Food intake rates of inactive fish are positively linked to boldness in three-spined sticklebacks Gasterosteus aculeatus

Abstract

To investigate the link between personality and maximum food intake of inactive individuals, food-deprived three-spined sticklebacks Gasterosteus aculeatus at rest in their home compartments were provided with ad libitum prey items. Bolder individuals ate considerably more than shyer individuals, even after accounting for body size, while sociability did not have an effect. These findings support pace-of-life theory predicting that life-history strategies are linked to boldness. © 2016 The Authors. Journal of Fish Biology published by John Wiley & Sons Ltd on behalf of The Fisheries Society of the British Isles.

Full text

Journal of Fish Biology (2016)
doi:10.1111/jfb.12934, available online at wileyonlinelibrary.com
BRIEF COMMUNICATION
Food intake rates of inactive sh are positively linked to
boldness in three-spined sticklebacks Gasterosteus aculeatus
J. W. J*, A. M  N. J. B
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, U.K.
(Received 27 October 2015, Accepted 27 January 2016)
To investigate the link between personality and maximum food intake of inactive individuals,
food-deprived three-spined sticklebacks Gasterosteus aculeatus at rest in their home compartments
were provided with ad libitum prey items. Bolder individuals ate considerably more than shyer
individuals, even after accounting for body size, while sociability did not have an effect. These
ndings support pace-of-life theory predicting that life-history strategies are linked to boldness.
© 2016 The Authors. Journal of Fish Biology published by John Wiley & Sons Ltd
on behalf of The Fisheries Society of the British Isles.
Key words: animal personality; body size; energy; foraging; metabolism; pace-of-life.
It is now well known that consistent individual differences in behaviour, referred to
as animal personality, are ubiquitous across the animal kingdom (Réale et al., 2007;
Dingemanse & Wolf, 2010; Sih et al., 2015). Personality differences have been shown
to be linked to tness, to affect population dynamics, and to have fundamental ecolog-
ical and evolutionary implications (Réale et al., 2007; Wolf et al., 2007; Dingemanse
& Wolf, 2010; Conrad et al., 2011). The major question remains, however, why animal
personalities exist in the rst place.
One of the most prominent theories to explain animal personalities from an adaptive
perspective is that they exist because of underlying individual differences in state
(Dingemanse & Wolf, 2010; Sih et al., 2015), with the most widely proposed mech-
anism explaining personality differences in the context of broad life-history strategies
(Stamps, 2007; Wolf et al., 2007; Biro & Stamps, 2010), integrating behaviour into the
concept of a pace-of-life syndrome (Réale et al., 2010). Central to this theory is that dif-
ferences in traits such as boldness and aggression may arise through growth– mortality
trade-offs (Stamps, 2007; Biro & Stamps, 2008), effectively linking energetics with
animal personality research (Careau & Garland, 2012). According to this view, indi-
viduals with high rates of growth and fecundity are expected to show physiological
and behavioural adaptations associated with greater energy needs, such as higher rates
*Author to whom correspondence should be addressed. Tel.: +44 1223 767 129; email: j.w.jolles@gmail.com
1
© 2016 The Authors. Journal of Fish Biology published by John Wiley & Sons Ltd on behalf of The Fisheries Society of the British Isles.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited.

