Behavioral Ecology Vol. 10 No. 5: 557-566
© 1999 International Society for Behavioral Ecology
Foraging among cannibals and kleptoparasites: effects of prey size on pike behavior
Department of Animal Ecology, Lund University, Lund, Sweden
Address correspondence to A. Nilsson, Ecology Building, SE-223 62 Lund, Sweden. E-mail: anders.nilsson{at}zooekol.lu.se .
Received 9 December 1998; revised 26 January 1999; accepted 15 February 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The northern pike (Esox lucius) is an important and selective piscivore that chooses smaller prey than predicted from energy / time budgets. In a laboratory experiment, we investigated pike predatory behavior to explain this selectivity. Northern pike feeding on different prey sizes in aquaria were observed when foraging alone, when in the presence of chemical cues from similar-sized or larger conspecifics, and when in the presence of conspecifics that were allowed to interact with the focal pike. The results show that prey handling time increases with prey size and that the duration of manipulating and handling prey inflicts a risk of exposure to cannibals and kleptoparasites on the pike. Therefore, the risk of falling victim to cannibals or kleptoparasites increases with prey size. Attracting and experiencing intraspecific interactors can be regarded as major fitness costs. Chemical cues from foraging conspecifics have only minor effects on pike foraging behavior. Furthermore, the ability to strike and swallow prey head first improves pike predatory performance because failing to do so increases handling time. Our findings emphasize the increasing potential costs with large prey and explain previous contradictory suggestions on the underlying mechanisms of behavior, selectivity, and trophic effects of northern pike predation.
Key words: cannibalism, Esox lucius, foraging, kleptoparasitism, northern pike, predation, trade-offs.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Foraging and avoiding predation may act as conflicting demands (e.g., Sih, 1980
). Although any
forager should maximize its energy intake, predation may indirectly or
directly decrease foraging efficiency and therefore lifetime fitness in the
forager (Lima and Dill, 1990).
Foragers under the risk of predation should adjust habitat use, diel activity,
or diet, for example, to minimize reductions in fitness (e.g.,
Godin, 1990;
Hughes, 1997;
Lima and Dill, 1990;
Mittelbach, 1986). Predators,
too, may be subject to predation threat, and if prey selection affects
predation risk, predators should choose prey that minimize risk
(Gilliam, 1990).
In many predators, intraspecific predation, or cannibalism, is an important
mortality factor that acts as a density-dependent population regulator
(Elgar and Crespi, 1992;
Fox, 1975;
Polis, 1981). Cannibalism may
affect population densities and year-class strength through direct, lethal
effects, but it may also have indirect, behavioral effects such as changes in
habitat use or activity patterns (e.g.,
Smith and Reay, 1991).
Cannibalism may occur at different life stages, from eggs to adults, and
between siblings or nonrelated individuals. It has also been shown that the
frequency of cannibalism is dependent on factors such as population density,
hunger level, and availability of alternative prey
(Polis, 1981;
Smith and Reay, 1991). Another
interaction that may be important among predators is kleptoparasitism (i.e.,
the stealing of food items from other foragers). The prevalence of
kleptoparasitism depends on a number of factors, including, for example, size
or dominance differences between foragers, prey size and abundance, forager
group size, host aggregation, and risks or costs involved with the behavior
(e.g.,
Bélisle,
1998; Cangialosi,
1991; Elgar, 1989;
Higgins and Buskirk, 1998;
Hockey and Steele, 1990;
Whitehouse, 1997). Both
cannibalism and kleptoparasitism are taxonomically widespread behaviors that
impose risks and costs on foragers (e.g.,
Barnard, 1984;
Elgar and Crespi, 1992).
Mortality through cannibalism and lost foraging opportunities through
kleptoparasitism should thus be considered costly in terms of fitness
(Barnard, 1992;
Elgar and Crespi, 1992), and
the risk of such interactions should affect foragers in the same way as risk
of predation. In this study we investigated how prey size affects the risk of
falling victim to cannibals or kleptoparasites in piscivorous fish. Changes in
the probability of intraspecific attacks with changes in prey size should
affect prey choice in piscivores; low-risk prey that minimize the risk of
cannibalism and kleptoparasitism should be preferred.
