and Leather 2002; Relyea and Hoverman 2003; Martel et al.
2011). Moreover, the experience with a specific environment
will also affect the behavior of an individual. For example, the
natal environment can trigger habitat choice, nearly always
increasing the acceptance for these habitats (Davis 2008).
Likewise, food plant experience during larval stages can lead
to preferences for the familiar food in adults of various herbivorous insect species (Barron 2001). Starvation was shown
to increase the death-feigning duration of the beetle Cylas formicarius (Coleoptera: Brentidae) (Miyatake 2001). However,
in how far the environmental conditions experienced during lifetime affect different behavioral variables consistently
across contexts and time, that is, the personality of an animal (Gosling 2001), and especially whether this can be interpreted as adaptive plasticity are currently little understood.
A recent study indicates that the social environment during
pregnancy and lactation affects the behavioral infantilization
in offspring of wild cavies (Cavia aperea, Hystricomorpha:
Caviidae), adjusting these animals to environmental conditions (Siegeler et al. 2011).
Several theoretical models highlight the adaptive values of
the emergence of personality and hypothesize that its function
Address correspondence to Caroline Müller. E-mail: [email protected]
Received 28 April 2012; revised 7 August 2012; accepted 4
September 2012
© The Author 2012. Published by Oxford University Press on behalf
of the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
can be explained with life-history trade-offs (Rands et al.
2003; McElreath and Strimling 2006; Stamps 2007; Wolf et al.
2007). Different personalities may be generated by rule-based
foraging decisions (Rands et al. 2003), differences in growth
rates (Stamps 2007), or imperfect information about ambient conditions combined with differences in individual states,
which can lead to stable variation between the responses of
individuals to environmental cues (McElreath and Strimling
2006). In particular, trade-offs between present and future
reproduction may lead to populations in which some individuals invest more into future reproduction than others (Wolf
et al. 2007). This assumption is based on the asset-protection
principle that predicts that the better the current condition
of an animal is the more cautious it should behave to protect its state. Thus, individuals with higher future prospects
should be less risk-prone than individuals with lower expectations (Clark 1994). Thereby, the shyness–boldness continuum
describes one of the major dimensions of personality, namely
the propensity to take risks (Réale et al. 2007).
In insects, consistent differences in a few behavioral traits
related to boldness and exploration were found between
females of short-winged and long-winged morphs of
firebugs, Pyrrhocoris apterus (Heteroptera: Pyrrhochoridae),
which persisted at least for 5 days (Gyuris et al. 2011).
Dropping behavior, a typical escape response of aphids
to predator attacks, was likewise shown to be consistent
over the same period in the pea aphid, Acyrthosiphon pisum
(Hemiptera: Aphididae) (Schuett et al. 2011). However, in
these sparse examples of personality of nonsocial insects,
only few behavioral traits were investigated. Furthermore,
personality was not tested in dependence of the influence of
environmental conditions.
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Tremmel and Müller • Environmental impact on personality
To investigate in how far the environment may shape not
only the performance parameters but also the personality of an insect, we carried out various behavioral tests with
the mustard leaf beetle, Phaedon cochleariae (F.) (Coleoptera:
Chrysomelidae). This species is a specialist on several species of Brassicaceae and can be a pest on crops of this family (Finch and Kienegger 1997). Earlier studies have shown
that growth and fertility of these beetles are impacted by the
food quality (Reifenrath and Müller 2009; Kühnle and Müller
2011). To analyze potential food-dependent differences in
personality, we performed a battery of 5 behavioral test setups derived from research on vertebrate behavior (Prut and
Belzung 2003; Ardayfio and Kim 2006). Our tests comprised
9 behavioral variables that were measured thrice during adult
life in individuals reared on either high or low food quality. We predicted that animals experiencing low food quality
should gain less body mass due to reduced energy availability
and consequently have lower expectations of future reproduction compared with animals experiencing high food quality (Reifenrath and Müller 2009; Kühnle and Müller 2011).
Furthermore, adult beetles feeding on low-quality diet should
have a generally bolder personality as their future prospectives are low and as these individuals have less to lose (Clark
1994; Wolf et al. 2007).
