Behavioral Ecology
doi:10.1093/beheco/arh127
Advance Access publication 21 July 2004
Risky decisions: a test of risk sensitivity in
socially foraging flocks of Lonchura punctulata
Gi-Mick Wua and Luc-Alain Giraldeaub
Department of Biology, Concordia University, bDépartement des sciences biologiques,
Université du Québec à Montréal, CP 8888, succursale Centre-Ville, Montréal,
Quebec H3C 3P8, Canada
a
Group foraging allows for individuals to exploit the food discoveries of other group members. If searching for food and
searching for exploitation opportunities within a group are mutually exclusive alternatives, the decision to use one or the other is
modeled as a producer-scrounger game because the value of each alternative is frequency dependent. Stochastic producerscrounger models generally assume that producer provides a more variable and uncertain reward than does the scrounger and
hence is a riskier foraging alternative. Socially foraging animals that are attempting to reduce their risk of starvation should
therefore alter their use of producer and scrounger alternatives in response to changes in energy budget. We observed flocks of
nutmeg mannikins (L. punctulata) foraging in an indoor aviary to determine whether their use of producer and scrounger
alternatives were risk sensitive. Analyses of the foraging rewards of three flocks of seven birds confirm that producer is a riskier
foraging strategy than is scrounger, although the difference in risk is rather small. We then submitted two other flocks to two
different energy budgets and observed the foraging decision of four focal birds in each flock. All but one bird increased their
relative use of the riskier producer strategy in the low food reserve treatment, but the overall use of producer did not differ
significantly between treatments, providing evidence for a small but consistent effect. Key words: energy budget, producerscrounger game, risk-sensitive foraging, social foraging. [Behav Ecol]
oraging groups provide animals with the opportunity to
exploit food discovered or otherwise made available by
other group members. This general form of exploitation or
joining has been documented in birds, fish, spiders, and
mammals (see Barnard, 1984; Giraldeau and Beauchamp,
1999 and references therein). Social foragers may be faced
with a decision if they can alternate between searching for
food or for joining opportunities, but not do both simultaneously (incompatible). There is evidence in some groundfeeding birds that the two alternatives are incompatible
(Coolen et al., 2001; Koops and Giraldeau, 1996), although
it is not universal (see Smith et al. 2002). This incompatibility
and its degree may depend on the visual, cognitive, or other
constraints of the animals that are specific to each foraging
system (Fernandez-Juricic et al., 2004). When the two foraging
alternatives are incompatible, the best allocation to each
strategy can be obtained by using a producer-scrounger (PS)
game analysis (Barnard and Sibly, 1981; Giraldeau and
Beauchamp, 1999; Giraldeau and Caraco, 2000). The payoff
structure of the PS game is such that either strategy pays more
than the other when rare. Thus, when scroungers are rare,
they should increase in frequency because scrounger pays
more than producer. This is because the scroungers can
exploit the discoveries of many searching individuals with very
little competition. When producers are rare, they will increase
because they do better than the numerous scroungers who
must then compete among themselves for the few available
discoveries. The result is that the payoff curves of producer
and scrounger strategists cross at an intermediate frequency
of scrounger: the stable equilibrium frequency (SEF; Mottley
and Giraldeau, 2000). Deterministic rate-maximizing PS
games hypothesize that animals attempt to maximize their
expected food intake and predict the SEF of scrounger within
F
Address correspondence to L-A. Giraldeau. E-mail: giraldeau.
[email protected].
Received 9 February 2004; revised 11 May 2004; 15 May 2004.
groups. Some empirical studies provide qualitative support for
their predictions (for reviews, see Giraldeau and Beauchamp
1999; Giraldeau and Caraco, 2000).
For small animals that have a high metabolic rate, however,
the probability of surviving some prolonged nonforaging
period, such as night for diurnal animals, may be more important than maximizing the expected intake while foraging
(Caraco, 1980). The energy budget rule (Stephens, 1981)
predicts that animals should prefer a less variable reward option
(risk-averse) when their expected energy budget exceeds the requirements to survive the nonforaging period and, conversely,
prefer a variable reward option (risk-prone) when expecting
to fall below this requirement. There is support for the energy
budget rule in small fishes, birds, and mammals (Bautista et al.,
2001; for a review, see Kacelnik and Bateson, 1996; Roche et al.
1998), in which individual subjects expecting an energy deficit
increased their preference for a variable (risk-prone) over
a constant (risk-averse) foraging option with equal means.