Cannibalism is common among piscivorous fish
(Smith and Reay, 1991). The
northern pike (Esox lucius) is an important piscivore in many north
temperate freshwater systems, and it is well known that cannibalism is a
common feature of pike populations (e.g.,
Grimm and Klinge, 1996), both
within (e.g. Bry et al., 1992;
Giles et al., 1986) and
between Craig and Kipling,
1983; Grimm, 1981)
cohorts. Further, kleptoparasitism has been observed among pike individuals
(Grimm and Klinge, 1996). Pike
is a selective predator that feeds on prey sizes well below its upper
size-limit (e.g., Hart and Hamrin,
1988; Nilsson and
Brönmark, 1999). Pike also prefer
shallowbodied over deep-bodied prey, both within
(Nilsson et al., 1995) and
between (Hambright et al.,
1991; Wahl and Stein,
1988) species. Different aspects associated with handling time,
foraging time, and energy gain have been suggested to account for prey
selectivity in piscivores, including pike (e.g.,
Hart and Connellan, 1984;
Hart and Hamrin, 1988,
1990;
Hoyle and Keast, 1987;
Nilsson et al., 1995).
However, when given a choice, pike prefer prey that are smaller than predicted
by optimal foraging models. These previous studies have used time as currency
when evaluating the costs in foraging success with changes in diet. However,
pike is an efficient ambush predator (Webb
and Skadsen, 1980) that spends relatively little time foraging
(e.g., Breck, 1993). Thus, it
is somewhat of a paradox that some seconds or, at the most, minutes in
manipulation and handling time would make pike prefer small prey instead of
larger, energetically more profitable prey. A plausible explanation is that
some external factor, acting on handling time, affects prey selectivity (see
Gilliam, 1990). Risk of
cannibalism and kleptoparasitism may be such factors. Pike are attracted to
their prey by visual, chemical, and mechanical cues
(Raat, 1988). When pike handle
their prey, they elicit such signals themselves, through erratic movements and
odors released from injured prey. Therefore, long handling times (associated
with large and/or deep bodied prey;
Nilsson et al., 1995) should
incur a risk if conspecifics are within sensory distance of the foraging pike
(see Chivers et al., 1996).
Consequently, adapting predatory behavior to the presence of potential
conspecific interactors should be beneficial.
Here, we measured the effects of prey size and indirect and direct presence of conspecifics on pike predatory behavior and subsequent intraspecific interactions. We hypothesized that increased prey sizes lead to increased handling times and increased exposure to both cannibalism and kleptoparasitism, which should both constitute major costs to the pike. Given that intraspecific interactions are costly, northern pike should alter predatory behavior in the presence of conspecifics. We also examined what effects intraspecific interactions and prey size have on frequency of cannibalism, kleptoparasitism, and prey survival, as well as the drawbacks of nonoptimal striking of prey (i.e., failing to strike and swallow prey head-on).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The experiments were performed in 300 l aquaria (LxHxD: 120x50x50 cm), that were divided into three compartments: two holding compartments (50x25 cm each) in one end, and an experimental arena (70x50 cm) in the other end. Gray PVC walls separated the compartments, and remotely controlled doors (20x20 cm) were installed between each of the holding compartments and the experimental arena. The bottom of each aquarium was covered with sand. The aquaria were kept at constant light (9:15 h light:dark) and temperature (12±1°C) regimes. Twelve wild-caught focal pike [219.8±13.8 mm (±SD) total length: TL] were each assigned one aquarium and placed in one of the holding compartments. We quantified pike predatory behavior in five different treatments: (1) control; chemical cues from (2) similar-sized or (3) larger conspecifics; and direct interaction with (4) similar-sized or (5) larger pike. The treatments were performed with four prey-size classes (Table 1), each replicated six times with separate pike. Half of the pike participated in treatments 1, 2, and 4, and half in the other. The treatments were completed in numerical order in order to avoid learning, recognition, and subsequent changes in focal pike behavior over the experiment. All trials were filmed using VCR equipment, and the recordings were checked for pike predatory behavior (Table 2).
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Control
The focal pike were starved 3-4 days before each trial. At the start of an
experiment, one crucian carp (Carassius carassius) from a randomly
chosen prey-size class was put in a remotely controlled plastic net cylinder
(18 cm diam; mesh size: 1.2x1.2 mm) in the center of the experimental
arena. The door to the pike was opened, and when the pike had entered the
experimental arena, the door was closed and the net cylinder removed, allowing
the pike to attack the crucian carp. When the pike had completely swallowed
its prey, the trial was over, and the pike was returned to the holding
compartment. Predatory behaviors 1-11 in
Table 2 were recorded.
