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


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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.
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Journal of Fish Biology (2016)
doi:10.1111/jfb.12934, available online at
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:
© 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.
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 306 to 525 cm (mean ±.. =407 ±004 cm).
Mass (M) was estimated from total length (LT; mean ±.. =513 ±005 cm) based
on LTand Mrelationship data from G.aculeatus extracted from www.
using the formula M=aL
Tb(a=00068, describes body shape and condition;
b=328, 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 056 to 302 g
(mean ±.. =150 ±005 g). After photographing, individuals were solitary housed
in compartments (185cm×95 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
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;, 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 ±.. 279±14% of their time out of cover (range: 00–628%) during
the boldness test and were at mean ±.. 479±23 mm from the compartment
housing conspecics (range: 130–1160 mm) during the sociability test. As indi-
vidual G.aculeatus (n=96) were repeatable in the time they spent out of cover
(rs=041, P<0001) and in their average distance from the shoal compartment
(rs=050, P<0001), 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=000, P>005) and
neither personality trait correlated with LS(rs=011, P>005; rs=010, P>005,
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 ±.. =127±04 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
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) 005 000 9303 <0001
Boldness 035 013 731 <001
Sociability 000 000 000 >005
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 ±.. =361±11). LSwas the strongest predictor of food intake, with
larger individuals eating signicantly more Chironomus sp. [P<0001; Table I and
Fig. 1(a)], although relative food intake in terms of percentage body mass dropped with
M(rs=−043, P<0001). 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<001; Table I and Fig. 1(b)].
Keeping LSconstant at the average LS(407mm), the shyest and boldest individuals
were predicted to still vary up to 20% in their food intake [322 and 401Chironomus
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
(a) (b)
60 60
25 50 75 100
0·0 0·2
Boldness score
0·4 0·6
Total number of worms eaten
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
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=000; P>005; 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 046 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 320% 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.
15 and 169% 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.55% of body mass
(Beukema, 1968), and digestion rate, up to 15% stomach contents h1(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
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... The data also indicated that, although there were differences between the treatments, boldness seemed to be more related with activity, exploration, and distance; while sociability remained aside. Accordingly, previous studies could not relate boldness and sociability (Bevan et al., 2018;Cote et al., 2011;Jolles et al., 2016). ...
... Bigger fish were bolder, less social, and explored the new object more. Overall, bolder individuals are expected to be bigger naturally because they can deal with opponents better and subsequently obtain more sustenance (Conrad et al., 2011;Jolles et al., 2016). As they were bolder, they would likely explore the new object more in comparison to shyer individuals. ...
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Tramadol is a widely used analgesic with additional antidepressant and anxiolytic effects. This compound has been reported in continental waters reaching concentrations of µg/L as a consequence of its inefficient removal in sewage treatment plants and increasing use over time. In this study, European chubs (Squalius cephalus) were exposed to 1 µg/L of tramadol in water for 42 days with a subsequent 14 days of depuration. Our results revealed that chubs exposed to this analgesic underwent changes in their behaviour as compared to the control group. The behavioural outcome was also influenced by the individual concentration of tramadol in brain tissue. In particular, experimental fish presented anxiolytic-like effects, characterized by less bold and less social individuals. Exposed animals were less frequently out of the shelter and moved a shorter distance, indicating that they explored the new environment less during the boldness test. In the novel object recognition experiment, although they distinguished the new item, they examined it less and displayed a reduced activity. Shoal cohesion was disrupted as observed in an increased distance between individuals. After the depuration phase, this alteration remained whereas the boldness effect disappeared. Moreover, the degree of behavioural changes was correlated with the concentration of the substance in brain. According to our findings, chronic presence of tramadol in the environment can impact the fitness of exposed aquatic fauna by altering evolutionary crucial behaviours.
... For example, in juvenile Atlantic salmon (Salmo salar), individuals with increased SMR tend to forage outside of covered areas more often and are thus able to attain higher rates of feeding. Bolder sticklebacks have also been observed to have higher overall food consumption as compared to shier individuals (Jolles et al., 2016). In contrast, larvae of many fish species decrease foraging under Fig. 1 Components of a typical foraging cycle in fish, beginning with the onset of searching for prey and ending with prey consumption. ...
