ANIMAL BEHAVIOUR, 1998, 56, 1477–1483
Article No. ar980917
Temporal prey distribution affects the competitive ability of
parasitized sticklebacks
IAIN BARBER & GRAEME D. RUXTON
Fish Biology Group, Division of Environmental & Evolutionary Biology, Institute of Biomedical and Life Sciences,
University of Glasgow
(Received 28 August 1997; initial acceptance 25 September 1997;
final acceptance 25 June 1998; MS. number: 5637R)
ABSTRACT
Parasitized animals are often reported to have a reduced competitive ability in experimental studies
designed to examine foraging success under a specific type of competitive interaction; however, since
animals compete under a range of competition regimes in natural situations, and because success is likely
to require different foraging skills under each, it is unclear whether infected animals should be equally
poor competitors under all competitive scenarios. We studied the foraging success of three-spined
sticklebacks, Gasterosteus aculeatus, infected with plerocercoids of a cestode, Schistocephalus solidus, in
competition with uninfected conspecifics. When pairs of differentially infected sticklebacks were
presented with sequentially introduced items, the numbers of available prey taken by infected and
uninfected competitors did not differ significantly, although nonparasitized fish were more successful at
taking items over which there was direct competition. In contrast, when prey items were presented
simultaneously in a locally dense patch, nonparasitized fish ingested significantly more of the available
food than their infected counterparts: an apparent consequence of their greater ability to take items in
rapid succession. Our results show that the type of competition conditions generated as a result of specific
prey distribution patterns plays a role in determining the relative foraging success of parasitized
sticklebacks, and suggest that this may have consequences for the distribution of different infection
classes in natural, heterogeneous environments.

conditions. Since, in natural environments, individuals
compete with one another in a variety of ways depending
on the particular spatial and temporal relationships of the
competitors and their prey, testing foraging success under
only one type of competition may give a distorted or
biased impression of the effects of parasites on host
competitive ability, and their subsequent role in host
ecology.
The way in which groups of foraging animals encounter food may influence the type of competition group
members experience. For instance, if prey are encountered singly and sequentially there is likely to be competition over individual items (Milinski 1982; Gill & Hart
1996), whereas if food is encountered in discrete patches,
so that the prey available at any one time outnumber the
foragers, individuals in groups are likely to deplete one
food patch before moving on to another, with little direct
competition over individual items. Successful competitors under the different types of competition generated
are likely to require certain morphological attributes or
behavioural strategies to be successful; the best competitors in the first situation described above will be those
Within a species, individuals vary in their ability to
compete for limited resources, such as food, territorial
space or mates; factors known to be important in generating intraspecific variation in competitive ability include age, experience, body size and social dominance
(Sutherland & Parker 1985; Milinski & Parker 1991).
However, for animals that form size- and age-matched
aggregations, such as many species of shoaling fish,
variation in the level of infection with debilitating parasites or other agents of infectious disease is potentially an
important source of competitive heterogeneity amongst
group members. In particular, certain types of infections
are thought to reduce the ability of their hosts to compete
with others for food (e.g. Crowden & Broom 1980;
Milinski 1984; Cunningham et al. 1994); however, foraging success in such studies is usually measured only under
conditions that generate a single type of competitive
interaction, and little is known about the competitive
ability of infected animals under alternative foraging
Correspondence: I. Barber, Division of Environmental & Evolutionary
Biology, Graham Kerr Building, University of Glasgow, Glasgow
G12 8QQ, Scotland, U.K. (email: [email protected]).
0003–3472/98/121477+07 $30.00/0
1998 The Association for the Study of Animal Behaviour
1477

1998 The Association for the Study of Animal Behaviour
1478 ANIMAL BEHAVIOUR, 56, 6
that react first and move quickest towards individual
items, whereas when feeding in patches of limited size
the most successful foragers will be those that can maximize their food intake rate to secure a disproportionate
number of the available prey. Therefore, individuals that
are successful competitors under one type of competitive
regime may not necessarily be equally proficient when
food is competed for in a different way. Consequently,
the reported negative effects of parasites on the ability of
hosts to compete for food may be reduced, or otherwise
altered, under changed competition conditions.
