DOI: 10.1111/eea.12079
Predation promotes survival of beetles with lower
resting metabolic rates
Indrikis Krams1,2,3*, Inese Kivleniece3, Aare Kuusik4, Tatjana Krama3, Raivo M€and1,
Markus J. Rantala2, Santa Znotinßa3, Todd M. Freeberg5 & Marika M€and4
1
Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, Tartu 51014, Estonia, 2Department of Biology,
University of Turku, Turku, FIN-20014, Finland, 3Institute of Systematic Biology, University of Daugavpils, Vienibas 13,
Daugavpils, LV-5401, Latvia, 4Department of Plant Protection, Institute of Agricultural and Environmental Sciences,
Estonian University of Life Science, Kreutzwaldi 1, Tartu 51014, Estonia, and 5Department of Psychology, University of
Tennessee, Austin Peay Building 301B, Knoxville, TN 37996, USA
Accepted: 22 April 2013
Key words: behavioural syndrome, Tenebrio molitor, natural selection, mealworm, Coleoptera,
Tenebrionidae, predation threat, Rattus norvegicus, personality type
Abstract
The energetic definition of fitness predicts that natural selection will maximize the residual energy
available for growth and reproduction suggesting that energy metabolism might be a target of selection. In this experimental study, we investigated whether female and male yellow mealworm beetles,
Tenebrio molitor L. (Coleoptera: Tenebrionidae), differ in their hiding behaviour, individual response
latency time, and duration of immobility to treatments mimicking an approaching predation threat.
We experimentally tested whether consistently repeatable anti-predatory responses and resting metabolic rates (RMR) correlated with survival rates of individuals exposed to a nocturnal predator, the
brown rat, Rattus norvegicus (Berkenhout) (Rodentia: Muridae). Resting metabolic rate was part of a
syndrome involving anti-predator behaviour. Individuals with lower RMR concealed themselves
against predators in substrate more successfully than individuals with higher RMR, and hiding was
associated with longer periods of immobility. Ultimately, mortality was higher in the high-RMR beetles compared to the low-RMR beetles. Our results provide direct evidence of natural selection
against mobility, i.e., for reduced RMR in T. molitor beetles.
Introduction
Natural selection is widely recognized as the primary cause
of adaptive evolution. This assertion is supported by
extensive studies carried out mainly on morphological and
life-history traits (e.g., Endler, 1986; Mappes et al., 2005).
In contrast, we know much less regarding selection pressure on such important physiological traits as maintenance
metabolism, the energetic processes occurring within an
organism that are necessary for the maintenance of life. As
fitness-related traits are often energetically costly, it has
been hypothesized that selection should act directly on the
energetics of individuals (Peterson et al., 1999; Lovegrove,
2003; Rezende et al., 2005). However, efforts to examine
the relationship between fitness and components of the
*Correspondence: I. Krams, Institute of Ecology and Earth Sciences,
University of Tartu, Vanemuise 46, Tartu 51014, Estonia.
E-mail: [email protected]
94
energy budget are surprisingly scarce. The existing studies
have focused primarily on resting metabolic rate (RMR),
reflecting the minimum energy required to keep an individual alive. It is still largely not certain whether natural
selection might influence RMR, and how consistent over
time such influences might be (Boratynski & Koteja, 2009).
Predation is widely recognized as the major cause of
mortality for active, bold, risk-taking individuals (e.g.,
Smith & Blumstein, 2008; Biro & Booth, 2009). As such,
predation has been identified as an important factor in the
evolution of personality traits, such as activity, exploration, and boldness (e.g., Dingemanse et al., 2007; Niemel€a
et al., 2012, 2013). Predation incurs not only direct mortality costs but also the loss of resources via such non-lethal
effects of predation as increased vigilance time and shifts
for safer and less profitable foraging sites (Preisser et al.,
2005; Stamps, 2007; Lima, 2009), unless the bold and
active individuals are dominants in their social groups.