Methods
Insect and plant rearing
Cabbage plants (Brassica rapa L. ssp. pekinensis “Michihili”,
Brassicaceae) and Tropaeolum majus L. (Tropaeolaceae)
were reared in a greenhouse at 20 °C and a photoperiod
of L16:D8 h. Seeds were obtained from Kiepenkerl (Bruno
Nebelung GmbH, Konken, Germany) and grown in composted soil (plant nursery, Bielefeld University) in pots (diameter: 12 cm). Cabbage plants used for larval rearing and
bioassays were 7–10 weeks old and nonflowering. Plants of
T. majus used for extracts were about 8 weeks old and flowering. Mustard leaf beetles had been collected in the field in
Germany and were subsequently reared in a climate chamber
(20 °C, 70% r.h., L16:D8 h) for several generations on B. rapa
leaves, with at least 700 beetles per generation distributed
over 4 rearing boxes (200 × 200 × 65 cm) and mixed randomly
for mating. Larvae were collected randomly from all rearing boxes at the day of hatching and used for the following
experiments.
Measurements of food-quality-related effects on
performance parameters
We weighed neonate larvae and transferred them individually in Petri dishes closed by a cup (diameter: 4.5 cm, height:
5.0 cm) to survey their performance parameters, namely
developmental time and adult body mass. Larvae were fed ad
libitum with cabbage leaf discs (diameter: 2.5 cm) of different
quality. High-quality food consisted of fully developed, young
cabbage leaves treated with 20 µL hexane per disc. Lowquality food consisted of the outer old cabbage leaves, which
were treated with 20 µL of a hexane extract of lyophilized
and homogenized leaves and stems of T. majus, because this
extract is known to impair larval feeding negatively (Kühnle
and Müller 2009). The extract concentration equaled the corresponding leaf-disc amount. Before offering the leaf discs
to the beetles, the solvent was allowed to evaporate. For each
food quality, initially 45 individuals were set up. Adult beetles
were weighed at the day of eclosion, and duration of developmental time was noted. Pairs of male and female beetles
of identical food experience were randomly assembled and
supplied in Petri dishes with leaf discs of the same quality
they had experienced as larvae.
Behavioral tests
Three to four weeks after adult eclosion, we performed a
battery of 5 test setups (contexts), comprising 9 behavioral
variables, with each individual (N = 48) and repeated this
battery totally thrice in a weekly interval (between day 27 and
day 44 of adult life). At first, we placed a beetle in an open field
(Petri dish, diameter: 8.8 cm) and recorded its movements
using a webcam (LifeCam VX-2000, Microsoft, Washington,
USA) for 1 h to investigate its behavior in a “motion” context.
Such open-field tests were originally developed to determine
the locomotor activity levels, exploration willingness, and
anxiety of vertebrates (Denenberg 1969; Prut and Belzung
2003). Motion detector software (CamAlert 2.9.23, Max
Christian Pohle) screened for movements once per second,
and whenever movement was detected a picture was taken.
Conversion software (PowerBatch 6.1.2.2, UniDream
Marketing Technologies Inc) was used to convert the pictures
taken into a video file. Using Bug Tracer Program (Version C,
Robert Winkler, based on a MATLAB motion detection script
by Lokesh Peddireddi), we reconstructed the path of the
beetle to derive 1) the distance a beetle covered (referred
to as covered distance hereafter), 2) the relative amount of
movements, 3) the number of turning angles <90°, 4) the variance
of turning angles, and 5) the relative amount of movements
in the inner area of a Petri dish (inner area movements) within
1 h. Afterwards, the beetle was offered food for half an hour
before the following tests were carried out subsequently.
Second, a dark-light test was performed to investigate the
behavior in a “hiding” context, usually used for measuring
anxiety-related behavior in mice (Ardayfio and Kim 2006).