To test whether the type of competition generated
under different feeding regimes could influence the competitive ability of supposed ‘poor’ competitors, we created
foraging environments designed to imitate the two situations described above. We chose three-spined sticklebacks, Gasterosteus aculeatus, as the study species, since
they naturally form foraging groups outside the breeding
season (Hart & Gill 1994) and are ideally suited to
laboratory-based behavioural investigations (Bakker &
Sevenster 1995). In lacustrine populations, a proportion
of individuals often harbour parasitic plerocercoid larvae
of the cestode Schistocephalus solidus, which they acquire
by feeding on infected copepods (Smyth 1962). Infected
fish are expected to be poor competitors for food since
they are physically disabled by the parasites (which
develop in the body cavity; Arme & Owen 1967) and
because infection is associated with correlates of poor
competitive ability during feeding (Milinski 1990; Barber
& Huntingford 1995). Here, we present results from two
studies examining the ability of S. solidus-infected sticklebacks to compete in pairs with size-matched uninfected
conspecifics for prey items presented either singly and
sequentially, or simultaneously in a spatially dense patch.
MATERIALS AND METHODS
Subjects
We hand-netted three-spined sticklebacks from an
urban park pond in Edinburgh, U.K. during August 1994.
Schistocephalus solidus plerocercoids are established parasites of sticklebacks at the site, and each year a proportion
of the population is infected (Tierney 1991; Barber 1995).
After capture, infected and uninfected fish were held
together in stock tanks and fed ad libitum with bloodworms (Chironomus spp. larvae) and flake food for 2
months to allow newly acquired infections to reach a size
at which they can be detected visually by the associated
swelling of the host’s abdomen (see Barber 1997).
Aquarium conditions (temperature: 12C; photoperiod:
12:12 h light:dark) ensured that experimental fish did not
undergo physiological changes associated with the sexual
phase (Wootton 1976).
Experiment 1: Sequentially Presented Prey Items
Twenty pairs of sticklebacks, each composed of one
infected and one uninfected fish, were selected from the
stock tanks and each pair housed separately in individual
compartments (202020 cm) in holding aquaria
(804020 cm). Because relative size is known to be an
important factor in determining competitive ability
(Wilson 1975; Ranta & Lindström 1990), we matched
each pair of fish with respect to total length. Since
sticklebacks in this population complete their life cycle in
a single year and then die (Tierney 1991), fish matched
for size in this study are also matched for age, all being
young-of-the-year. The sex of sticklebacks cannot be reliably determined outside the breeding season (Wootten
1976) and so it was not possible to match fish with
respect to sex; any differences associated with gender in
this study are assumed to be negligible.
The paired fish were fed ad libitum and to excess with
live bloodworms for 4 days before feeding was stopped,
24 h before the trials. Fish pairs were then introduced in
turn to the experimental tank, a glass aquarium measuring 302025 cm, filled with water to a depth of 20 cm
and covered on three sides to minimize disturbance. They
were left to settle for 2 h, during which they began to
display typical foraging activity. We then introduced
individual prey items (halved bloodworms, each 5 mm
long) sequentially to the experimental tank at 90-s intervals from behind a screen, using an extended pipette, and
videotaped the responses and feeding behaviour of both
fish. We terminated the experiment after 10 prey items
had been introduced, exposed the fish to a lethal dose of
benzocaine anaesthetic and dissected them immediately
to confirm their infection status.
General behaviour and video analysis
As each prey item was introduced it was quickly
approached by either one, or both, of the sticklebacks.
The responses of the fish to introduced prey were sometimes simultaneous (i.e. within the same frame of film,
approximately 0.05 s), although differences in their initial orientation and respective distance from the introduced food often resulted in one fish responding before
the other. Such responses had two outcomes: (1) the first
fish to respond quickly ingested the prey item before its
competitor showed any sign of being aware of the presence of the food; or (2) the nonresponding fish was
alerted to the presence of the food by the movements of
the responding fish and also approached the item. If one
fish arrived at the prey item before the other, ingestion
was generally swift and uncontested; however, if the two
fish arrived simultaneously, ingestion was frequently
achieved only after a contest, with each fish either biting
repeatedly at the prey item, or seizing an end of the worm
fragment and attempting to pull it away from the other.