Consequently, the adaptive significance of risk-taking
depends on the relative costs and benefits of being bold at
© 2013 Netherlands Entomological Society Entomologia Experimentalis et Applicata 148: 94–103, 2013
Predation risk and metabolism in a beetle 95
different times and in different microenvironments: bold
individuals may obtain a fitness advantage (higher
resource intake rates) if predation risk is low, whereas shy
individuals may have higher fitness if predation risk is high
(Sih et al., 2004). However, higher RMRs may be positively linked to greater fecundity (e.g., Scholnick, 1995),
and maximal RMRs are often seen as important selection
criteria for optimal foraging and escaping predators (Millidine et al., 2009; Houston, 2010).
Numerous studies have reported interspecific and intraspecific variation (Dohm et al., 2001; Lovegrove, 2003;
Labocha et al., 2004; Ronning et al., 2007; Gebczynski,
2008; Jetz et al., 2008), and also sex-specific variation
(Boratynski et al., 2010), in the metabolic rates and behaviour of animals. Some attempts have been made to explain
the evolutionary and ecological causes behind that variation (Garland & Carter, 1994; Watson & Lighton, 1994;
Angilletta & Sears, 2003; Konarzewski et al., 2005; Rezende
et al., 2005; Boratynski et al., 2010; Kortet et al., 2010a).
Recent studies reveal that differences in behaviour and
physiology of many animal species are individual-based:
differences among individuals are consistent across contexts and stable over time (referred to as temperament or
personality; Groothuis & Carere, 2005; Sih & Bell, 2008;
Bell et al., 2009; Dingemanse & Wolf, 2010; Nicolaus
et al., 2012).
Animal personalities are considered to be relatively stable over time because risk-taking and other behaviour promoting high food intake rates are driven by individually
consistent intrinsic growth rates (Stamps, 2007), which
appear to be dependent on consistent individual differences in energy metabolism (Biro & Stamps, 2008, 2010).
Some experimental evidence shows that individuals having
comparatively higher metabolic rates may also have higher
energy output (Speakman et al., 2003, 2004; Rezende
et al., 2005, 2009). However, experimental studies are
needed that relate RMRs, personality, energy output, and
survival. The best evidence linking energy metabolism and
fitness comes so far from the study by Artacho & Nespolo
(2009), showing directional selection against increased
energy metabolism in snails.
In this experimental study, we investigated whether
female and male yellow mealworm beetles, Tenebrio molitor L. (Coleoptera: Tenebrionidae) differed over time in
their RMR, individual response latency time, duration of
immobility, and hiding behaviour to treatments mimicking an approaching predation threat. We tested whether
anti-predatory responses correlated with survival rates of
individuals exposed to a nocturnal predator, viz., the
brown rat, Rattus norvegicus (Berkenhout) (Rodentia:
Muridae). Resting metabolic rate was used to test for any
relationships among individual anti-predator responses
and survival, to explain the origin and existence of different personality types in T. molitor. We also tested whether
there were any behavioural correlations in individual variation in two or more behaviours, termed behavioural syndromes (e.g., Sih et al., 2004; Kortet & Hedrick, 2007; Bell
et al., 2009; Reale et al., 2010a,b). Behaviour is an animal’s
way of interacting with its environment and it is therefore
a prime target for natural selection (Davies et al., 2012).
Materials and methods
Beetles
The beetles used in the experiment originated from a natural population. We captured the progenitor beetles in several barns in south-eastern Latvia (Daugavpils, – 55°55′N,
26°37′E; Preilßi, – 56°17′N, 26°43′E, Kraslava, – 55°53′N,
27°9′E) in 2008–2011. The stock culture was maintained at
25 2 °C on bran mixed with wheat flour, fresh carrots,
and apples. We removed pupae from the culture on the
day of pupation, weighed them, and determined their sex
according to Bhattacharya et al. (1970). We then kept the
pupae and newly emerged adults individually in numbered
200 ml plastic containers filled with a mixture of bran and
wheat flour and with fresh carrot and apple pieces offered
ad libitum. We weighed 10-day-old individuals using a
Kern analytical balance (Kern & Sohn, Balingen, Germany). We used beetles of average ( 4%) body mass.