Likewise, if producer and scrounger strategies have different
variability and predictability of rewards associated with each,
then the SEF of scrounger in a group may also depend on the
energy budget of the foragers (Barta and Giraldeau, 2000;
Caraco and Giraldeau, 1991; Giraldeau and Caraco, 2000).
Stochastic PS models assume that producer generally yields
a more variable intake than scrounger and hence offers a riskprone alternative to group foragers (Barta and Giraldeau,
2000; Caraco and Giraldeau, 1991; Giraldeau and Caraco,
2000). Producer is often the more variable option because it
yields either no food or a large fraction of a food discovery:
the amount eaten before the arrival of scroungers plus the
amount shared with scroungers. Scrounger is usually the less
variable option because the animal has a more certain
provision of scrounging opportunities, each generating a small
fraction of the food discovery. Risk-sensitive PS models predict
that the group will reach a SEF of scrounger as a consequence
of individuals each attempting to minimize their probability
Behavioral Ecology vol. 16 no. 1 International Society for Behavioral Ecology 2005; all rights reserved.
Wu and Giraldeau
•
Risk sensitivity in flocks of Lonchura punctulata
of energy shortfall, so that the use of the foraging strategies
will vary with the individuals’ energy budget.
To date, only one published study experimentally tested
a risk-sensitive PS model. Koops and Giraldeau (1996) tested
Caraco and Giraldeau’s (1991) risk-sensitive PS model by
manipulating the energy budget of starlings (Sturnus vulgaris)
foraging in a group. Although the starlings responded to
altered patch encounter rates as predicted by the model, they
did not respond as predicted to different levels of food
deprivation. Moreover, no study to date has been able to
ascertain the validity of the assumption of the risk-sensitive PS
model concerning the risk-prone and risk-aversive qualities of
producer and scrounger, respectively. The difficulty in
measuring the profitability and the risk associated to the two
strategies resides in the fact that although one can count the
number of food patches discovered or joined by an individual,
the effort invested in each strategy is unknown (Giraldeau and
Caraco, 2000).
Coolen et al. (2001) recently developed a behavioral means
of continuously monitoring the strategy used by nutmeg
mannikins (L. punctulata) independently of whether they
actually find feeding opportunities or not. When these birds
forage in groups for seeds dispersed on a feeding table, the
position of the head while hopping provides an indication of
whether the bird is playing producer or scrounger. Hopping
with the head down is statistically correlated with patch finding
(producer); hopping with the head up, with patch joining
(scrounger). Individuals were found to adjust their investment
in alternative strategies in response to changes in foraging
conditions. When the foraging conditions offered few rich
patches that called for a higher SEF of scrounger (Giraldeau et
al., 1990), the birds settled on a higher rate of hopping with the
head up. In addition, Coolen and Giraldeau (2003) show that
increasing the distance between food and cover increases the
use of head up in stationary birds, but not the frequency of
hopping with the head up. They conclude that the latter is
dedicated to the detection of scrounging opportunities.
In the current study, we reproduce the experimental setup
of Coolen et al. (2001) as closely as possible and use the birds’
hopping with the head up and with the head down to measure their investment in producer and scrounger strategies,
respectively. We use these behaviors to investigate the payoff
structure and risk associated with both strategies. We then test
for risk sensitivity in the birds’ use of producer and scrounger
strategies when they are placed in conditions of low and high
energy budgets by food depriving them.
EXPERIMENT 1: PAYOFF OF PRODUCER AND
SCROUNGER STRATEGIES
Methods
Study subject
Nutmeg mannikins are small 13.7 6 0.2g (6SE, n ¼ 8)
granivorous birds originally from southeast Asia. In the wild,
they feed mostly by hopping on the ground or climbing tall
grasses and twigs in search of the seeds of grasses and weeds
(Immelmann, 1965). The sexes are monomorphic, and the
birds are social throughout the year.
We formed three flocks of seven randomly selected birds
from a colony of 97 wild-caught adult birds, and observed
them as they foraged in an indoor aviary (195 3 305 cm, 240
cm high) kept at 22 C–24 C and a 12-h light/12-h dark
photoperiod. Each bird was identified with a unique combination of two color leg bands, and before experiments, each
was given a different colored acrylic paint mark on the head
and tail. Water was available ad libitum at all times, as was
a mixture of millet seeds outside experimental periods.