For each item introduced to the tank, we recorded the
following: (1) which of the fish reacted first to the prey
item (infected/uninfected/simultaneous response); (2) in
the case of simultaneous responses, which fish was closest
to the prey item when it responded (infected/uninfected/
equidistant); and (3) which of the fish ingested the prey
item (infected/uninfected/neither). Each ingested item
was then classified as ‘easy’, ‘difficult’ or ‘contested’,
based on the spatial relationships of the two fish and their
temporal reactions to the introduced prey (see Table 1
for classifications of prey categories). In addition, we
BARBER & RUXTON: PARASITES AND COMPETITION IN FISH 1479
Table 1. Definitions of categories of prey ingested by sticklebacks in
the sequential presentation experiment
Prey
category
Easy
Difficult
Contested
Definition
Either:
only the successful fish reacts to prey item, or
the successful fish reacts to prey item first, or
both fish react simultaneously to prey item
(with the successful fish closest to prey item),
and:
ingestion is not contested (see below).
Either:
the successful fish reacts second, or
both fish react simultaneously to prey item
(with both fish equidistant from prey item), or
both fish react simultaneously to prey item
(with the successful fish furthest from prey
item),
and:
ingestion is not contested (see below).
After any type of response, either:
both fish bite rapidly at the prey item before it is
consumed by the successful fish, or
each fish has one end of the prey item in its
mouth before it is eventually consumed by the
successful fish.
All prey items, and the way in which they were presented, were
identical; the categorization of ingested items into ‘easy’, ‘difficult’
and ‘contested’ relates solely to the spatial relations of the two
competing fish and their temporal responses to the introduced prey.
recorded the relative vertical positions of the two fish in
the water column throughout each trial, and calculated
the total amount of time that each fish spent closest to
the surface in each trial.
Experiment 2: Simultaneously Presented Food
Items
Eleven pairs of length-matched uninfected and infected
sticklebacks were selected from the stock tanks and maintained in separate tanks for 4 days, where they were fed
on live bloodworms presented in the same design of
feeder that was used in the subsequent experimental
trials. After 24 h of food deprivation, we introduced pairs
of fish to the experimental tank, which was identical in
dimension, substrate type and water depth to that used in
experiment 1 but was fitted with a feeder that held eight
live bloodworms anchored vertically in petroleum jellyfilled Plexiglas cells. The feeder design ensured that individual bloodworms were presented to the fish, and
removed from the substrate by them, in a manner similar
to that experienced in the natural environment (I. Barber,
personal observation).
Prior to each experimental trial, the feeder was hidden
from view by an opaque cover. Each pair of sticklebacks
was introduced to the experimental tank in turn, and
allowed to settle for 2 h before the food patch was
uncovered. The small size of the tank ensured that both
fish discovered the patch at the same time, and feeding
on the clumped prey began almost immediately. We
videotaped each trial until all of the bloodworms had
been consumed, and recorded the time taken from the
beginning of the trial to ingestion of each prey item by
both fish. In no trial did fish leave bloodworms in the
feeder, although on five occasions a single worm escaped
from the feeder into the gravel substrate, reducing the
number of available prey to seven.
RESULTS
Experiment 1: Sequentially Presented Prey Items
There were no apparent differences in the responses of
uninfected and infected competitors to the entry of
individual food items into the experimental tank, with
neither infection class more likely to be a lone responder
to the prey item (Wilcoxon signed-ranks test carried out
on the number of times per trial that the uninfected and
infected fish were lone responders: W=90.0, N=20 pairs,
P=0.86), to be the primary responder in nonsimultaneous
responses (Wilcoxon signed-ranks test carried out on the
number of times per trial that the uninfected and infected
fish were primary responders: W=63.0, N=20 pairs,
P=0.39) or to be closest to the incoming prey item prior
to a simultaneous response (Wilcoxon signed-ranks test
carried out on the number of times per trial that the
uninfected and infected fish were closest to the incoming
prey item: W=15.0, N=20 pairs, P=0.22). Nor was there a
consistent effect of infection status on relative vertical
position in the water column during the trials (paired t
test carried out on the amount of time per trial that the
uninfected and infected fish spent closest to the surface:
t19 = 0.44, P=0.66). Infection status did not influence
the proportion of available prey items consumed in a trial
when prey items were introduced sequentially (Fig. 1a)
and a paired t test, carried out to examine the difference
in the number of prey items taken by uninfected and
infected fish in each pair, revealed that there was no
significant difference in the numbers of prey taken by
either class of fish under this treatment (t19 =1.21,
P=0.24).