Chemical cues
We ran the chemical cues treatments in the same way as the control, but
with a conspecific, either larger (382.3±13.7 mm TL) or similar-sized
(213.2±15.0 mm TL), in the remaining holding compartment of each
aquarium. The secondary pike were not allowed access to the experimental arena
at the same time as the focal pike, but were fed crucian carp in the
experimental arena before and between trials, allowing for the focal pike to
recognize the scent of a foraging conspecific.
Interaction
In the interaction treatments, the focal pike were held in the experimental
arenas, while secondary pike (the same as in the chemical cues treatments)
were held in one of the holding compartments in each aquarium. In these
experiments, the crucian carp were simply dropped into the experimental arena,
and as soon as the focal pike had successfully struck its prey, the door to
the secondary pike was opened, and the two pike were allowed to interact. A
trial was completed when either of the pike had swallowed its prey. Behaviors
7-14 in Table 2 were recorded.
After a trial, the secondary pike were changed between aquaria (within each
treatment) so that any focal pike did not meet the same conspecific twice. In
seven experiments with larger conspecifics, the focal pike were attacked and
eaten and thus replaced with similar-sized pike (232.7±12.5 mm TL).
In the trials with large pike interacting with focal pike handling prey
from size class 4, half of the larger pike had by chance been cannibalistic in
the previous trial. The 3-4 days between trials did not allow for complete
digestion of such large prey (Nilsson and
Brönmark, personal observations). Because gut
fullness generally decreases foraging motivation (e.g.,
Hart and Hamrin, 1988,
1990), the cannibalistic pike
should have been less motivated to feed in the subsequent trial. Therefore, we
performed an additional experiment with new pike that had not been feeding on
large prey (i.e., other pike) prior to the experiment. In this experiment,
focal (242.2±12.0 mm TL) and large (381.2±10.3 mm TL) pike were
starved for 3 days before trials, and interaction experiments were run with
prey from size class 4 (Table
1).
Prey orientation
We recorded the effects of the orientation of prey in the mouth of the pike
after a strike on postcapture predatory behaviors. The results from all
treatments were pooled, and behaviors related to handling time (behaviors 7-11
in Table 2) were compared
between prey struck and swallowed head-on or other (tail-on or sideways).
Statistical analyses
There was no difference in behavior between pike individuals
(Table 3). Thus, pike
individuals were pooled in the analyses of effects of treatment and prey size.
We analyzed the effects of prey size, chemical cues, and interactions from
conspecifics on precapture (behaviors 1-6,
Table 2) and postcapture
(behaviors 7-11, Table 2) behaviors with MANOVAs with preysize class and treatment as fixed factors and
behaviors as dependent variables. The analyses of precapture effects included
data from treatments "control" and "chemical cues"
from large and small conspecifics, while analyses on postcapture effects
included data from all treatments. However, data from focal pike that did not
complete their predatory sequence due to interactions from conspecifics were
excluded from analysis. We analyzed the number of approaches and attacks from
larger and similar-sized secondary pike during focal pike hold, manipulation,
and handling time with t test. Number of approaches and attacks in
the interaction treatments were compared between prey-size classes with
ANOVAs. Effects of prey orientation in the mouth of the pike on
handling-time-related events were evaluated with t tests with head
first or other direction as independent and each separate behavior as
dependent variables. Differences in size class between lost and retained prey,
as well as between prey swallowed head first or in other directions were
analyzed with Mann-Whitney U tests. We conducted all statistical
tests using Systat 5.2.1 for the Macintosh
(Wilkinson, 1992).
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Animal care
Pike and crucian carp were caught in the field and directly transported to
the Ecology building, Lund University, and acclimatized to laboratory
conditions. Before experiments, all pike and crucian carp were kept in large
aquaria and fed crucian carp or frozen chironomids, respectively. At the end
of the experiments, we returned remaining fish to their natural habitat. The
results of the experiment depend on the natural behaviors of the experimental
animals. Thus, care was taken to minimize disturbance and stress. The
Malmö/Lund Committee for Animal Experiment
Ethics examined and commissioned the experimental procedure (permission no. M
32-97) to certify that ethical concerns were complied with.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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When the northern pike in our experiments foraged, neither treatment nor prey size had any effects on precapture behaviors (Table 3). Postcapture behaviors, on the other hand, were affected by both treatment and prey size (Table 3). Post-hoc ANOVAs revealed that treatment affected the postcapture behaviors hold and distance moved during handling time (DHT; Table 4, Figure 1c, f). In treatments with chemical cues from both larger and similar-sized pike, as well as during interactions with larger conspecifics, the focal pike decreased holding behavior (Figure 1c). DHT was lower in the control than in the treatments and increased the most in treatments using chemical cues from similar-sized pike and interactions with larger and similar-sized conspecifics (Figure 1f). Prey size affected all postcapture behaviors, generally increasing behaviors with increasing prey size (Table 4; Figure 1a, b, d, e, g, h). There was also a significant interaction effect of treatment and prey size on DHT (Table 4). These results imply that northern pike are reluctant to alter predatory behavior, but that prey size has inevitable effects on the duration of postcapture behaviors.
