Behavioral Ecology Vol. 13 No. 4: 439-442
© 2002 International Society for Behavioral Ecology
Individual variation in risk taking: the effect of a predatory threat on fighting behavior in Nannacara anomala
Department of Zoology, Division of Ethology, Stockholm University, 106 91 Stockholm, Sweden
Address correspondence to O. Brick. E-mail: brick{at}zoologi.su.se .
Received 27 March 2000; revised 12 June 2001; accepted 18 August 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The nature of fights in a species depends on the asymmetry in fighting ability of the contestants and the value of the contested resource. Animals of a population may also differ in their assessment of how dangerous it is to fight in relation to the risk of predation. To address this issue, we classified 36 males of the small South American cichlid fish, Nannacara anomala, according to how much each individual inspected a model predator in the presence of its own mirror image. We assigned each fish to either of two groups: bold (prone to inspecting) or cautious (averse to inspecting). We allowed bold and cautious dyads, matched for equal body weight within each dyad, to fight in the presence of the model predator. During these fights, there was no significant difference between the groups in inspection of the model predator, but bold dyads escalated significantly faster to mouth wrestling than cautious dyads. Bold dyads also performed significantly more low-intensity behavior (i.e., visual assessment and tail beating) compared to cautious dyads. Only two fights (22%) in the bold group and one fight (11%) in the cautious group had a clear winner. About 3 months later, the same dyads fought again without the model predator present. Both groups then decreased the time to reach mouth wrestling, but bold dyads still escalated significantly faster than cautious dyads to mouth wrestling. There was no significant difference in the use of low-intensity behaviors between groups. The results suggest that there are individual differences in the response toward predators among male N. anomala, which also correlates with the performance of fighting behavior when the animals' perceived risk of predation increases.
Key words: boldness, cichlids, contest, behavior, Nannacara anomala, predation risk.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The relationship between individual differences in boldness, defined as confidence in a novel situation or propensity to take risks, and behavioral variation is a research area of general interest because it occurs in a wide variety of animal taxa (Budaev, 1997
; Coleman and Wilson,
1998; Wilson et al.,
1993,
1994). Wilson and co-workers
(1993,
1994) showed that individuals
within populations of juvenile pumpkinseed sunfish (Lepomis gibbosus)
differ along a shyness-boldness continuum, which influences choice of diet,
risk of predation, and parasitic infection. However, few attempts have been
made to investigate to what extent individual differences in boldness may
explain observed patterns in specific behavior (e.g., aggressive behavior). In
a pivotal study, Huntingford
(1976; see also
Huntingford, 1982) found
consistent individual variation in intraspecific territorial aggressiveness in
three-spined sticklebacks (Gasterosteus aculeatus) during the
breeding season. The level of territorial aggression correlated with boldness
toward a predator outside the breeding season. The study provided evidence
that the same physiological mechanism regulates territorial aggression toward
conspecifics and boldness toward predators in sticklebacks. Theoretical
studies on fighting behavior show that the nature of fights should vary in
relation to differences in fighting ability between contestants and the value
of the contested resource (Austad,
1983; Enquist and Leimar,
1987; Grafen,
1987; Maynard Smith,
1982; Parker,
1974). Because the potential effect of differences in risk
assessment in relation to predation risk has been largely neglected so far,
both in the theory of optimal contest behavior and in most empirical studies
(but see Brick, 1998,
1999;
Jakobsson et al., 1995), the
aim of our study was to investigate the effect of predation risk on the choice
of behavior patterns in contests between dyads that differ in estimated
boldness in the South American cichlid Nannacara anomala. |
METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We used fish from a stock bred at Tovetorp Zoological Research Station in southeast Sweden. We housed the fish from approximately 6 weeks after hatching in 250-1 tanks. In November 1996, we isolated 36 individuals that were beginning to show male characteristics, one in each holding aquaria (30 x 30 x 30 cm). All aquaria contained a substrate of gravel (2-3 cm) and a clay flowerpot. The temperature was kept constant at 26°C and the light regime was maintained at 12:12 h light:dark. We fed the fish, which were sexually mature when tested, twice daily on live midge larvae. Thus, all specimens came from broods originating from our laboratory population and were of similar age and size. We defined boldness as the willingness of an individual fish to inspect a model predator in the presence of its own mirror image. Similar methods that we used to classify individuals as either bold or cautious have been used in other studies (e.g., Magurran and Girling, 1986
).