Therefore, we placed the beetle in a semitransparent brown
glass vial (length: 6 cm, diameter: 1.9 cm). After 1 min of
acclimatization, the vial was shortly flicked to force the beetle
to the bottom of the vial, and the vial was laid down. Then,
the time the beetle needed to 6) emergence from a refuge was
measured once it had started to move, which should indicate
its position on a shy–bold continuum. The time was stopped
when the head was completely protruded from the vial
or after a maximum of 5 min. Third, we placed the beetle
into the center of an open-field arena (diameter: 17.2 cm)
surrounded by a wall (height: 0.8 cm). When the beetle
started walking, the time that the beetle needed to 7) reach
the wall (wall time) was measured to investigate its behavior
in an “unprotected environment” context. Fourth, the beetle
was placed in the center of an arena (diameter: 17.2 cm),
which contained 4 red rubber plugs (height: 0.7 cm, diameter:
1.2 cm) as novel objects placed about 3.5 cm away from the
wall and in equidistance of about 7 cm in the open arena in
a “foraging” context. The 8) number of novel objects visited by
a beetle within 5 min was counted. Fifth, we measured the 9)
duration of death-feigning behavior (thanatosis) in a simulated
“predator response” context by gently squeezing a beetle
shortly with forceps and measuring the time until it started to
move again. Because beetles habituated to mechanical stimuli
during experiments, death-feigning behavior was measured
3 days after the other 4 tests. After every third trial, material
for behavioral tests was wiped with 70% ethanol to remove
residual beetle traces.
Statistical analyses
We used Bartlett’s test and Shapiro–Wilk test to test for variance homogeneity and normal distribution of data, respectively.
To investigate the influence of food quality on duration until
388
Behavioral Ecology
eclosion and adult body mass, data were analyzed with a multivariate analysis of covariance (MANCOVA), whereby developmental time and adult body mass were used as response variables,
and food quality (high, low), sex (male, female), and initial larval body mass as explanatory variables. Nonsignificant variables
were removed using the Akaike information criterion to find the
minimal adequate model. Univariate ANCOVAs (type II) were
used as post hoc tests to reveal the influence of food quality and
sex on developmental time and adult body mass.
To investigate whether adults are ranked similarly across all
9 tested behavioral variables, Kendall’s W coefficient of concordance was calculated (Legendre 2005) for the behavioral
ranks of the first test battery series for all individuals regardless of food-quality experience. Kendall’s W coefficient of concordance was also calculated to test for consistency of behavior
over time, comparing the ranks for each individual behavioral
test variable. To find possible associations among the tested
variables and thus identify personality dimensions, we performed an agglomerative cluster analysis (Gyuris et al. 2011),
using “agnes” function with Ward’s clustering method in the
R-package irr. Therefore, 1 minus the absolute values of coefficients of a Kendall’s tau rank correlation matrix (Table S1)
calculated from the first test battery series were used as dissimilarity values. The number of groups (=personality dimensions)
was identified with a Silhouette plot (Maechler et al. 2011)
using the R-package cluster. Kendall’s W coefficient of concordance was calculated again within each personality dimension
to test for consistency across variables, using the behavioral
responses of the first test battery, as well as to test for consistency over time, using the composite variables (see below) for
each personality dimension from all 3 replicate test batteries.
To test for significant influences of food quality and sex
of animals on these personality dimensions, we calculated a
composite rank variable by adding the ranks of each behavioral variable within a personality dimension for each beetle.
The 3 respective composite variables were used as response
variables, and food quality (high, low) and sex (male, female)
of beetles as explanatory variables in a mutivariate analysis of
variance (MANOVA). As sex and the interactions of variables
did not significantly influence the overall personality in the
minimal adequate model, these variables were not taken into
account for the following univariate ANOVAs (type II), which
were performed to investigate the influence of food quality
on each individual personality dimension. To account for
multiple testing, all P-values within a test series were adjusted
using false discovery rate (Benjamini and Hochberg 1995).
All analyses were conducted with the program R 2.10.1 (R
Development Core Team, http://www.R-project.org).
Results
Effects of food quality on performance parameters
Plant quality significantly influenced performance parameters of animals that were either reared from larval hatching onwards on high-quality food (i.e., young cabbage leaves
treated with hexane) or low-quality food (old cabbage leaves
treated with T. majus hexane extract) (MANCOVA, Table 1).