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Both large and similar-sized secondary pike approached and attacked foraging focal pike. However, approaches and attacks from larger and similar-sized conspecifics were elicited by different foraging behaviors in the focal pike. Large pike approached and attacked throughout focal pike handling time, as long as the focal pike were active in any way (Figure 2a, b; differing from zero: p <.01, df = 23, t = 2.883 and p <.02, df = 23, t = 2.638, respectively). That is, any motion in the focal pike potentially attracted cannibals. When the focal pike were inactive and no motion was detectable, larger conspecifics never approached or attacked (Figure 2a, b). Further, the number of approaches from larger conspecifics differed between prey-size classes handled by the focal pike (p =.049, F3,44 = 2.840), whereas number of attacks did not (p =.115, F3,44 = 2.095; Figure 2c, d). Interestingly, larger pike never approached focal pike handling prey from the smallest size class (Figure 2c, d). In contrast, for similar-sized secondary pike, there was no effect of prey size on approach or attack frequency (p =.590, F3,44 = 0.646 and p =.495, F3,44 = 0.810, respectively). Showing somewhat different behavioral patterns, similar-sized conspecifics approached (p =.006, df = 23, t = -3.019) and attacked (p =.009, df = 23, t = -2.849) focal pike more often when they manipulated their prey (Figure 2e, f), compared to when the prey was held. The larger pike did not show this pattern (p =.295, df = 23, t = -1.071 and p =.679, df = 23, t = -0.419, respectively). Further, similar-sized pike never approached focal pike after the prey had been secured head first or tail first into the mouth.
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Some of the focal pike lost their prey during interactions with larger conspecifics. There was a tendency that lost prey were larger than those retained, but the difference was not significant (p =.074, n = 24, U = 42.0; Figure 3a). In interactions with similar-sized conspecifics, on the other hand, the difference between lost and retained prey was significant (p =.006, n = 24, U = 22.5; Figure 3b), indicating that the risk of lost foraging opportunity increases with prey size.
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The interactions with larger pike led to cannibalism in some cases, and prey size handled by the focal pike affected the risk of cannibalistic interaction. One focal pike was cannibalized when handling prey from size class 1, two when handling size class 2, three with size class 3, and one with size class 4 (Figure 4a). In the additional experiment on interaction with larger pike, where new, nonsatiated pike were used, five of the six small pike were cannibalized when handling prey of size class 4 (Figure 4a). This pattern of increasing risk with increasing prey size also shows in the experiments with similar-sized pike. Focal pike handling prey of size class 1 never lost their prey, while one prey from class 1, four from class 3, and four from prey-size class 4 were lost to kleptoparasites in interactions with similar-sized pike (Figure 4b). In the trials with interactions with larger pike, prey size also had effects on the chance of escape for the prey. One crucian carp from size class 1, one from 2, three from 3, and one from 4, escaped and survived trials with interactions from larger pike because the focal pike let go of them after it was caught (Figure 4c). In the additional experiment, five out of six size class 4 crucians escaped predation after the interaction.