This was done to avoid any possible body mass effects on
RMR and anti-predator behaviour. Body mass of males
used in this study did not differ significantly from that of
females (mean SD = 0.1259 0.0003 and 0.1247 0.0002 g, respectively; t-test: t = 47.86, d.f. = 478,
P = 0.46). The study was conducted between January and
April 2011.
Flow-through CO2 respirometry
The gas analyser and flow-through respirometer were calibrated at different flow rates by means of calibration gases
(Tr€agergase; Saxon Junkalor, Dessau, Germany) with gas
injection (see also Kuusik et al., 2002; M€and et al., 2006).
When the respirometry was carried out in dry air, the
insect chamber (3 ml Eppendorf test tube) was perfused
with dry (5–7% r.h.) CO2-free air, produced by passing air
over Drierite (WA Hammond Drierite, Xenia, OH, USA)
and soda-lime granules at a flow rate of 60 ml min 1.
Baseline drift of the analyser was corrected during analysis
from the measurements at the beginning and end of each
trial with the respirometer chamber empty (Duncan, 2003;
Duncan & Byrne, 2005; Gray & Bradley, 2006).
A single beetle was placed into the insect chamber. The
respirometric device was combined with an infrared (IR)
optical system using IR-emitting diodes (TSA6203) and
96 Krams et al.
IR-sensor diodes (BP104) that were placed on the sides of
the insect chamber. Infrared-diodes made it possible to
record CO2 production and movements of each beetle
simultaneously (Figure 1). The beetles were kept in the
insect chambers for at least 20 min. All the beetles reached
the lowest rates of CO2 production in a 10–15 min period,
when they were motionless. The mean metabolic rate was
calculated by averaging data obtained over long periods
(e.g., Metspalu et al., 2002). As the beetles were either
immobile or active just for short periods, the baselines of
recorded CO2 emissions roughly corresponded to the
RMR of each insect. As soon as the measurements were
over, we returned the beetles to their plastic containers.
The RMR trials were repeated 8 days later. Nespolo &
Franco (2007) showed that repeatabilities are linearly
reduced with time between measurements, suggesting
habituation to experimental manipulations. However, the
time interval of 8 days seems to be sufficient in the case of
such short-lived organisms as mealworm beetles. In total,
we obtained behavioural data from 480 individuals (240
males and 240 females).
Mimicking of predator approach
Three days after the second RMR trials, we exposed the
beetles to a different context, to assess reactions to a mimicked predatory stimulus. For each beetle, in the beginning
of the night (20:00–23:00 hours) we hit its 200 ml plastic
container on the side with a stick, applying a mass of about
40 g from approximately 10 cm distance. We observed
the response of the beetles under red light (25-W red
5
560
4
3
400
2
320
1
240
0
160
–1
80
–2
0
0
5
10
15
20
Time (s)
25
30
Volts
VCO2 (µl h–1)
480
–3
35
Figure 1 Simultaneous recordings of an infrared gas analyser
(lower trace) and infrared sensors (upper trace, V), showing
metabolic rate (VCO2 ml h 1) coinciding with active struggling
movements of the mealworm Tenebrio molitor (0–7 s) and
heartbeats modulated by abdominal pulsations (8–26 s) after
flicking an insect chamber at the 8th sec (arrow), and resumed
struggling movements (26–35 s).
incandescent bulb); because members of the Tenebrio family likely cannot see long (red) wavelengths (Briscoe &
Chittka, 2001), the dim red light should mimic nocturnal
conditions of the beetles (Kivleniece et al., 2010; Krams
et al., 2011), without an effect on beetle activity. We
recorded individual response latency time to the mechanical stimulus and total time the beetles spent motionless,
either on the bran surface or hidden in the layer of bran. If
the beetle continued to move under the layer of bran, it
was not considered to be immobile. We repeated this trial
6 days later.
Predators and survival experiments
Major predators of wild mealworm beetles include birds,
and rodents such as mice and rats. In this study, wild
brown rats were used as predators of mealworm beetles.