9
Foraging apparatus
The birds foraged on a grid consisting of two plywood boards
joined to form a 2.0 3 1.2-m surface. The grid contained 198
wells in total (mean diameter and depth (6SE, n ¼ 10) of
1.32 6 0.02 cm and 0.83 6 0.01 cm, respectively) spaced on
average at 10.16 6 0.05-cm intervals. The grid rested 92 cm off
the aviary floor to allow a seated observer to film the birds by
using a handheld 8-mm color camcorder. Outside of experimental periods, a sheet of opaque paper covered the grid.
Training
After a 7–10-day habituation period in the aviary, the birds
were trained to search for white millet seeds placed in the
grid’s wells. Because these birds use their crop to store seeds,
they had to be food-deprived overnight (12 h) plus a short 3-h
period from lights on. The experimenter (G.M.W.) initially
placed a small handful of seeds around the center of the grid
and an increasing proportion of the seeds directly in the wells.
Once the birds were searching in the wells, they were exposed
to a dispersed food distribution (three seeds placed in each of
60 randomly pre-selected wells) and then to a clumped food
distribution (10 seeds placed in each of 20 randomly preselected wells).
A trial typically started once the experimenter left the aviary
and the birds flew down from their perches onto the grid.
Trials ended after 3 min of foraging or 1 min after all the birds
flew back to their perches, after which the remaining seeds
and husks were removed. Training consisted of six trials per
day at 30-min intervals. Under the dispersed food distribution,
the SEF of scrounger is expected to be low, whereas it should
be higher for clumped distributions (Coolen et al., 2001;
Giraldeau et al., 1990; Livoreil and Giraldeau, 1997). After
3 days of training in the dispersed food distribution, all birds
could find at least five patches per trial in three consecutive
trials. After 3 days of training in the clumped food distribution, all birds had joined at least three patches per trial
in three consecutive trials, and training was considered
complete.
Testing
Testing started the day after complete training and was carried
out on consecutive days. The flocks were food deprived and
given six trials per day on the clumped distribution as for
training. A different focal bird was randomly selected and
videotaped in each trial. The testing period was interrupted
once for each flock owing to the birds not flying down on the
grids to forage or to technical difficulties. Test days that immediately followed an interruption were discarded to reduce
possible effects of the interruption. Testing for flocks 1 and 2
was interrupted during two consecutive days, after which the
subsequent 2 days of testing were discarded. Tests for flock 3
were interrupted 1 day, after which the following day of
testing was discarded. Because tests that yielded less than 45 s
of observation were discarded, flocks were observed for
unequal number of days depending on their performance.
Flocks 1, 2, and 3 were tested for 15, 22, and 19 days,
respectively, such that each bird was observed at least six
times, on average 8.6 6 0.3 times (6SE, n ¼ 21).
Behavior patterns
Eight behavior patterns were noted from the video records by
using the Observer 3.0 event recorder software (60.1 s): (1)
finding a patch, (2) joining a patch, (3) eating a seed from
a patch that was found, (4) eating a seed from a patch another
bird found, (5) hopping with the head up, (6) hopping with
the head down, (7); stationary with the head up, and (8)
stationary with the head down. No aggression was observed
among the birds while foraging. A bird’s head position was
10
based on a projected line going from its eye through its nares.
The head was up when this line pointed to the horizon or
higher, and down otherwise (Coolen et al., 2001). A series of
hops was treated as continuous when each hop was separated
by less than 1.0 s. A bird remaining in one place for more than
1.0 s was recorded as stationary. Hops were categorized
a posteriori into pursuit and search hops (sensu Coolen et al.,
2001). The two hops immediately before a patch discovery
were defined as producer pursuit hops irrespective of head
orientation. A continuous series of hops in the same head
position immediately before a patch-joining event was defined
as scrounger pursuit hops irrespective of head orientation.
The remaining hops were categorized as producer search hops
if the bird had the head down, and scrounger search hops if
the bird had the head up. Hopping rate was calculated by
dividing the frequency of hops by their durations. Patch
encounter rate (patches per second) and seed intake rate
(seeds per second) were calculated for producer and
scrounger separately by dividing the number of patches and
seeds respectively, by the time invested in each strategy: the
sum of search, pursuit, and feeding times recorded for each
strategy. We calculated the proportional use of producer and
as the proportion of time which the bird had its head down
and up while searching, respectively.