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Northern pike predatory performance was affected by the direction of prey in the mouth after a strike. Failing to strike and swallow prey head first significantly increased manipulation time (p =.005, df = 121, t = -2.862), handling time (p =.015, df = 121, t = -2.476), and the time to swallow the prey after securing it (p = 0.038, df = 121, t = -2.098; Figure 5). Nonoptimal striking and swallowing of prey occurred in about 15% of the trials and was not significantly related to prey-size class (p =.171, U = 1525.5, n = 144).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Behavioral interactions
Cannibalism and kleptoparasitism are common in pike populations (e.g., Bry et al., 1992
;
Grimm, 1981;
Grimm and Klinge, 1996;
Mann, 1982). To minimize the
risk of cannibalism and kleptoparasitism, pike may, for instance, use habitats
that lack large conspecifics, forage in patches with low pike density, and
generally avoid any behavior that may attract conspecifics. In our
experiments, treatments had only minor effects on focal pike predatory
behavior, and then only on postcapture events. Chemical cues from conspecifics
and interactions from larger pike decreased the time holding the prey. These
changes may be due to focal pike avoiding potential competition or risk of
cannibalism through minimizing handling time. Treatment, prey size, and their
interaction all affected distance moved during handling time. Here, the effect
of treatment originates in behavioral interactions and chases from
conspecifics that may have made the focal pike increase DHT. Increasing prey
size increased the struggle and time elapsed during handling and swallowing,
therefore potentially increasing DHT. Thus, both treatment and prey size
affect DHT, and because conspecific interactions are more likely with
increasing handling time (i.e., increasing prey size), there was also a
significant interaction between treatment and prey-size class. Apart from the
effects above, treatment did not affect focal pike predatory behavior.
However, pike predatory performance diminished when pike were unable to strike
and swallow prey head first. Swallowing prey sideways or tail first
significantly increased manipulation, handling, and swallowing time. These
events are crucial considering the risk of attracting potentially
cannibalistic or kleptoparasitic conspecifics. Thus, striking and swallowing
prey head first should be advantageous to pike.
Generally, risk of predation and/or chemical cues from potential
interactors elicit behavioral changes in prey animals, including behaviors
such as escape, avoidance, reduced activity, habitat change, or altered
life-history traits (Kats and Dill,
1998; Lima and Dill,
1990). Because there is a trade-off between avoidance of risks and
foraging efficiency, any of these behavioral changes should minimize the risk
per energy intake (see Gilliam,
1990; Krebs,
1980). Animals that expose themselves to predation when foraging
(e.g., while searching or hunting for prey) should optimally choose to
minimize this exposure (i.e., decrease foraging intensity or exposure to the
risk). Intuitively, pike should therefore adapt foraging strategy to the
presence of chemical cues from foraging conspecifics because potential
cannibals and kleptoparasites constitute a risk during foraging. However, no
such changes in behavior were observed. In nature, pike often live closely
together in dense populations (e.g., Raat,
1988) and continuously smell and see conspecifics. Thus, under
natural conditions, changing foraging behavior in the presence of other pike
may not be optimal regarding foraging efficiency. Because pike with their
sit-and-wait foraging behavior already minimize exposure time to conspecifics,
changing predatory behavior in response to continuous chemical cues from
neighboring pike individuals may not be adaptive.
Cannibalistic and kleptoparasitic pike interact with focal pike during
different foraging events. Large pike approach and attack when focal pike emit
mechanical and visual cues through motion, whereas similar-sized pike approach
and attack primarily when focal pike manipulate their prey while securing it
in the mouth. This is probably explained by the fact that large pike do not
distinguish between the crucian carp and the smaller pike, but regard them
both as a potential package of prey, whereas the similar-sized pike do not
have this choice. The similar-sized pike must rely on their ability to steal
the prey from the focal pike, and thus approach and attack when the chance of
succeeding is the greatest (i.e., when the focal pike manipulates its prey).
This phenomenon may also explain why focal pike maintain relatively long
holding times during interactions with similar-sized pike, even though this
behavior potentially increases handling time. Holding the prey in the presence
of similar-sized conspecifics momentarily minimizes the amount of attractive
signals emitted and thus decreases the risk of kleptoparasitism. Foragers may
thus change and adapt handling time according to the current circumstances,
balancing different demands. That is, in the absence of predators, foragers
should maximize energy gain per handling time (i.e., generally minimize
handling time). While in the presence of a predator, on the other hand,
foragers should minimize mortality rate per foraging rate, if necessary by
increasing handling time (see Gilliam,
1990). There may also be digestive constraints or demands in the
handling time equation. Birds feeding out of cover may minimize handling time
to minimize exposure to and risk of predation
(Valone and Lima, 1987). When
able to handle their food in cover, however, they choose to increase handling
time, breaking up the food in smaller pieces, presumably decreasing digestion
time. Thus, optimizing handling time is not always a matter of minimization
but is context dependent, and foragers behave accordingly.