The developmental time from the neonate larva until eclosion of the adult was about 10% shorter in insects reared on
high-quality food compared with insects that consumed lowquality food, whereas adult body mass was on average about
24% higher (ANCOVA; Table 1, Figure 1a,1b). There was no
difference in developmental time between sexes, but females
gained significantly higher biomass than males (Table 1).
Effects of food quality on insect behavior
In a battery of 5 behavioral test setups (contexts), comprising
9 behavioral variables, the behavior of adult beetles was
consistent across all tested variables, indicated by the highly
significant correlation of ranks (Table 2). When repeating
the tests in total thrice in a weekly distance during day 27
and day 44 of adulthood, beetles also behaved consistently
in 8 of 9 tested variables through time, with the number of
novel objects being the only nonconsistent variable (Table 2).
Tested behavioral variables could be divided into 3 groups in
an agglomerative cluster analysis (Figure 2) and a Silhouette
plot. The first group consisted of the variables inner area
movements, novel objects, wall time, emergence from a refuge, and
death-feigning behavior (here defined as personality dimension
“boldness,” in accordance with the majority of variables), thus
Table 1 Influence of food quality on the performance of leaf beetles
MANCOVA results on complete model
Performance
Quality
Sex
Residuals
Df
Wilks lambda
Approx F
num Df
den Df
P-value
1
1
65
0.431
0.665
42.252
16.093
2
2
64
64
<0.001
<0.001
Sum Sq
Df
F-value
P-value
32.245
26.440
55.289
1
1
65
37.909
31.084
<0.001
<0.001
70.849
0.538
109.641
1
1
65
42.002
0.319
<0.001
0.574
ANCOVA results on single performance parameters
Body mass
Quality
Sex
Residuals
Develop. timea
Quality
Sex
Residuals
The influence of food quality on performance was analyzed with a MANCOVA using developmental (develop.) time and adult body mass as response,
and food quality, sex, and initial larval body mass as explanatory variables. Nonsignificant variables were removed to obtain the minimal adequate
model. Univariate ANCOVAs were used as post hoc tests to reveal the influence of food quality and sex on adult body mass and developmental time.
a:Bartlett-test: P-value < 0.01.
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Tremmel and Müller • Environmental impact on personality
Table 2 Consistency of behavior across contexts and over time in the mustard
leaf beetle
Behavioral trait
Figure 1 (a) Developmental time and (b) adult body mass of mustard leaf
beetles reared on either high (N = 41) or low food quality (N = 27).
At the day of adult eclosion, duration of developmental time
was noted, and adult beetles were weighed. Data were analyzed
by MANCOVA with developmental time and adult body mass as
response variables, and food quality (high, low), sex (male, female),
and initial larval body mass as explanatory variables. Boxplots show
the median, quartiles, and maximum and minimum values of each
data set. Asterisks denote significant differences (***: P < 0.001; for
statistical details see Table 1).
comprising behavioral variables that were tested in 5 different
contexts. The second personality dimension grouped the
variables covered distance and amount of movements (summed as
“activity”), whereas the third dimension combined the number
of turning angles <90° and variance of turning angles (termed
“nontargeted explorativeness”). Within these 3 dimensions,
the variables also correlated significantly among each other,
and the composite variables (sum of the ranks of each
behavioral variable response within a personality dimension
for each beetle) correlated significantly over time, indicating
the high consistency and repeatability of each group of
variables (Table 2).
The food experience significantly affected the composite rank variables within 2 of these personality dimensions (MANOVA; Table 3). Beetles feeding on low-quality
diet were significantly bolder but also less active than animals feeding on high-quality diet (Table 3, Figure 3a,3b),
whereas sex had no significant effect. With regard to nontargeted explorativeness, there were no significant differences between beetles feeding on high- or low-quality diet
(Table 3, Figure 3c).
Discussion
Food quality had a pronounced influence on life-history traits
of the mustard leaf beetle, in accordance with earlier studies on this herbivore species (Reifenrath and Müller 2009;
Kühnle and Müller 2011). Individuals reared on low-quality
diet had a longer developmental time and weighed less
than insects reared on high-quality diet (Table 1, Figure 1).