2J. W. JOLLES ET AL.
of food intake and a greater tendency to take risks (i.e. bolder), both as a cause and
consequence of their fast lifestyle (Biro & Stamps, 2008; Careau & Garland, 2012).
Empirical evidence is accumulating to support this theory: traits such as activity,
aggressiveness and boldness have been found to positively correlate with growth,
fecundity and other life-history traits (Biro & Stamps, 2008; Burton et al., 2011;
Conrad et al., 2011; Careau & Garland, 2012), and are positively related to rates
of food consumption (Biro & Stamps, 2008). For example, Ioannou et al. (2008)
showed that pairs of three-spined sticklebacks Gasterosteus aculeatus L. 1758 that
were quicker to leave refuge took less time to explore a potentially risky environment
and consumed more live prey than those that hid under cover for longer. In addition,
individuals with higher growth rates and fecundity would also require higher-capacity
‘metabolic engines’ (Biro & Stamps, 2010), which is reected by their higher resting
metabolic rates (RMR; Huntingford et al., 2010; Burton et al., 2011; Martins et al.,
2011). Therefore, even when not currently engaging in any energetically expensive
activities, such individuals are predicted to have higher energy requirements and thus
food intake (Biro & Stamps, 2010).
Here, for the rst time, it is tested whether personality differences are linked to food
intake rates when individuals are at rest and risk-reward trade-offs are kept at a mini-
mum, providing a more mechanistic link between boldness and food intake compared
to previous work focused on ecological consequences (Ioannou et al., 2008). Most vari-
ation in the food intake of inactive individuals is expected to be due to body size, with
larger individuals eating more (Beukema, 1968; Allen & Wootton, 1984). Nevertheless,
as boldness has been shown to positively correlate with growth and fecundity (Biro &
Stamps, 2008; Careau & Garland, 2012), and risk-taking behaviour with RMR (Killen
et al., 2011), it was predicted that bolder individuals would have a higher maximum
food intake than shyer individuals, even when at rest and after accounting for body size.
In contrast, personality traits that may not be strongly linked to growth or fecundity,
such as sociability, are expected to not affect maximum foraging rates when at rest.
To test these predictions, 96 G.aculeatus were randomly selected from a wild stock
which had been caught in tributaries of the River Cam, Cambridge, U.K., and were
socially housed in an environmentally controlled laboratory. During this time before
the start of experiments (over 6 months), the socially kept G.aculeatus were fed blood-
worms (Chironomid sp. larvae) ad libitum at the end of each day. Individuals were
individually photographed to measure their standard length (LS, from tip of snout to
caudal peduncle), which ranged from 3⋅06 to 5⋅25 cm (mean ±.. =4⋅07 ±0⋅04 cm).
Mass (M) was estimated from total length (LT; mean ±.. =5⋅13 ±0⋅05 cm) based
on LTand Mrelationship data from G.aculeatus extracted from www.shbase.org
using the formula M=aL
Tb(a=0⋅0068, describes body shape and condition;
b=3⋅28, describes isometric growth in body proportions) following Froese et al.
(2014). This formula thus does not take into account any individual variation in
other body measurements. The resulting Mestimates ranged from 0⋅56 to 3⋅02 g
(mean ±.. =1⋅50 ±0⋅05 g). After photographing, individuals were solitary housed
in compartments (18⋅5cm×9⋅5 cm; 18 cm deep) that were lined with gravel and
contained an articial plant for cover. To minimize stress of isolation, compartments
had perforated transparent Perspex walls that enabled the transfer of visual and chem-
ical cues of seven conspecics in neighbouring compartments. Each compartment
contained a 2 cm wide feeding dish at the plant cover so that individuals could feed
while staying concealed under cover.
© 2016 The Authors. Journal of Fish Biology published by John Wiley & Sons Ltd
on behalf of The Fisheries Society of the British Isles. 2016, doi:10.1111/jfb.12934