... Bolder individuals probably spend more time outside shelters to search for food Fig. 4 Box plots for the change in the rate of mirror attack (postexperience rate -pre-experience rate) for test fish with better (CAbetter) and worse (CA-worse) competitive abilities that were given winning (W), losing (L) or no-contest (N) experiences (n = 28 for each of the bars). Boxes indicate the inter-quartile range (IQR), with the central line depicting the median and the whiskers extending to 1.5 × IQR, and outliers (Jolles et al. 2016), which supplies more fuel to produce the energy needed for raising aggressiveness. Interestingly, preexperience aggressiveness was negatively associated with the change in aggressiveness after experience treatments. ...
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Many animals raise and lower aggressiveness after recent wins and losses, respectively. Individuals that differ in internal/external conditions could also differ in their responsiveness to winning and/or losing experiences. Personality traits have been suggested to have close links with an individual’s responsiveness to environmental stimuli. Whether the responsiveness to winning-losing experiences is related to personality traits, however, remains unclear. Using a mangrove killifish, this study tested the hypothesis that personality traits (aggressiveness and boldness) and responsiveness to winning/losing experiences are linked because of their common associations with competitive ability. We also measured oxygen consumption rates to evaluate the importance of energy supply to the responsiveness. The results showed that aggressiveness, but not boldness or oxygen consumption rate, was associated with competitive ability and affected by winning/losing experiences. The fish’s responsiveness to winning-losing experiences was dependent only on competitive ability, but not aggressiveness or boldness; individuals with better (instead of worse) competitive abilities showed greater decreases in aggressiveness in response to losing experiences. The strong signals from multiple losing experiences together with worse competitors also exhibiting low aggressiveness (floor effects) may have given rise to these unpredicted results. Furthermore, (1) aggressiveness, boldness and oxygen consumption rate were positively correlated both before and after experience treatments and (2) individuals that were bolder or had higher oxygen consumption rates had higher increases in aggressiveness after experience treatments, consistent with the notion that individuals that are able to pay high metabolic costs can afford to behave boldly and aggressively and to raise aggressiveness further. Significance statement To adapt to changing environments, animals often show plasticity in behaviours. Personality traits have been suggested to have close links with responsiveness, such that bolder and more aggressive individuals are less responsive to environmental stimuli. Using a mangrove killifish, our study showed that aggressiveness and boldness did not affect whether or how the fish responded to recent wins or losses. Competitive ability, however, played an important role; better competitors had greater decreases in aggressiveness after losing experiences, contrary to our expectations. These results together with the results of previous studies of the fish suggest that the fish’s responsiveness to winning-losing experiences could be sensitive to its internal conditions, the strength of the stimuli and potential floor/ceiling effects. This study also showed that individuals that are able to pay high metabolic costs are able to behave boldly and aggressively and to raise aggressiveness further.
... The dietary condition varied strongly between individuals. The amount of consumed prey depends on the boldness of the individual (Jolles et al., 2016) and on the response time an individual needs to approach a detected prey item (MacGregor et al., 2020). The foraging success of schooling three-spined sticklebacks depends on the group organization (MacGregor et al., 2020). ...
... BI are inclined to run and are more exploring and adventurous, so their behaviors are more sensitive and mobile to a new environment. Moreover, BI have a higher feeding tendency, and are found to be more likely to find food (Ioannou et al., 2008;Jolles et al., 2016). Our results are consistent with other evidence that BI are prone to adapt to and explore new environments quickly, while SI are more likely to retreat or become cautious (Wilson and McLaughlin, 2007). ...
In farmed animals, individuality have demonstrated links to performance traits, health and disease susceptibility, and animal welfare. This research aimed at exploring whether there are differences in the secretion of hormones in the caudal neurosecretory system of different individuailty, and investigating whether it is related to physiological behaviors. In the experiment we selected through multiple behavioral tests two types of olive flounders, bold individuals (BI) and shy individuals (SI), and found that they differed in behavior and physiology. The standard metabolic rate, maximum metabolic rate, and absolute aerobic scope of BI were markedly higher than those of SI. Additionally, the swimming speed of BI was also higher than that of SI in the natural photoperiod. BI and SI showed distinct coping styles to deal with acute stress. Overall, the number of Dahlgren cells secreting UI, the relative UI and CRH mRNA expression in the caudal neurosecretory system (CNSS) of SI was relatively higher than that in BI. By contrast, the number of Dahlgren cells secreting UII and the mRNA expression of UII is lower than that of BI. Through the correlation analysis, it was found that there are some differences in hormone secretion among different individuality groups, which indicates individuality affects hormone production and the number of secretion cells and existed correlation with respiratory metabolism, spontaneous behavior, appetite. It means differences in the regulation mechanism of the flounders in BI and SI.