However, the food quality did not only affect performance
parameters but also the personality of the individuals. The
adults feeding low-quality diet were consistently bolder but
less active than adults feeding high-quality diet, whereas nontargeted explorativeness was independent of diet experience
(Table 3, Figure 3). Moreover, our results demonstrate that
adult herbivorous insect personalities, which are shaped by
Across contexts
All 9 behavioural variables
5 variables for boldness
2 variables for activity
2 variables for nontargeted
explorativeness
Across time
Boldness (composite variable)
Novel objects
Inner area movements
Emergence from a refuge
Wall time
Death feigning behavior
Activity (composite variable)
Covered distance
Amount of movements
Nontargeted explorativeness
(composite variable)
Number of turning angles <90°
Variance of turning angles
Kendall’s
coefficient of
concordance W
P-value
0.258
0.298
0.970
0.834
<0.001
0.016
<0.001
0.003
0.550
0.377
0.584
0.540
0.494
0.663
0.583
0.615
0.572
0.775
0.008
0.270
0.006
0.011
0.031
0.001
0.006
0.003
0.008
<0.001
0.740
0.691
<0.001
<0.001
Consistency across context was estimated by performing a battery
of behavioral tests with adult beetles and calculating Kendall’s
coefficient of concordance W involving all tested variables (N = 48),
using the data of the first run. To test consistency over time, the
battery of behavioral tests was performed 3 times within a period of
approximately 17 days (N = 30–37, as some beetles died), and for each
variable, Kendall’s W was calculated. The composite variables were
calculated by adding the ranks of each behavioral variable within a
personality dimension (see Figure 2) for each beetle. All significant
P-values remained significant after false discovery rate correction for
multiple testing (Benjamini and Hochberg 1995); P-values are shown
before correction.
the environmental conditions, are quite robust (Table 2).
Such food-dependent differences in behavior are expected
to have significant ecological consequences and thus to be
potentially adaptive.
Influence of experienced food quality on fitness
expectations
An individual’s fitness can be affected fundamentally
by experiences and environmental conditions during
development (Lindström 1999; Awmack and Leather
2002; Relyea and Hoverman 2003; Martel et al. 2011). In
accordance with this, mustard beetles reared as larvae on
high-quality food gained higher body mass than individuals
consuming low-quality food (Figure 1b), whereby heavier
females of this species are known to produce more eggs
(Kühnle and Müller 2011). Due to the different starting
conditions as adults and the contrasting nutrient availability
in different food qualities throughout adult lifetime, there
should also be a difference in the future expectations of adult
beetles. This should lead to diverging behavioral variables
that contribute to risk-proneness of beetles. According to the
asset-protection principle, the individuals with high future
prospects should be more cautious and less likely to be bold
(Clark 1994). Furthermore, if this behavior is adaptive, it
should be consistently shown across context and time; thus,
beetles should develop personalities (Gosling 2001), which
first needed to be demonstrated.
390
Figure 2 Construction of personality dimensions of the mustard leaf beetle.
A battery of behavioral tests was conducted with adult beetles
(N = 48). To find possible associations of behavior among the
tested variables, an agglomerative cluster analysis was performed
(coefficient: 0.53). The groups indicate putative personality
dimensions, whose number was identified using a Silhouette plot.
The height indicates similarities on the absolute values of the
Kendall’s tau rank correlation matrix among the variables.
Personality dimensions in mustard leaf beetles
Mustard leaf beetles indeed clearly behaved consistently
across various contexts and through time and thus developed
personalities according to the definition by Gosling (2001).
Three behavioral dimensions could be derived from 9 behavioral variables tested in 5 different test setups or contexts.
The 5 variables that clustered in the boldness dimension and
highly correlated among each other (Table 2, Figure 2), novel
objects, inner area movements, emergence from a refuge, wall time,
and death-feigning behavior, were derived from all 5 test setups,
demonstrating a high consistency across a very broad range
of contexts. To our knowledge, there are only few other studies in which personality of a nonsocial insect was tested by
clustering various behavioral variables. For example, in firebugs only 2 variables, namely emergence and walking latency,
grouped in one cluster described as boldness (Gyuris et al.