FOOD INTAKE RATES AT REST LINK TO BOLDNESS 3
After 3 days of acclimatization, G.aculeatus were rst assessed for boldness, i.e.
their willingness to take risks, and sociability, i.e. their tendency to approach others
excluding aggressive behaviour (Réale et al., 2007). To quantify boldness, an exper-
imental setup was used as detailed in Jolles et al. (2014, 2015). In short, individuals
were placed in a rectangular tank (55 cm length ×15 cm width ×20 cm height) lined
with sand in a slope ranging from a deep (15 cm ×10 cm; 13 cm depth), ‘safe’ area
that contained an articial plant for cover, to a shallow depth (3 cm) at the other side.
Boldness was quantied as the amount of time an individual spent out of plant cover
during the 30 min trial, with bolder individuals spending more time out of cover. To
quantify sociability, individuals were placed in the larger middle compartment (30 cm
width) of a tank (50 cm ×30 cm, 8 cm water depth) that was lengthwise divided by
two transparent Perspex partitions. One of the two smaller side compartments (10 cm
width) contained ve conspecics. Sociability was quantied by measuring the aver-
age distance of the focal individual from the compartment containing the conspecic
shoal during a 15 min trial. The conspecic shoal was created by randomly select-
ing individuals from the stock tanks, and allowed to acclimatize to the compartment
for 45 min at the start of each test day. The position of the compartment housing the
shoal was randomized every four trials, and after each compartment swap the shoal
was allowed to acclimatize for 10 min before the start of the next trial. Eight individu-
als were tested in identical tanks simultaneously, and different conspecics were used
to form the shoal in each of the eight sociability test tanks and for each test day. Test
trials were video-recorded from above and subsequently tracked using custom track-
ing scripts in Python (version 2.7.5; www.python.org), providing detailed positional
co-ordinates for each individual during each boldness and sociability trial. To stan-
dardize hunger levels, individuals were fed three Chironomus sp. at the end of each
day until all personality testing was nished.
To investigate the repeatability of behaviour, the key requirement of animal per-
sonality, individuals received two boldness sessions (on days 4 and 8 after individual
housing) and two sociability sessions (on days 6 and 10). Based on the positional
co-ordinates during the personality trials, it was found that individual G.aculeatus
spent mean ±.. 27⋅9±1⋅4% of their time out of cover (range: 0⋅0–62⋅8%) during
the boldness test and were at mean ±.. 47⋅9±2⋅3 mm from the compartment
housing conspecics (range: 13⋅0–116⋅0 mm) during the sociability test. As indi-
vidual G.aculeatus (n=96) were repeatable in the time they spent out of cover
(rs=0⋅41, P<0⋅001) and in their average distance from the shoal compartment
(rs=0⋅50, P<0⋅001), boldness and sociability scores were calculated for each
individual by averaging their behaviour across the two test sessions for each per-
sonality trait. Boldness was not correlated with sociability (rs=0⋅00, P>0⋅05) and
neither personality trait correlated with LS(rs=0⋅11, P>0⋅05; rs=0⋅10, P>0⋅05,
respectively).
A week after personality testing, during which two G.aculeatus had died from
unknown causes, all individuals (n=94) received a single Chironomus sp. daily
for three consecutive days to minimize stomach fullness and to ensure that Chi-
ronomus sp. would be consumed immediately when provided (Beukema, 1968).
Starting at 1430 hours on the fourth day of food restriction, individuals’ maxi-
mum food intake was measured by dropping ve medium-sized Chironomus sp.
(mean ±.. =12⋅7±0⋅4 mg wet mass, n=50 worms) onto the feeding dish in each
individual’s home compartment. After 15 min, the number of Chironomus sp. eaten
© 2016 The Authors. Journal of Fish Biology published by John Wiley & Sons Ltd
on behalf of The Fisheries Society of the British Isles. 2016, doi:10.1111/jfb.12934