However, S. solidus infection status was important in
determining the manner in which prey were taken, with
a higher proportion of those prey classed as ‘difficult’ or
‘contested’ being included in the diet of uninfected fish
than expected, and more ‘easy’ prey being taken by the
parasitized fish (see Table 2). The types of prey captured
by both uninfected and infected competitors were distributed more or less evenly over the 20 replicates (Fig. 2).
Experiment 2: Simultaneously Presented Food
Items
When prey items were presented simultaneously, however, infection status did appear to influence the proportion of available prey items consumed in a trial (Fig.
1b): uninfected fish took more prey than infected fish
(paired t test: t10 =2.45, P=0.034).
1480 ANIMAL BEHAVIOUR, 56, 6
Table 2. Contingency table, showing the observed (O) and
expected (E) frequencies of uninfected and infected sticklebacks
capturing different classes of prey in experiment 1
1
(a)
Easy
Difficult
Contested
Total
Uninfected
O
E
(O−E)2/E
66.0
73.7
0.80
20.0
14.9
1.78
14.0
11.4
0.58
100
Infected
O
E
(O−E)2/E
63.0
55.3
1.08
6.0
11.1
2.37
6.0
8.6
0.77
75
Total
129
26
20
175
0.75
Proportion of available prey ingested
0.5
0.25
Chi-square test: χ22 =7.39, P<0.05. See Table 1 for definitions of prey
capture types.
0
Uninfected
Infected
1
(b)
0.75
ingested their second prey item more quickly than their
infected competitors (see Fig. 3). Subsequent statistical
analysis confirmed this to be the case (Mann–Whitney U
test: median time taken for uninfected fish to catch
second bloodworm=8.5 s, median time taken for
S. solidus-infected fish to catch second bloodworm=
19.6 s, N=10 trials; W=93.5, P<0.05).
DISCUSSION
0.5
0.25
0
Uninfected
Infected
Infection status
Figure 1. The proportion of available prey items ingested by
uninfected and S. solidus-infected sticklebacks when prey items
were presented (a) singly and sequentially (experiment 1) and (b)
simultaneously. Bars show means ± SD of 20 trials in (a) and of 11
trials in (b).
Figure 3 shows the times taken by uninfected and
infected competitors to ingest successive food items in
the trial. The temporal pattern of successive prey ingestion differed between infection classes; whereas uninfected fish consumed their first few prey items in rapid
succession, slowing after this initial burst of feeding
activity, infected fish had an initially slower, more steady
rate of food intake. Although infection status did not
predict which of the pair was first to ingest a prey item
(infected first=4 trials, uninfected first=5 trials, dead
heat=2 trials), when the times taken for subsequent prey
items to be ingested were plotted for uninfected and
infected fish separately, it appeared that uninfected fish
In natural environments, individuals compete with each
other in a variety of ways, ranging from passive exploitation competition (where a food supply is depleted by
noninteracting competitors) and interference competition (where the presence of one individual physically
prevents others from feeding) to aggressive contest competition (where competitors actually fight over a limited
food resource). Which type of competition is generated
depends to a large extent on the temporal distribution of
prey (Blanckenhorn 1991).
In stratified aggregations of species that are able to
handle only a small number of prey items at any one
time, temporal variation in resource distribution is
known to alter the relative foraging success of subordinate group members. When a large number of prey items
are encountered simultaneously, less competitively able
group members are able to exploit the remaining
resources for the period of time the dominant individual(s) is incapacitated whilst handling prey (the ‘synchrony hypothesis’: Blanckenhorn 1991; Grant & Kramer
1992; Bryant & Grant 1995), and in this way benefit
from group membership more than when resources
are encountered sequentially and are therefore more
defensible.