We housed the fish individually in their holding aquaria between all
treatments and subjected each male to the following pre-experimental
treatment.
Estimation of boldness
Between 11 April and 25 May 1997, when the fish were about 11 months old,
we moved each male from its holding aquarium to an experimental aquarium (60
x 30 x 30 cm) divided in half by an opaque, plastic partition with
a substrate of gravel. After approximately 24 h, we enclosed the male in a box
(10 x 4 x 4 cm). We took away the partition and introduced a model
pike (Esox lucius) predator (20 x 3.5 x 2.5 cm plastic
fishing lure made by Salmo). We placed the model predator with its head in the
middle of the aquarium and attached it with fishing line approximately 3 cm
above the gravel facing the box with the enclosed fish. Although N.
anomala will not encounter a pike in the wild, the model shares many
general characteristics of piscivorous predators native to the waters of
N. anomala, such as Crenicichla spp. Male N.
anomala also react to the pike model with the typical antipredator
behaviors shown toward live Crenicichla spp. (Brick and Jakobsson,
personal observations). We placed a mirror outside the aquarium at the side
opposite the box. Five minutes later, we slowly raised the box by remote
control to an upright position and the trial began. A male had to swim
approximately 60 cm to the other side of the aquarium, passing the model
predator, to be able to start interacting with its mirror image. We filmed the
males from behind a blind, and we recorded the duration of inspection bouts
toward the model predator for each fish. We defined inspection behavior as an
approach toward the model predator in a tentative manner while visually
fixating the model predator (e.g., Pitcher
et al., 1986). After the treatment, we returned the fish to its
holding aquarium. We analyzed the videotapes for 45 min.
Staging contests
To be able to investigate if estimated boldness covaries with performance
of contest behavior in N. anomala, we assigned males either to a bold
or to a cautious group according to how much they had inspected the model
predator. Roughly, the fish were of two types with respect to how much they
had inspected the model predator. The distribution of values suggests that the
variation is bimodal but not completely discontinuous. We assigned 14 fish
(39%) that inspected the model predator for more than 2 min to the bold group
(median: 3 min 56 s, range: 2 min 5 s-11 min 34 s). We assigned 14 fish (39%)
that inspected less than 10 s to the cautious group (median: 0 s, range: 0-7
s). The remaining eight fish (22%) inspected the model predator for 17, 17,
21, 46, 47, 49, 57 s, and 1 min 12 s, respectively. To avoid small sample
sizes, we randomly assigned these fish either to the bold or to the cautious
group. This procedure created some overlap between the two experimental groups
in estimated boldness. However, one group was biased toward bold individuals
(prone to inspecting, median: 3 min 24 s, range: 17 s-11 min 34 s, n
= 18), and one group was biased toward cautious individuals (averse to
inspecting, median: 0 s, range: 0-57 s, n = 18). In the bold group,
15 fish out of 18 interacted with their mirror image. In the cautious group,
five fish out of 18 interacted with their mirror image.
We staged contests between bold dyads and cautious dyads between 27 July
1997 and 20 January 1998. Approximately 2 months had passed since the
estimation of the fish boldness. We matched fish into dyads with only minor
asymmetries in relative body weight, thus only varying the degree of estimated
boldness between groups. Twenty-four hours before a contest, we moved a dyad
to the experimental aquarium (60 x 30 x 30 cm) divided in half by
an opaque, plastic partition. We placed the males one on each side of the
partition. Before the test, we enclosed each male in a box (10 x 4
x 4 cm), took away the partition, and introduced the model pike
predator. Five minutes later, we slowly raised the box by remote control to an
upright position and the trial began. After the trial, we returned each fish
to its original holding aquarium. None of the fish suffered any physical
damage during the fight. We videotaped the contests from behind a blind and
recorded the duration of lateral display, the number of tail beats, and time
to the onset of mouth wrestling and the time the fish inspected the model
predator. We analyzed the first 45 min, after which little happened. Enquist
and Jakobsson (1986) give a
detailed description of the fighting behavior of N. anomala.