In our experiments, we used wild-caught northern pike and crucian carp to
experimentally determine effects of prey size on predator behavior and
interactions. The experiments were carried out in aquaria, which may confine
the behaviors of some animals. However, pike and crucian carp easily adapt to
aquarium conditions, and because pike is an ambush predator that moves little
during foraging, pike predatory behavior is not seriously constrained by the
experimental scale. In natural environments, pike are often associated with
the littoral vegetation-open water interface. For logistic reasons, our
aquaria did not contain any macrophytes or other structural elements, as any
complexity would have seriously interfered with the quantification of
behaviors. However, when pike attack their free-swimming prey, they
momentarily leave the complex vegetation to forage in open water (e.g.,
Raat, 1988). Therefore,
complexity has little or no effect on the foraging and interactive behaviors
measured in this work. Further, cannibalism and kleptoparasitism commonly
occur in pike populations in nature (e.g.,
Grimm and Klinge, 1996).
Hence, we conclude that pike behavior was not induced by the experimental
setup, rendering our results valid also for natural circumstances.
Risks and costs
The costs involved with experiencing cannibalism and kleptoparasitism are
obvious. To stay away from cannibals or at least decrease the risk of
attracting them should decrease the risk of mortality. If the risk of being
cannibalized increases when taking larger prey, large prey should be avoided.
In the initial experiment, the number of cannibalized focal pike increased
with prey size in the trials with prey-size classes 1-3. This increasing trend
was, however, interrupted with the largest prey-size class, where only one
focal pike was cannibalized. We suggest that this latter, somewhat
contradictory result is an experimental artifact: in the trials with larger
pike interacting with focal pike handling the largest prey, half of the larger
pike had cannibalized focal pike in the previous trial. Keeping the original
experimental setup with 3-4 days between trials did not allow the cannibals to
digest those relatively large prey. Gut fullness generally decreases foraging
motivation (e.g., Hart and Hamrin,
1988, 1990), and
this resulted in the larger pike taking no notice of the foraging focal pike
in the next trial. This artifact should also explain the trend in the number
of approaches and attacks on focal pike handling the largest prey, as well as
the number of crucian carp escaping predation and surviving trials with
interactions with large pike, as chances of escape depend on the focal pike
being disturbed by interactions. In the additional experiment, where we reran
the trials with interaction from larger pike when focal pike handled prey from
size class 4, we used new pike that had been deprived of food for 3 days and
thus were motivated to forage. Here, the results clearly show that the largest
prey size leads to the greatest risk of cannibalism, as well as the greatest
chance of escape for the prey.
Losing an already captured prey is the most direct cost for
kleptoparasitized foragers. To avoid this, or any other cost with the
interaction, foragers should strive to minimize the risk of kleptoparasitism.
Prey size selectivity may be a way of reducing that risk. It has been shown in
kleptoparasitic species of birds that the larger the food item, the greater
the risk of being parasitized (e.g.,
Hockey and Steele, 1990).
Analogously, the focal pike in our experiments lost prey that were larger than
the ones they succeeded in retaining during interactions with kleptoparasites.
Further, the frequency of kleptoparasitic events increased with prey size
handled. There was also a tendency that focal pike lost larger prey more often
in interactions with cannibals. Therefore, large prey items inflict greater
risks of losing a meal and should be avoided if the probability of attracting
conspecifics is high. Further, when the focal pike were attacked by
kleptoparasites, there was often fierce interaction and fight over the prey.
Kleptoparasitic pike attack toward the prey in the mouth of the focal pike,
and thus risk of contracting injuries to the eyes is prominent. Because pike
to a large extent rely on vision when foraging (e.g.,
Raat, 1988), such injuries may
severely decrease future foraging efficiency and ultimately decrease fitness.
Fighting with kleptoparasites may inflict further costs. Because fighting
increases reaction time and escape reaction distance in case of a predator
attack (Jakobsson et al.,
1995), engaging in fights over food decreases vigilance and
increases risk of attracting and falling victim to predators. Another example
of how kleptoparasitism may affect fitness is the wild dog-hyena interactions
in South Africa (Gorman et al.,
1998). Here, the costs are not necessarily associated with direct
injuries, but with energy expenditure. Because wild dogs use a lot of energy
when hunting for prey, kleptoparasitism by hyenas not only deprives the wild
dogs of their food item, but also of the energy consumed for catching it, thus
having large effects on energy budgets.