In our study, the relative foraging success of sticklebacks infected with S. solidus plerocercoids (generally
regarded as being poor competitors) was also dependent
on the type of conditions under which they are forced to
compete. However, when in competition with a single
uninfected fish, parasitized sticklebacks fared comparatively better when prey were introduced asynchronously
than when they were presented simultaneously, that is,
BARBER & RUXTON: PARASITES AND COMPETITION IN FISH 1481
1000
10
(a)
8
P < 0.05
100
Time taken (s)
6
Number of prey items
4
10
2
1
Uninfected
Infected
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
0
10
(b)
Easy
Difficult
8
Contested
1
2
3
4
n th prey item
5
6
Figure 3. The time taken by uninfected sticklebacks and S. solidusinfected sticklebacks to ingest successive prey items when prey were
presented simultaneously in a patch (experiment 2). Horizontal bars
show mean values.
6
4
2
0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
Trial number
Figure 2. The numbers of prey items classified as ‘easy’, ‘difficult’
and ‘contested’ ingested by (a) uninfected and (b) S. solidus-infected
sticklebacks during the 20 replicates of the sequential prey introduction experiment. Definitions of prey ingestion types are provided in
Table 1.
apparently opposite to that predicted by the ‘synchrony
hypothesis’. This apparent reversal of the expected pattern is likely to be attributed to the well-documented
physical, physiological and behavioural effects on competitive ability specifically associated with S. solidus
infection.
Although we found no consistent effect of infection
status on feeding success in our first experiment, it was
not the case that in these trials items were shared equally
between the two competitors, and in some trials one
individual clearly outcompeted the other. This suggests
that competitive ability varied under this type of prey
presentation, but that this variability was associated with
factors other than relative size and infection status. Competitive ability may be viewed as a trait in which individuals can invest differentially, depending on stochastic
internal and external factors, and differential motivation
to be competitive could result in the observed variation.
Although investment in competitive ability may be more
costly (either energetically, or in terms of increased risk of
predation whilst foraging) for parasitized fish, and eventually limit their scope for competitiveness, over short
periods of foraging under sequential prey introduction it
seems they can perform well enough to mask the effects
of infection.
This hypothesis is supported by our analysis of the way
in which prey were taken in the first experiment. Infected
fish were not successful when there was direct competition for individual prey (taking very few ‘difficult’ or
‘contested’ items), yet were able to secure a large proportion of ‘easy’ prey, improving their overall foraging
success to a level equivalent to that of uninfected competitors. It is unlikely that this was due to infected fish
having greater access to ‘easy’ prey items for which there
was no competition because of changes in their habitat
use; although it has been suggested that S. solidus-infected
fish may swim closer to the surface of the water under low
oxygen tensions or elevated water temperatures (Lester
1971; Giles 1987a), and therefore be closer to incoming
food, we did not replicate such conditions in our experiments and did not see such behaviour. Also, neither
infection class was more likely than the other to be closest
to incoming prey, nor to be significantly more likely to be
the primary or sole responder. Instead, the larger proportion of ‘easy’ items ingested by infected fish is more
1482 ANIMAL BEHAVIOUR, 56, 6
adequately explained by the hypothesis that they are
probably better at dealing with items encountered in
isolation, away from other competitors. This is possibly
a consequence of the risk-reckless foraging strategies
known to be used by S. solidus-infected sticklebacks (Giles
1983) and their reduced investment in vigilance, which
would otherwise reduce foraging efficiency under such
apparently risky conditions. The propensity of uninfected
fish to take more prey for which they need to compete
directly with another individual demonstrates that they
are more efficient at securing food items in the presence
of other individuals, which is probably perceived as a less
risky foraging situation.
In contrast, in the second experiment, where prey were
presented simultaneously in a patch, infected sticklebacks
were not able to moderate the effects of their disability by
investing more heavily in competitive ability, and were
outcompeted by uninfected competitors. Uninfected fish
were able to achieve this by ingesting their first few prey
items in rapid succession, thus depleting the patch available for the infected competitor, which fed in a slower,
more steady manner and did not bolt the food in the
same way. When food is distributed in discrete patches,
foraging animals typically increase their ingestion rate as
group size increases (Uematsu & Takamori 1976; Barnard
1984; Street et al. 1984); one plausible explanation for
this is that by increasing ingestion rate, individuals
obtain the maximum possible proportion of food
from the patch and reduce interference from other
group members (Pitcher & Parrish 1993). Clearly, when
food patches are small the ability to ingest the first
few items rapidly is the most important factor in determining overall foraging success, so why did infected fish
not bolt prey items in the same way as uninfected
conspecifics?