Observations from populations in large tanks suggest that a male tries to
dominate a territory containing several females, which defend spawning
grounds. The dominant male will court the females and attack other males if
they try to court. A dominant male will challenge any unfamiliar male.
To investigate the effect of predation risk on fighting behavior of dyads that differ in estimated boldness, the dyads first interacted in the presence of the model predator (predator-present treatment). To investigate the effect of the first contest on later contest behavior in bold and cautious dyads, each dyad interacted a second time without the model predator present (predator-absent treatment). Approximately 3 months passed between the predator-present and predator-absent treatments. Thus, the fish have the same experience of predation risk and potentially the same experience of agonistic interactions throughout the experiment. Only estimated boldness differs between the two groups. Because the order of the sequence is not balanced in order to avoid small sample sizes, it was not possible to establish the exact effect of differences in estimated boldness on fighting behavior. However, the design made it possible to evaluate the effect of perceived predation risk on fighting behavior in fish that differ in estimated boldness.
In the predator-present treatment, we used nine bold dyads and nine cautious dyads. In the predator-absent treatment, we used nine bold dyads and eight cautious dyads. The sample size in the predator-absent treatment is smaller because of a technical failure in one trial. The weight asymmetries in dyads did not differ significantly between the two groups (mean ± SE; predator present: bold, 3% ± 1%, cautious, 3% ± 1%, t test for independent samples, t16 = -0.019, p =.98; predator absent: bold, 12% ± 3%, cautious, 7% ± 2%, t test for independent samples, t15 = 1.35, p =.20). There was no significant difference in absolute weight of fish between the two groups (mean ± SE; predator present: bold, 5.6 g ± 0.4 g, cautious, 5.9 g ± 0.2 g, t test for independent samples, t34 = -0.6, p =.53; predator absent: bold, 6.1 g ± 0.4 g, cautious 6.6 g ± 0.2 g; t test for independent samples, t32 = -1, p =.31).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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First treatment, predator present
Dyads assigned to the bold group escalated significantly faster to mouth wrestling compared to the dyads assigned to the cautious group (Gehan's generalized Wilcoxon test for censored time series: test statistic = -2.14, p =.03, Figure 1). There was no significant difference between the two groups in the duration of inspection of the model predator (bold, median 99 s, range 4-187 s; cautious, median 33 s, range 0-108 s, Mann-Whitney U test, U = 27, p =.23, power, 34%,
=.05). The number of fights escalating to
mouth wrestling during the experimental time (45 min) was seven (78%) in the
bold group and three (33%) in the cautious group. Bold dyads performed
significantly more visual assessment and tail beats compared to cautious dyads
(t test for independent samples, t16 = 2.8,
p =.01; Figure 2). Two
fights (22%) in the bold group and one (11%) in the cautious group had a clear
winner within the experimental time.
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Second treatment, predator absent
Bold dyads escalated significantly faster to mouth wrestling compared to
the cautious dyads also when there was no predator stimuli (Gehan's
generalized Wilcoxon test for censored time series: test statistic = -2.5,
p =.014; Figure
1).
The number of fights escalating to mouth wrestling was nine (100%) in the bold group and six (75%) in the cautious group. There was no significant difference in the use of visual assessment and tail beating during the 45 min comparing the two groups (t test for independent samples, t15 = 0.12, p =.90; Figure 2). Six fights (67%) in the bold group and two (25%) in the cautious group had a clear winner. The bold dyads reduced their use of low-intensity behaviors compared to predator-present treatment, while cautious dyads maintained their use of low-intensity behaviors (Table 1 and Figure 2). Both bold and cautious dyads escalated significantly faster to mouth wrestling in the predator-absent treatment compared with predator-present treatment (Table 1 and Figure 1).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Our study shows that estimated boldness, defined as the willingness to inspect a model predator, covaries with the performance of contest behavior in N. anomala. Bold dyads fought significantly more compared to the cautious dyads in the presence of the model predator. This difference was already evident during the estimation of the fishes' boldness. Fifteen out of 18 fish in the bold group interacted with their mirror image, whereas only five out of 18 did so in the cautious group. The amount of inspection during the predator-present treatment did not differ significantly comparing the bold with the cautious group, although the power of the analysis was low. Still, the maintained level of inspection of the model predator in the bold group suggests that bold fish still regarded the model as dangerous.