Prey selectivity
An optimal forager should select prey that contribute the most gain and
least cost. Several studies have shown that pike is a selective forager that
chooses to feed on small prey (Beyerle and
Williams, 1968; Hart and
Hamrin, 1988,
1990). Further, pike prefer
shallow-bodied prey fish over deeper bodied fish
(Hambright et al. 1991,
Nilsson et al. 1995,
Wahl and Stein 1988). For
example, crucian carp may exist in two different morphs, a shallow-bodied
morph and deep-bodied morph, where the deep-bodied morph is induced by the
presence of piscivores
(Brönmark and
Miner, 1992;
Brönmark and
Pettersson, 1994). When given a choice, pike prefer to feed on
shallow-bodied, noninduced individuals of crucian carp over predator induced,
deep-bodied ones
(Brönmark and
Miner, 1992; Nilsson et al.,
1995). They also prefer shallow-bodied roach (Rutilus
rutilus) over deep-bodied common bream (Abramis brama;
Nilsson and
Brönmark, 1999). As handling time
increases with increasing size and body depth (e.g.,
Nilsson et al., 1995), pike
may be expected to choose prey that minimize handling time per energy input.
Yet, pike actually prefer prey fish that are smaller than predicted from
optimal foraging models based on energy and time budgets
(Hart and Connellan, 1984).
The predictions in the models overestimate optimal prey size because they fail
to acknowledge that handling time per se does not restrict pike foraging. Pike
use an ambush foraging strategy, and the amount of time spent actively
pursuing prey is relatively short (e.g.,
Breck, 1993). However, taking
into account that northern pike are exposed to cannibals and kleptoparasites
while foraging and that this exposure increases with handling time, which in
turn increases with prey size, validates prey size selectivity in pike. The
preference for small-bodied prey is thus a result of a trade-off between
energy gain and time of exposure to conspecifics (i.e., risk), not in time per
se (see Gilliam, 1990;
Hughes, 1997;
Stephens and Krebs, 1986).
Risk of predation has also been shown to affect the food choice of guppies
(Godin, 1990). In the absence
of predators, guppies fed on prey sizes according to what is predicted from
optimal foraging models. Under the risk of predation, however, the guppies
changed prey preference to smaller sizes than predicted.
Prey more deep bodied than their neighbors (e.g., induced crucian carp or
common bream) benefit from their morphology by being selected against by pike.
Also, even if a deep-bodied prey is struck by a northern pike, it may still
benefit from its body depth. Postcapture interactions with larger conspecifics
made our focal pike lose large prey. Therefore, deep-bodied prey have an
increased chance of escape. Out of the total 19 events where large pike
actively interacted with focal pike, 13 of the crucian carp escaped and
survived. This suggests that being large or deep bodied and thus attracting
further pike while being handled is beneficial to the prey. Similarly, Chivers
et al. (1996) showed that
attacked and injured minnows release alarm substances that attract further
predators that may interact with the first. They also showed that these
interactions increase the opportunity of prey escape and suggested this as a
mechanism behind the evolution of alarm substances in fish.
Effects in natural ecosystems
In natural systems, the risk of cannibalism and kleptoparasitism should
vary with density (e.g., Giles et al.,
1986) and size structure
(Smith and Reay, 1991) of the
populations. With increased density, the distance to neighbors decreases,
increasing the risk of handling large prey. In stunted populations only the
smallest individuals, if any, would risk cannibalism, but kleptoparasitism
would be common. In more diversely size-structured populations, cannibalism
would be a real risk also for intermediate-sized individuals. One has to bear
in mind, however, that the above phenomena should be most prominent in systems
with relatively dense populations and somewhat depleted prey abundances.
Further, an increased risk involved with handling large or deep-bodied prey
should affect prey size selectivity in the predator and subsequently affect
population and community dynamics. If predators prefer small prey, prey
population size-structure will be skewed. Also, high-cost interference, such
as intraspecific interactions in the predator, may have effects on the
stability of predator-prey interactions (e.g.,
Fryxell and Lundberg, 1997).
In conclusion, the risk of conspecific attacks may affect predator behavior
and therefore behavioral size-refuges for their prey, potentially decoupling
top-down impact of predation on trophic interactions (see
Hambright et al., 1991).
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank Grant Brown, Thomas Madsen, and three anonymous reviewers for valuable comments on earlier versions of the manuscript. Financial support was received from the Swedish Board for Agriculture and Forestry Research, and the Royal Swedish Academy of Science.
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