One possibility is that the restriction on gut expansion,
caused by the physical presence of the parasite, may
prevent rapid bolting. As S. solidus plerocercoids grow in
the body cavity of infected sticklebacks, the host viscera is
displaced, severely restricting space (Arme & Owen 1967).
Since the stomachs of uninfected sticklebacks normally
distend to fill most of the available space in the body
cavity after periods of intensive feeding (Hart & Gill
1992), this visceral displacement reduces the number of
prey that can be consumed during a single feeding bout
(Milinski 1985; Cunningham et al. 1994). In addition,
sticklebacks are known to maximize the number of prey
that can be consumed in one bout of feeding by packing
them into the stomach systematically (Hart & Gill 1992),
a process that requires extensive prey handling and orientation, and that may also be affected by the physical
presence of S. solidus.
Alternatively, the reduced success of infected fish in
competition with uninfected conspecifics at food patches
could be a result of their adopting a different feeding
strategy. Fish infected with S. solidus have higher nutritional demands than uninfected size-matched conspecifics (Pascoe & Mattey 1977), yet the experimental
evidence presented here and elsewhere suggests that they
are probably poor physical competitors for food. One
solution to this double-edged problem could be for
infected sticklebacks to maximize the postingestive transfer of energy and nutrients from their prey. Since bolting
food may have digestive costs (Pitcher & Parrish 1993),
infected fish may maximize their energetic gain from
foraging by ingesting food more slowly.
Although it is generally accepted that one of the main
costs of infection with debilitating parasites or other
pathogens is a reduction in the competitive ability of the
host, there are relatively few studies demonstrating such
effects in natural situations, and infected animals often
survive for long periods and stay healthy. Indeed, since
many parasites rely on the survival of their hosts to
enable essential development or reproduction, a complete infection-associated reduction in host competitive
ability would often appear counteradaptive. Schistocephalus solidus is such a parasite, since it needs to grow to
50 mg before it becomes infective to its subsequent host,
a piscivorous bird (Tierney & Crompton 1992). Infected
sticklebacks adopt several strategies that are thought to
enable them to overcome the twin effects of ‘poor’ competitive ability and increased nutrient demands associated with infection; they alter prey choice, both to
minimize competition levels (Milinski 1984) and to maximize energetic gain on a J/s basis (Cunningham et al.
1994); they are quicker to return to a foraging area after a
disturbance (Giles 1983, 1987b); and they leave foraging
groups more readily to exploit individual foraging opportunities (Barber et al. 1995). In addition, our results
suggest that where prey distribution varies between habitats, infected fish may also improve their foraging success
by moving to habitats where they can adopt behavioural
strategies that ensure prey are encountered in a manner
that enables them to maximize their competitive ability.
We have shown that the relative foraging success of
supposed poor competitors (infected sticklebacks) in
competition with uninfected conspecifics in short-term
feeding experiments is dependent on the type of competition conditions imposed. However, whether the differences in competitive ability we have shown are a direct
result of infection cannot be ascertained from our data.
One of the problems associated with studies using naturally infected host organisms is that it is often unclear
whether behavioural differences are a cause or a consequence of infection (Poulin 1995); in other words, poor
competitors in our study may be (for whatever reason)
more prone to infection, rather than the infection itself
causing poor competitive ability. Although this possibility cannot be ruled out in the stickleback–S. solidus
system, the former explanation is less likely to be the case
than the latter, since at least some of the behavioural
deviations associated with infection do not appear in the
infected fish until the parasite reaches a critical size
(Tierney et al. 1993). However, experimental studies that
assign infection status at random, using experimental
infections, are required to separate these two possibilities
definitively.
Acknowledgments
This work formed part of a NERC-funded Ph.D. studentship, completed by I.B. We are grateful to Felicity
BARBER & RUXTON: PARASITES AND COMPETITION IN FISH 1483
Huntingford and D. W. T. Crompton for discussions
relating to the experiments, and thank Neil Metcalfe,
Mark Witter, Paul Hart, Roger Hughes, Matthew Gibbons,
Kai Lindström and two anonymous referees for
comments on the manuscript.
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