2011). In contrast, in these hemimetabolic insects, novel objects
clustered with 2 other variables in a separate dimension,
which they name the exploratory axis (Gyuris et al. 2011),
whereas it was grouped in the boldness dimension in mustard
leaf beetles (Figure 2). The variables clustering within the
boldness dimension for the mustard leaf beetle are typically
Behavioral Ecology
used to characterize anxiety-like behavior in vertebrates (Prut
and Belzung 2003; Ardayfio and Kim 2006). For example, a
longer time needed to emerge from a refuge, a shorter time
to reach the protected wall area, and a longer duration of
thanatosis are interpreted as lower boldness. Anxiety-related
behavior of mice is often tested using a dark-light emergence
assay by measuring the time that an animal needs to emerge
from a secure refuge (Ardayfio and Kim 2006). Comparable
shy–bold -continua with regard to risk-taking behavior have
been described in a number of vertebrates (Sloan Wilson
et al. 1994). Furthermore, an increased time spent in the
central unprotected part of an open field is an indication of
less anxious or bold behavior of animals (Prut and Belzung
2003). Such behavior is expected to increase the number of
contacts to novel objects positioned in the central part, and
therefore the clustering of these 2 variables, inner area movements and novel objects, in 1 group is evident. Alternatively,
responses to novel objects can be interpreted as exploration
behavior (see above, Russell and Pearce 1971; Gyuris et al.
2011; Dammhahn 2012).
The activity dimension of the beetles was well described by
the covered distance and the amount of movements, whereas the
nontargeted exporativeness dimension included the variables
number of turning angles <90° and variance of turning angles.
Such increase in turning angles has been interpreted as thorough exploration behavior by Morales and Ellner (2002). As
no stimuli were offered in this test, we termed the personality
dimension “nontargeted explorativeness”.
All but one behavioral variable of the mustard leaf beetles
proved to be consistent over a quite long time span (Table 2),
testing the animals in weekly intervals more than about 3
weeks. As the overall life cycle of this species lasts 35–45 days
(Mahar et al. 2007), these 3 weeks are a substantial part of
the adult life. Earlier studies on the consistency of behavioral
traits over time in insects tested only repeatedly within less
than a week, partly due to shorter life time of the animals
(Gyuris et al. 2011; Schuett et al. 2011). Whether the consistency remains stable under changing environmental conditions needs to be tested in future studies.
Influence of food quality on personality dimensions
In accordance with our prediction, personalities differed
depending on the food quality that the beetles were facing,
especially with regard to the boldness and activity dimensions
(Figure 3a,3b). Beetles feeding low-quality diet were bolder
than animals reared on high-quality food. Such a pattern
is in line with theoretical models postulating an adaptive
explanation for the presence of personality (Stamps 2007;
Wolf et al. 2007). The behavioral variables clustering
within the boldness dimension may strongly contribute to
antipredator behavior. For example, strains of red flour
beetles, Tribolium castaneum (Coleoptera: Tenebrionidae),
selected for long death-feigning durations experienced a
lower frequency of predation when confronted with jumping
spiders, Hasarius adansoni (Arachnida: Salticidae), than
beetles with short death-feigning (Miyatake et al. 2004). At the
same time, prolonged antipredator behavior is expected to be
costly because of reduced foraging and mating opportunities
(McNamara and Houston 1990). Therefore, if individuals
differ in their antipredator behavior, consequences for
future expectations are likely to be of enormous relevance.
Although bolder animals potentially have a shorter life span,
there is a general trend that bolder individuals exhibit higher
reproductive success than shyer ones (Smith and Blumstein
2008). This can be explained by the fact that activity and
boldness are often positively correlated with food intake
rates, growth, and/or fecundity (Biro and Stamps 2008). The
391
Tremmel and Müller • Environmental impact on personality
Table 3 Influence of food quality on overall personality and on single personality dimensions of leaf beetles.