These rats were chosen for this study as their searching,
predatory, and neophobic behaviours were not impaired
by captivity and selection. We used 22 rats (13 females and
9 males) kept in the municipal zoo of Daugavpils (Latvia)
for insect survival trials, and all trials were carried out in
the laboratory of the zoo. Three hours prior to the trials,
rats were placed in individual cages (60 9 50 9 40 cm)
with water and food consisting of cereals and vegetables
(product number ZVP-1500; Vitapol, Brzoza, Poland) ad
libitum and Vitapol bedding for rats (product number
ZVP-1053).
To provide a measure of the effect of individual antipredator responses on survival, we placed beetles in predation exposure arenas (30 9 50 9 40 cm) and exposed
them to rats deprived of food for 2 h before the onset of
the trial. The predation trial arena was set up to be as natural as possible, with the floor covered with a 2-cm layer of
bran. We used this depth of bran to provide beetles their
usual food supply, to allow the beetles to walk without
slipping, and to burrow as a form of escape mechanism.
All beetles were marked individually with a correction pen
(Optex, Berlin, Germany), by drawing small dots on the
dorsal side of their abdomens. During a preliminary study,
in which rats were offered a marked and an unmarked beetle, they chose the marked beetles first in 17 of 34 cases
(two-tailed sign-test: Z = 0.17, P = 0.87), indicating that
the markings per se did not influence mealworm survival.
An hour before each predation trial, a rat was released
into the predation cage to familiarize with the environment. After 30 min, the rat was removed and returned to
its cage. Ten beetles (males or females) were then released
into the arena, ensuring that no beetles were left lying on
their backs. In each trial, we used five individuals that had
remained active and five individuals that were consistently
hiding during previous predator-approach mimicking
experiments. The beetles were then left undisturbed for a
Predation risk and metabolism in a beetle 97
further 30 min, giving them ample time to search out and
find cover. After this 30-min period, a rat was placed back
into the predation exposure arena, and each predation
experiment lasted 15 min. We recorded whether the beetles dug in the layer of bran as soon as the rat was released
in the cage. As soon as the trial was over, we removed the
rat and counted the survivors. We used actual predation
events here, rather than simulated predation events or
proxy measures, as the most direct test of a potential
selection pressure on RMR. However, we intended to
limit the total exposure of beetles to potential depredation, therefore, each beetle was only tested once with rat
predators.
We carried out survival experiments separately for
male and female beetles. Each rat was used only twice:
during a male beetle survival experiment and during a
female beetle survival experiment, which were separated
by a 60-min break for each individual rat. The order of
trials was chosen randomly for each sex of beetles and for
each predator. Thus, each individual test beetle (n = 480)
was exposed to two simulated predator-approach tests in
an open arena and a single survival test. The RMR of each
individual beetle was known (see above). All measurements and observations were done at 23 °C. Beetles were
weighed to the nearest 0.001 g with an electronic balance
(Kern ABS 120-4; Kern & Son), and this measure was
highly repeatable (R = 0.97, P<0.0001).
Data analysis
Values of behavioural and metabolic data were not distributed normally and so were square root transformed prior
to further statistical analysis. We used one-way analysis of
variance (one-way ANOVA) to compare means of different variables. The strength and direction of the linear relationship between two variables were tested by using the
analysis of correlation. Pearson’s correlation coefficient
was calculated for continuous variables, whereas Spearman’s coefficient was used for discrete variables. Fisher’s
exact test was used in the analysis of contingency tables.
The general linear model (GLM) is a generalization of a
multiple linear regression model, and we used it to test for
functional relationships in the case of several variables (Sokal & Rohlf, 2012). To ascertain whether individual test
beetles were consistent in their behaviour, the repeatabilities (i.e., the fractions of behavioural variation that is due
to differences between individuals; Bell et al., 2009) of
latency to resume movement following the mechanical
stimulus, and the total time beetles spent immobile, were
calculated across two trials. Lessells & Boag (1987) suggested a method for calculating approximate repeatability
(R) values from the F ratio, which we also used in this
study. We calculated mean values of the two behavioural
responses and used these means in subsequent analyses.