... Based on the results and experimental set-up, the authors cannot determine why sea bass ignored the glass eels. Different personalities, such as shy or bold individuals among the test fish (Jolles et al., 2016;Sih et al., 2015), may explain different responses to the experimental setup. Although based on significantly different behaviour (latency and grid change) between the two groups, stress might be the crucial factor in ignoring the glass eels. ...
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Barriers in the estuaries of the rivers prevent the immigration of glass eels (Anguilla anguilla) arriving on the European coast every spring. This leads to an unnatural accumulation of migrating glass eels below the barriers and this may lead to additional losses in glass eels by piscivorous fish. The proportion of predation losses can be estimated using mark-recapture techniques and abundance estimates in combination with stomach content analysis of piscivorous fish. However, whether tagging transparent glass eels increases predation risk and what the digestion rate of glass eel is in piscivorous fish are unknown. This study aimed to determine whether there is an increased predation risk for tagged glass eel; it also studies glass eel digestion status in piscivorous fish after appointed time frames. A laboratory experiment with 48 trials was conducted. Tagged (Visible Implanted Elastomer, VIE) and untagged glass eels were exposed to small (19.1-24.4cm) and large (31.9-43.5cm) sea bass (Dicentrarchus labrax) during a 2-hour trial. In 48% of the trials successful predation was present and 13% showed clear predation attempts in which bass did not capture glass eels. No significant difference was found in predation rate between tagged and untagged glass eels and between red and blue tagged glass eels. Large sea bass predated more, but all sizes consumed glass eel under laboratory conditions. Stomach content analysis showed intact glass eel bodies 4-6 hours after ending the 2-hour trial and parts of glass eel bodies up to 16-18 hours. This study showed that tagging does not increase predation in mark-recapture studies using VIE-tags in transparent glass eel. It also shows that the proportion of predation in relation to local glass eel abundance can be estimated if stomach content analysis is conducted within 4-6 hours after predation. This article is protected by copyright. All rights reserved.
... bold vs shy) (Mittelbach et al., 2014;Wolf and McNamara, 2012). Bold individuals (BI) are willing to explore novel environments, exhibit a higher tendency to food intake and have higher social rank, whereas shy individuals (SI) are more reclusive and show lower food tendency especially under stress situations (Jolles et al., 2016;Sneddon, 2003;Yuan et al., 2018). Except for the behavior, links between the animal individuality and physiological process have also been studied previously. ...
Animal individuality is proposed to describe individual differences in behavior. Individuals may exhibit consistent differences in behavioral traits within a population, and these traits are heritable. It has also been known that animal individuality can be attributed to both genetic and environmental effects. We previously observed the presence of bold individuals (BI) and shy individuals (SI) in olive flounder (Paralichthys olivaceus). However, the individuality distribution and the behavioral phenotype of offspring with different individualities remain unclear. In this study, the temperature and acidity challenges of larvae at 25 days-post-hatch (DPH) and juvenile (50 DPH) of bold and shy flounder offspring were investigated at pH = 7.3, 7.7, 8.1 and temperature at 4, 18, 28 °C. On 25 DPH, bold offspring (BO) showed higher survival rates with acidity at pH = 7.3 and 4 °C challenge. Three behavioral phenotypes (bold, middle and shy individuals, BI, MI and SI) were observed in both juvenile (8 MPH) bold and shy flounder offspring. The percentage of SI offspring from the shy maternal line (SS) was higher than BI offspring from the bold maternal line (BB) (0.75 vs. 0.58). BI from both BO (BB) and SO (SB) were more motivated to feed and active during net confinement than SI (BS and SS). Furthermore, BB and SB exhibited higher metabolic rates and actively responded to predator stressor, while BS and SS showed a divergent tendency. However, the metabolism of the offspring seemed to be partially affected by their maternal line. Taken together, our study indicates that screening of animal individuality in population would improve animal welfare and increase the output efficiency of flounder in aquaculture.