4J. W. JOLLES ET AL.
T I. Coefcients of GLM on the maximum number of Chironomus sp. eaten by
food-deprived Gasterosteus aculeatus
Estimate .. Wald statistic (𝜒2)P
LS(mm) 0⋅05 0⋅00 93⋅03 <0⋅001
Boldness 0⋅35 0⋅13 7⋅31 <0⋅01
Sociability 0⋅00 0⋅00 0⋅00 >0⋅05
Data were tted to a Poisson distribution with log-link function (n=94). Backward stepwise elimination
was used and statistics for non-signicant terms were obtained by adding the non-signicant term to the
minimal model. LS, standard length.
was determined and ve additional Chironomus sp. were provided in the same manner
unless some Chironomus sp. remained uneaten. In the latter case, no additional Chi-
ronomus sp. were provided during that round. If during a later round all Chironomus
sp. were eaten, an additional ve were provided. Individuals were considered satiated
if they did not consume any Chironomus sp. for at least 30 min while Chironomus sp.
were still available on their feeding dish. As the maximum daily food intake may be
inuenced by the speed at which G.aculeatus can empty their stomach, provisioning
rounds were stopped after 3 h when all individuals were satiated. A generalized linear
model (GLM) was run with LS, boldness and sociability as xed factors to investigate
how these variables affected the total number of Chironomus sp. eaten. The data
were tted to a Poisson error distribution with log-link function, as appropriate for
count data, and residuals were visually inspected to ensure homogeneity of variance,
normality of error and linearity.
The maximum number of Chironomus sp. eaten during the feeding experi-
ment varied considerably among individuals, ranging from 15 to 59 bloodworms
(mean ±.. =36⋅1±1⋅1). LSwas the strongest predictor of food intake, with
larger individuals eating signicantly more Chironomus sp. [P<0⋅001; Table I and
Fig. 1(a)], although relative food intake in terms of percentage body mass dropped with
M(rs=−0⋅43, P<0⋅001). These ndings were unsurprising as larger individuals have
larger stomachs and can thus consume more food, and are in line with the common
nding that across teleosts a larger body mass is linked to a higher overall RMR but
lower mass-specic RMR (Clarke & Johnston, 1999). Next to LS, boldness was also
positively correlated with maximum food intake [P<0⋅01; Table I and Fig. 1(b)].
Keeping LSconstant at the average LS(40⋅7mm), the shyest and boldest individuals
were predicted to still vary up to 20% in their food intake [32⋅2 and 40⋅1Chironomus
sp., respectively; Fig. 1(a)]. This shows that individuals with different personality
types differ in their food intake even when inactive, i.e. not engaging in energetically
expensive activities (Biro & Stamps, 2010) and when foraging is not directly linked
to risk-reward trade-offs (Ioannou et al., 2008). This complements existing evidence
that bolder individuals tend to have higher feeding rates (Biro & Stamps, 2008), but is
the rst time this relationship has been shown for individuals at rest.
Various mechanisms may explain why even the food intake of G.aculeatus that
were inactive was positively linked to their boldness. First of all, bolder individuals
may have relatively larger stomachs than shyer G.aculeatus and are therefore able
to eat for longer. Secondly, bolder individuals may have a stronger motivation to eat,
with shyer individuals not continuing to feed to the same fullness level. Thirdly, bolder
© 2016 The Authors. Journal of Fish Biology published by John Wiley & Sons Ltd
on behalf of The Fisheries Society of the British Isles. 2016, doi:10.1111/jfb.12934

FOOD INTAKE RATES AT REST LINK TO BOLDNESS 5
(a) (b)
(c)
60 60
50
40
30
20
60
50
40
30
20
25 50 75 100
0·0 0·2
Boldness score
0·4 0·6
50
40
Total number of worms eaten
30
20
30 35 40
Standard length LS (mm)Sociability score
45 50
F. 1. Scatterplots showing the relationship between (a) standard length (LS), (b) boldness (the average pro-
portion of time out of cover during the risk-taking test) and (c) sociability (the average distance from the
compartment housing conspecics in the sociability test) and the total number of Chironomus sp. eaten
(n=94). Lines in plot (a) are predicted maximum food intake for the shyest ( ), intermediate ( )and
boldest individuals ( ).
individuals may be able to eat more due to a faster metabolism and digestion of food
in their stomach, therefore enabling them to empty part of their stomach more quickly.
Rapid digestion may especially be expected as the individual G.aculeatus had min-
imal stomach contents at the start of the experiment. All these explanations t the
‘performance model’ (Careau et al., 2008; Careau & Garland, 2012) and pace-of-life
theory (Réale et al., 2010), which suggests that an active, risky lifestyle is associated
with well-developed machinery for acquiring and processing food (Biro & Stamps,
2010), supporting the idea that boldness is linked to life-history strategies (Stamps,
2007; Wolf et al., 2007). These results are in line with the nding that bolder individ-
uals have higher metabolic rates (Huntingford et al., 2010), and that individuals with
higher metabolic rates show increased risk-taking after food deprivation (Killen et al.,
2011), as a larger ‘metabolic engine’ may come with higher maintenance costs (Biro
& Stamps, 2010). Bold compared to shy individuals were not simply more motivated
to feed because of having a larger LS, as the two were uncorrelated in this study, in line
with other studies on G.aculeatus (Bell & Sih, 2007; Jolles et al., 2015). As bolder
individuals are more likely to consume prey in a risky environment (Ioannou et al.,
2008), and foraging shes are less able to detect predators and predators more likely to
target foraging prey (Krause & Godin, 1996), it may be suggested that risk is an impor-
tant factor in the nding that bolder individuals had higher maximum food intake. This
possibility is not likely however, as food was provided on a feeding dish at the plant
cover, thus enabling individuals to eat while remaining concealed under cover. Fur-
thermore, individuals were inactive and tested in their small home compartment after
3 weeks of acclimation time. Also, G.aculeatus were given 30 min to nish a batch
of Chironomus sp. despite being able to nish it within seconds after provisioning (J.
© 2016 The Authors. Journal of Fish Biology published by John Wiley & Sons Ltd
on behalf of The Fisheries Society of the British Isles. 2016, doi:10.1111/jfb.12934