The existence of a behavioural syndrome was then assessed
from the correlations between latency to resume movement following mechanical stimulus and the immobility
time. All statistical analyses were performed in Statistica
8.0 for Windows (StatSoft, Tulsa, OK, USA). All the tests
were two-tailed.
Results
Consistency and correlations of RMR and anti-predator behaviour
over time
Resting metabolic rate of mealworm beetles (mean SD = 0.84 042 VCO2 ml h 1) was found to be highly
repeatable among individual beetles (R = 0.926;
F479,480 = 52.44, P<0.0001). The latency to become immobile in response to flicking the plastic container varied
between 2 and 240 s (42.43 40.42 s), and the total time
spent motionless after flicking varied between 3 and 293 s
(93.87 50.75 s). The response latency to flicking and
the total time spent immobile were negatively correlated
(Pearson’s r = 0.473, P<0.0001; Figure 2) indicating
that rapid interruption in activity was associated with
longer periods of immobility, which suggests a behavioural
syndrome. Response latency after flicking of the plastic
container was also highly repeatable (R = 0.613;
F479,480 = 4.166, P = 0.001), as was the total time spent
immobile (R = 0.848; F479,480 = 12.162, P<0.0001).
We found that 158 of 480 beetles dug in the layer of bran
when the plastic container was flicked. The number of
females (n = 103) and males (n = 55) hiding in the layer
of bran was significantly different (v2 = 21.738, d.f. = 1,
P = 0.0001). Digging in the layer of bran was associated
Figure 2 Negative relationship between response latency to
simulated predator approach and duration of time spent
motionless of mealworm beetles in the plastic container.
98 Krams et al.
with the total time spent immobile while hiding in bran in
the plastic container. The duration of immobility of individuals that dug in the bran layer was significantly greater
than that of individuals that did not dig in the layer of bran
(131.91 35.51 vs. 55.83 45.72 s; one-way ANOVA:
F1,478 = 91.715, P<0.0001). In contrast, the latency to
become immobile of individuals that dug in the layer bran
(45.42 35.75 s) was similar to that of individuals that
did not dig in the layer of bran (39.43 13.03 s;
F1,478 = 3.003, P = 0.085).
Determinants of survival
Rats depredated all the beetles within a zone around the
tips of their whiskers, independent of whether the beetles
moved or stayed motionless within this zone. Beetles that
stayed outside the zone were not attacked (Fisher’s exact
test: P<0.001) suggesting that rats used information they
got by touch of their whiskers. Rats were never seen digging in the layer of bran for immobile beetles.
Rats depredated 7.77 0.91 (mean SD) beetles during each experimental trial and only 107 of 480 beetles survived. The number of female (n = 78) and male (n = 29)
survivors was significantly different (v2 = 28.88, d.f. = 1,
P<0.001). The average values of RMR did not differ
between sexes (males: 0.88 0.39, females: 0.79 0.50
VCO2 ml h 1; one-way ANOVA: F1,105 = 0.08, P = 0.64,
whereas the RMR of survivors was significantly lower than
that of non-survivors (0.54 0.23 vs. 1.33 0.41
VCO2 ml h 1; F1,478 = 100.437, P<0.0001) (Figure 3).
This was confirmed by GLM analysis showing that survival
was dependent on the RMR and not on sex of the beetles
(Table 1).
Resting metabolic rate correlated positively with
response latency (Pearson’s r = 0.280, P<0.01)
(Figure 4). Response latency in the simulated predatorapproach trials did not differ between survivors and
non-survivors (30.61 11.46 vs. 34.36 35.58 s;
F1,478 = 0.284, P = 0.59). The results of GLM analysis
also showed that latency to respond was dependent on
RMR, and was not dependent on sex, nor on their
interaction (Table 2).
Figure 3 Resting metabolic rate (mean SE) of survivor and
non-survivor mealworm beetles.
Resting metabolic rate correlated negatively with
total time of immobility (Pearson’s r = 0.247, P<0.01)
(Figure 5), and it differed significantly between survivors
and non-survivors (115.78 40.47 vs. 71.95 23.45 s;
F1,478 = 95.882, P<0.0001). The results of GLM analysis
confirmed that the duration of immobility was dependent
on the RMR and sex, whereas the interaction of RMR and
sex was not significant (Table 2). This indicates that individuals with lower RMRs had longer periods of immobility.