Bold dyads also escalated significantly faster to mouth wrestling compared to cautious dyads in the predator absent treatment. This significant difference could partly be due to carryover effects. Cautious fish were reluctant to engage in fighting during the first contest when the model predator was present. This may have influenced the nature of the fight during the predator-absent treatment. Bold dyads, in contrast, engaged in fighting during the first contest, which may have influenced the willingness to escalate the fight during the second contest. The difference between bold and cautious fish during the second contest would then be more pronounced than what it would have been if the sequence of fights had been reversed.
According to the sequential assessment game (Enquist and Leimar,
1983,
1987;
Leimar and Enquist, 1984),
fights should precede in a stepwise manner, with each step giving a more
accurate estimate of relative fighting ability. Empirical studies have
supported the sequential assessment game model, but the model does not predict
some of the variation. For example, there is temporal overlap between
different behavior patterns in cichlid fights; the contestants abandon a
behavior of higher intensity for a behavior of lower intensity (e.g., mouth
wrestling is replaced by tail beating)
(Enquist et al., 1990;
Koops and Grant, 1993). This
could be due to the fact that individual animals differ in what behavior
element they prefer to use (Leimar,
1988). The difference becomes evident when the animals' perceived
risk of predation increases as in the present study. Fish classified as
cautious were reluctant to engage in fighting when there was an increased risk
of predation. If a population consists of more or less bold and more or less
cautious individuals and they randomly engage in contests, we would expect an
intermediate distribution of time to mouth wrestling and an increased
variation in the use of low-intensity behavior compared to an entirely bold or
an entirely cautious group. The extensive use of low-intensity behavior in the
bold group instead of escalating to mouth wrestling when the predator was
present could be interpreted as a way for the animals to compensate for the
increased risk of predation. Previous studies have shown that N.
anomala reduces vigilance during escalated fighting but is able to
maintain vigilance during low-intensity agonistic behaviors
(Jakobsson et al., 1995).
The significant difference between bold and cautious fish found in the
present study suggests that the competitive advantage of bold and cautious
fish covary with local predation risk. Potentially, bold fish may have a
competitive advantage over cautious fish under low predatory conditions and
vice versa. Barlow and co-workers
(1986) found that aggressive
behavior in Midas cichlids toward a model conspecific could predict the winner
in fights where both contestants had little information about the territory
(dare contests). In these fights, relative size played no role. In fights
where both contestants had prior information about the territory and appeared
to regard the territory as their own (prowess contests), size was the chief
determinant of the outcome of fights. Huntingford's
(1976) study and the present
study have shown that estimated boldness toward a predator correlates with
performance of agonistic behavior. These findings may contribute to the
understanding of the outcome of dare contests in Midas cichlids (see
Barlow et al., 1986). Bolder
fish may respond faster to or disregard the threats of an unfamiliar
environment to a larger extent and may have an advantage, regardless of size,
in fights with individuals that are more cautious. If this proves to be the
case, the different response of fish to the threat from a predator is likely
to influence the strength and nature of sexual and natural selection in
habitats with different predation risk regimes.
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ACKNOWLEDGEMENTS |
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We thank Olle Leimar for discussions leading to this study and for comments on the manuscript. We thank Björn Birgersson, Magnus Enquist, Tomaso Pizzari, Jörgen Johnsson, and three anonymous referees for comments on the manuscript. We thank Lena Timan for collecting data on boldness and Nils Andbjer, Anders Bylin, and Susanne Strömberg for animal care.
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