An animal’s behavioural traits can influence the outcomes of ecological interactions within their food-web, including what they eat, their vulnerability to predation and who they compete with. Despite this, few studies have directly measured links between among-individual behavioural and trophic variation. Invasive species like the round goby (Neogobius melanostomus) are often found to have consistent among-individual differences in behaviour within and between populations across their invasion front. Therefore, an individualized approach to invasive populations and their ecological interactions may be valuable to understanding how their impacts on recipient ecosystems. Using non-lethal methods to measure trophic variation (i.e., stable isotope analysis via fin clips) and passive individual tagging, we analysed behavioural trait/personality variation and trophic variation to explore links between the two. Focusing on an established population of round gobies in Guldborgsund strait in the southwest Baltic Sea, we found significant among-individual variation in bold-exploratory traits in novel environment and refuge emergence assays. We also found strong intraspecific trophic variation, with particularly high variation in carbon-12 – carbon-13 (δ13C) suggesting that individual round gobies differ in what are feeding on and/or where they forage. Diet reconstruction results support previous studies showing that gastropods and bivalves are major contributors to their diet, but the large differences in isotope values suggest that individual variation influences how they interact with prey communities. There were few links between behavioural and trophic variation, nonetheless this study shows that measuring behavioural-trophic links is a viable approach for exploring the role of behavioural traits in individual-level ecological variation.
Animals can gain large benefits from living in groups but must coordinate with their groupmates in order to do so. Social interactions between groupmates drive overall group coordination and are influenced by the characteristics of individual group members. In particular, consistent inter-individual differences in behaviour (e.g. boldness) and familiarity between individuals in groups profoundly affect the individual interactions that mediate group coordination. However, the effects of boldness and familiarity have mostly been studied in isolation. Here we describe how familiarity and boldness interact to affect individual performance, leadership, and group coordination in small shoals of three-spined sticklebacks (Gasterosteus aculeatus) solving a novel foraging task. Groups of higher average boldness were less cohesive, but only when group members were familiar with one another. Familiarity affected shy and bold individuals’ foraging performance and leadership tendencies differently depending on group characteristics: the shyest group member experienced declining foraging success and leadership with increased group boldness in familiar groups, but experienced the opposite effect on foraging and no effect on leadership in unfamiliar groups. The boldest group member, in contrast, exhibited the opposite pattern: leading and eating more with increasing group boldness in familiar groups, but eating less with increasing group boldness in unfamiliar groups. These results suggest that both boldness and familiarity are important for establishing group behaviour and coordination, and that consistent inter-individual differences in behaviour may primarily impact group coordination once familiarity has been established.
Ecological research demonstrates how intraspecific phenotypic variation can have consequences for community dynamics. However, the effects of animal personalities (i.e., intraspecific behavioral variation) on ecological processes remains relatively understudied. Using Red-backed Salamanders (Plethodon cinereus) and the detrital food web as a model system, we conducted a laboratory mesocosm experiment to explore whether or not the personality type of a top-level predator could affect the community structure within a complex, terrestrial food web. We used behavioral assays to investigate the repeatability of salamander behaviors, and classified individuals as either active or inactive. We then subjected laboratory mesocosms to one of four treatments for 3 mo: one active salamander, one inactive salamander, control (no salamander), and a pre-experimental reference. Our results indicate that the effect of P. cinereus on the detrital food web might be behaviorally mediated, with only the most active salamanders affecting community structure. Specifically, mesocosms housing active salamanders contained less diverse invertebrate communities than all other treatments. This difference was primarily driven by springtails, which were more abundant within mesocosms housing active salamanders. We also found that salamander personality was associated with cover board use inside mesocosms, with inactive salamanders exhibiting a more philopatric use of cover objects than active individuals. Leaf-litter degradation did not differ between treatments, indicating that the ecological effects of salamanders were too weak to influence basal resources within the detrital food web. Our study prompts further questions regarding the potential for animal personalities to influence ecological processes within terrestrial communities.