Survivors were highly likely to hide in the bran layer (99
of 107 individuals), whereas only 24 of 373 non-survivors
dug in the layer of bran (v2 = 309.07, d.f. = 1, P<0.0001).
The results of GLM analysis suggested that digging behaviour was dependent on RMR, and was not dependent on
sex or on the interaction of sex and RMR in the plastic
container (Table 1).
An additional GLM showed that survival was dependent
on the duration of immobility (F1,121 = 2.53, P<0.001),
duration of hiding in the bran layer (F1,121 = 259.34,
P<0.001), and the interaction between the total time spent
immobile and the propensity to dig in the layer of bran
(F1,121 = 5.86, P<0.001) under the risk of predation. These
results suggest that longer periods of hiding in the bran
Table 1 General linear model analysis of the effects of resting metabolic rate (RMR) and sex on survival and digging behaviour of Tenebrio
molitor mealworms
Survival
RMR
Sex
RMR*sex
Error
Digging behaviour
d.f.
F
MS
P
d.f.
F
MS
P
85
1
26
367
3.793
0.381
1.153
0.333
0.330
0.101
0.001
0.54
0.30
85
1
26
367
2.481
2.562
1.445
0.328
0.339
0.190
0.02
0.011
0.10
Predation risk and metabolism in a beetle 99
Figure 4 Correlation between resting metabolic rate of
mealworm beetles and response latency to flicking the plastic
container.
Figure 5 Correlation between resting metabolic rate of
mealworm beetles and duration of immobility to flicking the
plastic container.
increased rates of survival. Total time spent immobile of
survivors that dug in the bran layer was higher than total
time of immobility of non-survivors that dug in the layer
of bran (151.69 32.99 vs. 102.78 29.30 s; one-way
ANOVA: F1,121 = 24.610, P<0.001). The response latency
and the interactions were not significant (P>0.05).
adult individuals can be associated with low fitness (Bochdansky et al., 2005; Czarnoleski et al., 2008; Artacho &
Nespolo, 2009). Although T. molitor usually stays in places
with abundant food resources, several studies have shown
that the energy budget of T. molitor may be seriously constrained due to reproductive behaviour of the species.
Males and females of T. molitor often mate repeatedly,
chases and fights are not uncommon, and both pre- and
post-copulatory behaviours are important components of
sexual selection in this species (Worden & Parker, 2001,
2005). Our results provide evidence of natural selection
for reduced RMR in T. molitor beetles. Individuals with
higher RMR were eliminated by nocturnal predators,
whereas individuals with reduced RMR were less negatively impacted by these predators. Thus, this study reveals
directional selection against high RMR, which is the trait
that represents costs under severe risk of predation.
Why is mortality increased in T. molitor individuals
with higher RMR rates? Our results suggest that RMR may
be part of a syndrome that involves anti-predator behaviour. Individuals with reduced RMR appear to hide in the
Discussion
This study revealed survival costs of being active, as mealworm beetles with shorter latencies to become immobile,
longer immobility times, and those hiding in the layer of
bran survived significantly better than individuals that
were slow to freeze, resumed movement quickly, or failed
to hide in the bran. It was also found that RMR in T. molitor was negatively associated with the probability of survival under the risk of nocturnal predation. It is important
to note that this cost of higher RMR was not sex-specific.
The energetic definition of fitness predicts that natural
selection maximizes the residual energy available for
growth and reproduction (Brown et al., 1993; Bochdansky
et al., 2005). This means that high maintenance costs in
Table 2 General linear model analysis of the effects of resting metabolic rate and sex of Tenebrio molitor mealworms on their response
latency to flicking, and on the duration of immobility
Response latency
RMR
Sex
RMR*sex
Error
Duration of immobility
d.f.
F
MS
P
d.f.