MANOVA results on complete model
Personality
Quality
Df
Wilks lambda
Approx F
num Df
den Df
P-value
1
0.787
3.965
3
44
0.014
Sum Sq
Df
F-value
P-value
8090
53084
1
46
7.011
0.011
4135.7
31552.3
1
46
6.030
0.018
151.6
30528.9
1
46
0.228
0.635
ANOVA results on single personality dimensions
Boldness
Quality
Residuals
Activity
Quality
Residuals
Nontargeted exploratives
Quality
Residuals
The 3 respective composite variables were used as response variables and food quality as explanatory variable in MANOVA. Non-significant
variables were removed to obtain the minimal adequate model. Univariate ANOVAs were used as post hoc tests to reveal the influence of food
quality on single personality dimensions.
increased boldness of mustard leaf beetles reared on lowquality food may contribute to increased future productivity
by compensating lower reproductive values. Differences
in boldness independent from environmental conditions
were found in Myrmica ants (Hymenoptera: Formicidae).
Individuals from the patroller casts were shown to be bolder,
more aggressive, and more active than members from the
foraging-recruit and brood-carer casts (Chapman et al. 2011).
Male field crickets (Gryllus integer, Orthoptera: Gryllidae)
become less bold after maturation. This has been explained
by the fact that males use a conspicuous call to attract females,
Figure 3 Influence of experienced food quality on (a) boldness, (b) activity,
and (c) nontargeted explorativeness of the mustard leaf beetle. For
each personality dimension, a composite variable was calculated
by adding the ranks of an individual for each included behavioral
variable. These 3 respective variables were used as response variables,
and food quality and sex of the beetles as explanatory variables in
a MANOVA (for statistical results see Table 2). Boxplots show the
median, quartiles, and maximum and minimum values of each data
set (N = 26 for high-quality food animals, and N = 22 for low-quality
food animals). Asterisks denote significant differences (*: P < 0.05);
n.s.—not significant.
which, however, leads to a higher predation risk (Hedrick
and Kortet 2012).
Furthermore, beetles feeding high-quality diet were
more active, that is, covered a larger distance and showed
more movements, than beetles reared on low-quality food.
Interestingly, this result points in the opposite direction than
the one for the boldness dimension, thus activity and boldness
are not necessarily positively correlated. The reduced activity
of the insects feeding low-quality diet may be interpreted as
a constraint, which is due to the fact that lower amounts of
energy reserves such as proteins are available in their food,
namely old cabbage leaves, compared with the young cabbage
leaves serving as high-quality food (Travers-Martin and Müller
2008). To compensate for the consequences of reduced activity due to a lower energy availability, these animals have to
increase their boldness to improve their reproductive chances.
The third personality dimension describing nontargeted
explorativeness by the number of turning angles <90° and the
variance of turning angles was not affected by food quality
(Figure 3c). Thus, life-history strategy has likely no influence
on this personality dimension. Nevertheless, this personality dimension might play an important role for individuals
searching for targets (i.e., food, mate, and so on), as it has
been suggested that an alteration of properties of movement
can increase the chances to find unknown objects of interest
without prominent cues (Bartumeus et al. 2005, Komin et al.
2004). Furthermore, there were no differences in personality
dimensions between females and males. Thus, although the
investment into reproduction is usually higher for females
than for males, this is not necessarily mirrored in differences
in boldness, activity, or explorativeness. Further experiments
are needed to disentangle the influence of larval experience
separately from adult experience on adult personalities, to
gain insights into the mechanisms of personality shaping.
However, taken together, our results illustrate that the behavior of insects is composed of various modules that apparently
relate differently to life-history expectations.
The present study demonstrates the importance of
environmental conditions in shaping not only performance
but also behavior of a specialist insect pest. Diverse behavioral
traits, which are typical for invertebrates and vertebrates
alike, were found to be consistent over various contexts and
392
through time, grouping in personality dimensions. Future
studies should elaborate whether the phenomenon shown in
the mustard leaf beetle is more general in herbivores that are
strongly dependent on the host quality and whether it may be
also found in generalists.
Supplementary Material
Supplementary material can be found at http://www.beheco.
oxfordjournals.org/.
Funding
German Research Foundation (DFG Forschergruppe FOR
1232, MU 1829/8-1).
We thank the gardeners of Bielefeld University for help in plant
cultivation, Helge Landskron for help in insect rearing, and Fritz
Trillmich for helpful comments on an earlier draft of the manuscript.
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