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Social animals must time and coordinate their behaviour to ensure the benefits of grouping, resulting in collective movements and the potential emergence of leaders and followers. However, individuals often differ consistently from one another in how they cope with their environment, a phenomenon known as animal personality, which may affect how individuals use coordination rules and requiring them to compromise. Here we tracked the movements of pairs of three-spined sticklebacks, Gasterosteus acu- leatus, separated by a transparent partition that allowed them to observe and interact with one another in a context containing cover. Individuals differed consistently in their tendency to approach their partner's compartment during collective movements. The strength of this social attraction was positively correlated with the behavioural coordination between members of a pair but was negatively correlated with an individual's tendency to lead. Social attraction may form part of a broader behavioural syndrome as it was predicted by the boldness of an individual, measured in isolation prior to the observation of pairs, and by the boldness of the partner. We found that bolder fish, and those paired with bolder partners, tended to approach their partner's compartment less closely. These findings provide important insights into the mechanisms that govern the dynamics and functioning of social groups and the emergence and maintenance of consistent behavioural differences.
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The emergence of leaders and followers is a key factor in facilitating group cohesion in animals. Individual group members have been shown to respond strongly to each other’s behavior and thereby affect the emergence and maintenance of these social roles. However, it is not known to what extent previous social experience might still affect individual’s leading and following tendencies in later social interactions. Here, by pairing three-spined sticklebacks (Gasterosteus aculeatus) with 2 different consecutive partners, we show a carryover effect of a previous partner’s personality on the behavior of focal individuals when paired with a new partner. This carryover effect depended on the relative boldness of the focal individual. Relatively bold but not shy fish spent less time out of cover and led their current partner less if they had previously been paired with a bolder partner. By contrast, following behavior was mainly influenced by the personality of the current partner. Overall, the behavior of relatively bold fish was more consistent across the stages, whereas shy fish changed their behavior more strongly depending on the current context. These findings emphasize how the history of previous social interactions can play a role in the emergence and maintenance of social roles within groups, providing an additional route for individual differences to affect collective behavior.
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Foraging in animals is often associated with characteristic body postures, such as the head-down posture. When foraging conflicts with the ability to detect predators or to flee, individuals may incur a greater risk of mortality to predation than otherwise. Here we investigate the influence of different foraging postures (horizontal versus nose-down body posture) on the ability of individuals to respond to approaching predators and on the risk of mortality to predation in the guppy (Poecilia reticulata). Individuals engaged in nose-down foraging were assumed to be able to visually scan a smaller area for predators and to escape less effectively due to their body posture, and thus are more vulnerable to stalking predators than horizontally foraging ones. In a first experiment, we separately exposed nonforaging, horizontally foraging, and nose-down foraging guppies to an ap- proaching cichlid fish predator model. Nonforaging guppies reacted sooner to and initiated flight further away from die approaching model than did foraging fish collectively, and horizontally foraging individuals responded sooner to the model than nose-down foraging ones. Comparing all test guppies, nose-down foraging individuals were die most likely not to exhibit any response to the predator model. When presented with a simultaneous choice of two guppies behind a one-way mirror, individual blue acara cichlid (Aequidens pulcher), a natural predator of the guppy, preferred to attack foraging guppies over nonforaging ones and nose-down foraging guppies over horizontally foraging individuals. In a final experiment with free- swimming cichlids and guppies, we demonstrated that individual risk of predation for guppies foraging nose down was greater than for guppies foraging horizontally, and both were at greater risk than nonforaging guppies. This latter result is consistent with the above differences in the guppy's responsiveness to approaching predators depending on dieir foraging behavior, and with the finding that cichlid predators preferred fish that were less likely to show any response to them. Our results therefore indicate that die ability to respond to approaching predators and the risk of mortality to predation in the guppy is strongly influenced by their foraging activity, and in particular their foraging posture, and that cichlid predators preferentially select less wary and more vulnerable guppies. Key words: cichlid fish, fleeing, foraging, foraging posture, guppy, Poecilia reticulata, predation risk. (Behav Ecol 7:264-271 (1996))
An exciting area in behavioural ecology focuses on understanding why animals exhibit consistent among-individual differences in behaviour (animal personal-ities). Animal personality has been proposed to emerge as an adaptation to individual differences in state vari-ables, leading to the question of why individuals differ consistently in state. Recent theory emphasizes the role that positive feedbacks between state and behaviour can play in producing consistent among-individual covari-ance between state and behaviour, hence state-dependent personality. We review the role of feedbacks in recent models of adaptive personalities, and provide guidelines for empirical testing of model assumptions and predictions. We discuss the importance of the me-diating effects of ecology on these feedbacks, and pro-vide a roadmap for including state–behaviour feedbacks in behavioural ecology research. State–behaviour feedbacks and the emergence of personality differences The past decade has seen tremendous interest in animal personalities [1–3], stemming from accumulating evidence for individual repeatability and significant correlations between various behaviours (e.g., boldness, aggres-siveness, activity, exploration, or sociability). Empirical studies show that animal personalities and behavioural syndromes (correlations across contexts) vary as a function of ecology [4,5]; for example, aggressiveness and boldness are often positively correlated but the strength of this correlation varies depending on the predation regime [6,7]. Variation in syndrome structure also exists across different temporal scales; for instance, early experiences (e.g., exposure to stressors) can have large effects on the development of personality structure but such effects can
A Bayesian hierarchical approach is presented for the estimation of length-weight relationships (LWR) in fishes. In particular, estimates are provided for the LWR parameters a and b in general as well as by body shape. These priors and existing LWR studies were used to derive species-specific LWR parameters. In the case of data-poor species, the analysis includes LWR studies of closely related species with the same body shape. This approach yielded LWR parameter estimates with measures of uncertainty for practically all known 32 000 species of fishes. Provided is a large LWR data set extracted from, the source code of the respective analyses, and ready-to-use tools for practitioners. This is presented as an example of a self-learning online database where the addition of new studies improves the species-specific parameter estimates, and where these parameter estimates inform the analysis of new data.