F
MS
P
85
1
26
367
3.129
1.687
0.963
17.18
9.195
5.248
0.001
0.20
0.52
85
1
26
367
2.400
6.023
1.038
3.598
2.271
2.006
0.001
0.01
0.30
100 Krams et al.
layer of bran more often and longer than individuals with
elevated RMR. Hiding in the layer of bran was found to be
the most important anti-predator strategy of T. molitor in
this study. Digging in bran and reduced rates of RMR were
also positively associated with longer periods of immobility. Thus, reduced rates of RMR, propensity to find shelter,
and longer total duration of immobility accounted for
increased survival when attacked by the brown rat, a common predator on beetles in barns. Individuals with higher
levels of RMR were bold, and bold individuals were found
to be more exposed to the risk of rodent predation. We
also found another behavioural syndrome, where the
latency to respond with immobility was negatively correlated with the total duration of immobility. Overall, our
results support the fact that RMR may be positively related
to mortality, as recently found in land snails, juvenile
squirrels, captive voles, and mealworm beetles (Alvarez &
Nicieza, 2005; Smith & Blumstein, 2008; Artacho &
Nespolo, 2009; Boratynski & Koteja, 2009; Larivee et al.,
2010; Lantova et al., 2011 Krams et al., 2013). Repeatabilities for our four main measures (RMR, hiding behaviour,
latency to become immobile, and total time spent immobile) were all statistically significant and ranged from 0.613
(latency to respond after flicking of the plastic container)
to 0.926 (RMR). Such high repeatabilities further point to
the variability among individuals, but consistency within
individuals, for these different measures.
Recent theoretical studies have emphasized that consistent individual behavioural differences should be linked
to life-history differences (Stamps, 2007; Wolf et al.,
2007). However, only a few experimental studies have
shown a link between life history and behaviour within a
species (e.g., Dingemanse & de Goede, 2004; Boon et al.,
2007; Biro & Stamps, 2008; Reale et al., 2009, 2010a,b).
Although energy metabolism promises to be a general
physiological explanation for consistent individual differences in behaviour (Biro & Stamps, 2008), even fewer
studies have established a clear link between personality
and metabolic rate (Careau et al., 2008). Our results show
that such physiological traits as RMR can be strongly associated with personality types in T. molitor beetles, and that
energy metabolism can be a target of natural selection.
However, it is still not clear whether metabolic costs and
personality traits are reflected also in the absolute fitness
of individuals in terms of increased net reproductive rate.
Our results are consistent with a recently proposed
hypothesis suggesting that personality traits may couple
with life-history traits and form integrative pace-of-life
syndromes, in which behaviour and life history co-vary in
a fast–slow lifestyle continuum (Careau et al., 2009, 2010;
Reale et al., 2010a,b). For example, bold behaviour should
yield higher fitness when combined with high metabolism
and early (rather than late) maturation, because higher
mortality of bold individuals would make them unsuccessful in ever reaching the age required for late maturation
(Wolf et al., 2007). A high RMR may represent a higher
energetic budget that necessitates more time to be spent
foraging, elevating predation risk.
Different behavioural types may yield equal expected
life-time fitness, or perhaps absolute fitness may differ
across different environments (Biro et al., 2006; Boon
et al., 2008; Dingemanse & Wolf, 2010; Reale et al.,
2010a,b; Wolf & Weissing, 2010). Future studies need to
test predictions based on various combinations of life history, senescence-related effects (Daukste et al., 2012), and
physiological and behavioural variables to explain the
maintenance of different RMR and behavioural types in
populations. Finally, it has been suggested that parasites,
including pathogens, impose fitness costs comparable to
those from predators, and influence the adaptiveness of
personality traits associated with reproduction (Kortet
et al., 2010b). Therefore, future experimental and theoretical work in the field of personality research should
focus on the condition dependence of immune function
and coevolutionary dynamics between hosts and
parasites.
Acknowledgements
This work has been supported by Target Financing grant
SF170057s09 and European Social Fund within the Project
‘Support for the implementation of doctoral studies at
Daugavpils University’ (Agreement Nr. 2009/0140/1DP/
1.1.2.1.2./09/IPIA/VIAA/015) to Inese Kivleniece.
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