6J. W. JOLLES ET AL.
W. Jolles, pers. obs.). Future work could examine the link between boldness repeata-
bility and metabolism in more detail by assessing metabolite concentrations in the
water of individually housed shes (Killen et al., 2011, 2012), and investigate the
possibility that shyer individuals may compensate for lower food intake by showing
reduced activity.
In contrast to boldness, sociability was not linked to maximum food intake
[𝜒2=0⋅00; P>0⋅05; Table I and Fig. 1(c)]. This result was predicted, as sociability is
a personality trait that is not directly linked to energy production or metabolism. Never-
theless, it is likely that sociability has important indirect links to energy requirements.
For example, more sociable individuals may have higher hydrodynamic benets
(Herskin & Steffensen, 1998) related to their spatial positioning in moving shoals
(Jolles et al., 2015), but may also have higher energy needs due to lower potential
likelihood to discover food patches as well as scramble competition. This study is
one of the rst to test for an association between sociability and energetics (Careau
& Garland, 2012). Future work is required to further investigate the link between
sociability and energetics (Réale et al., 2010), which may help to better understand
the adaptive signicance of sociability variation.
The results presented here on the feeding rates of food-deprived G.aculeatus may
be helpful for future sh studies that are focused on foraging dynamics or aim to use
food reward paradigms, as they show that adult G.aculeatus are capable of eating up
to 36 Chironomus sp. on average, or 0⋅46 g in wet mass, in a relatively short time scale
(c. 1–3 h). Although no direct mass measurements were available, based on a large
number of LTand Mestimates of G.aculeatus it was calculated that individuals ate
roughly 32⋅0% of their body mass. This is very high considering that in the wild the
average daily food intake rates of G.aculeatus have been shown to range between c.
1⋅5 and 16⋅9% of their body mass (Beukema, 1968; Manzer, 1976; Rajasilta, 1980;
Allen & Wootton, 1984). This may for a large part be explained by the high wet mass
of the food, c. 80% for Chironomidae (Armitage et al., 2012). Ultimately, food intake is
limited by the capacity of a well-lled stomach, predicted to equal c.5⋅5% of body mass
(Beukema, 1968), and digestion rate, up to 15% stomach contents h−1(Rajasilta, 1980).
These results highlight that researchers studying personality traits and planning to use
food rewards, such as for investigating the stability of personality or learning effects,
should take into account that shy and bold shes show intrinsic feeding differences
irrespective of their body size.
In conclusion, individual G.aculeatus at rest varied considerably in their maxi-
mum food intake, even after accounting for body size. This variability correlated
positively with boldness but not with sociability, as predicted by individual differ-
ences in life-history strategies and growth– mortality trade-offs associated with these
personality traits.
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