A perplexing new question that has emerged from the recent surge of interest in behavioural syndromes or animal personalities is – why do individual animals behave consistently when behavioural flexibility is advantageous? If individuals have a tendency to be generally aggressive, then a relatively aggressive individual might be overly aggressive towards offspring, mates or even predators. Despite these costs, studies in several taxa have shown that individuals that are more aggressive are also relatively bold. However, the behavioural correlation is not universal; even within a species, population comparisons have shown that boldness and aggressiveness are correlated in populations of sticklebacks that are under strong predation pressure, but not in low predation populations. Here, we provide the first demonstration that an environmental factor can induce a correlation between boldness and aggressiveness. Boldness under predation risk and aggressiveness towards a conspecific were measured before and after sticklebacks were exposed to predation by trout, which predated half the sticklebacks. Exposure to predation generated the boldness–aggressiveness behavioural correlation. The beha-vioural correlation was produced by both selection by predators and behavioural plasticity. These results support the hypothesis that certain correlations between behaviours might be adaptive in some environments. Behavioural correlations are difficult to explain because behavioural flexibility is advantageous (Sih et al. 2004a). For example, if individuals have a tendency to be generally aggressive, then a relatively aggressive individual might be overly aggressive towards offspring (Wingfield et al. 1990; Ketterson & Nolan 1999), mates (Johnson & Sih 2005) or even predators (Sih et al. 2004a). Despite these costs, studies in several taxa have shown that individuals that are more aggressive are also relatively bold (Huntingford 1976; Hedrick & Riechert 1989; Riechert & Hedrick 1990; Bell 2005; Johnson & Sih 2005). However, the behavioural correlation is not universal, even within a species: popula-tion comparisons (Bell 2005; Dingemanse et al. in press) have shown that sticklebacks from populations that are under strong predation pressure behave consistently towards predators and conspecific competitors, but their counterparts from safe environments do not. One possible reason why there is a behavioural correla-tion in high but not low predation populations could be that predators favour the correlation between boldness and aggressiveness via correlational selection. Correlational selection occurs when certain combinations of traits are favoured over others, such that the fitness of one trait depends on the value of other traits (Lande & Arnold 1983; Brodie et al. 1995; Svensson et al. 2001). For example, correlational selection favours certain combinations of colour patterns and escape behaviours in garter snakes (Brodie 1992). As both behavioural reactions to predators (Tulley & Huntingford 1987; Huntingford et al. 1994) and to conspecifics (Bakker 1986) are partly heritable in stickle-backs, a response to natural selection by predators might have produced the correlation in high predation
INTRODUCTIONThe undulatory movements of a swimming fish generate thrust-type vorticesshed into the wake (Rosen, 1959; Mu ller et al., 1997). These vortices may aVectthe locomotor eYciency of a trailing fish depending on mutual positions (Breder,1965). Several studies have dealt with hydrodynamic interactions of schoolingfish as a possible energy conserving mechanism (Breder, 1965; Belyayev & Zuyev,1969; Zuyev & Belyayev, 1970; Weihs, 1973, 1975; Partridge & Pitcher, 1979;Partridge et...