Analysis
Analysis was limited to the first 60 s of each trial in order to
reduce the effect of patch depletion. From each trial in which
a bird was observed, we extracted all available 10-s sequences of
investments for producer and scrounger strategies and randomly selected one of each for analysis in order to avoid pseudoreplication. For each selected sequence, we calculated the
intake rate for producer or scrounger by dividing the number of
seeds from found or joined patches, respectively, by the time
invested in the sequence (10 s). We then used these estimates to
obtain the mean and coefficient of variation (CV) of intake rate
of producer and scrounger for each bird. We compared the
mean and CV of intake rates between strategies by using
repeated-measures ANOVAs with each bird as an independent
data point and blocking by flock. When homoscedasticity could
not be achieved among flocks, we analyzed them separately by
using paired t tests and combined the probability tests if they
were in the same direction (Sokal and Rohlf, 1981). In addition,
we used the cumulative frequency distribution of these intake
rates to estimate a bird’s probability of incurring an energy
shortfall as a function of energy budget for producer and
scrounger strategies. For each strategy, we averaged the
frequency distribution of intake rates of all birds and used
the log-likelihood ratio (Zar, 1996) to test for differences in the
distribution of intake rates between strategies. Statistical tests
were run on SPSS 10.0 and were two-tailed.
Results
General results
A total of 182 trials yielded 335.6 min of foraging for 21
subjects. Only 14 trials (8%) included disruptions, which
together lasted 5.8 min, leaving a total of 329.8 min of
observation time. The birds flew down on the grid and
foraged on average (6SE, n ¼ 21) 110 6 14 s per trial. They
spent 52.9 6 6.6% of their time feeding in patches, 39.3 6
6.6% hopping, and 7.8 6 5.1% stationary. During the average
trial, a bird obtained 9.6 6 5.1 seeds from 1.9 6 1.1 discovered
patches, and 7.7 6 4.4 seeds from 3.1 6 1.9 joined patches.
Behavioral indicators of strategy use
The proportion of time a bird had its head up while searching
was a strong predictor of the proportion of patches that a bird
Behavioral Ecology
Figure 1
Correlation between the proportion of patches joined by a bird
and the proportion of time it had the head up while searching. Each
point is the average of six to 10 trials for one bird (n ¼ 21).
joined (arcsine-square root transformation) among the
patches from which it fed (partial correlation, controlling
for flock: r ¼ .71, df ¼ 18, p , .001) (Figure 1). In addition
a two-way repeated-measures ANOVA testing for strategy
(producer/scrounger) and hop type (search/pursuit) with
flocks as a between subject factor, showed that scrounger hops
occurred at a higher rate than producer hops (F1,18 ¼ 8.32,
p ¼ .01). Birds also hopped at a higher rate during pursuit
than during search (F1,18 ¼ 8.02, p ¼ .01), more so for
scrounger, but the interaction between the two factors was
marginally nonsignificant (F1,18 ¼ 4.33, p ¼ .05).
Payoffs of producer and scrounger strategies
One bird was excluded from the analysis of payoffs, because it
played scrounger too rarely to provide sufficient data for
a comparison of strategies. Data from the remaining 20 birds
showed that birds had a significantly lower mean (6SE, n ¼
20) patch encounter rate while playing producer (0.075 6
0.003 patches/s) than scrounger (0.162 6 0.007 patches/s)
for an equal time investment (repeated-measures ANOVA
testing for strategy and flock effects: F1,18 ¼ 153.28, p , .001).
On the other hand, birds obtained significantly more seeds
from finding a patch (producer, 5.0 6 0.2 seeds) than joining
one (scrounger, 2.6 6 0.1 seeds; repeated-measures ANOVA
testing for strategy and flock effects: F1,18 ¼ 198.85, p , .001).
The resulting seed intake rate for producer (0.21 6 0.02
seeds/s) was lower than for scrounger (0.25 6 0.01 seeds/s)
but not significantly (repeated-measures ANOVA testing for
strategy and flock effects: F1,18 ¼ 2.46, p ¼ .14). The variability
of intake rates as measured by the mean coefficient of
variation (CV) was significantly higher for birds while
producing (1.00 6 0.02) than scrounging (0.55 6 0.01;
combined probability of paired t tests for three flocks: v26 ¼
20.32, p , .01). This payoff structure tends to produce a lower
probability of incurring an energy shortfall for scrounging
birds than for producing birds at the lowest food intake
requirements and the reverse at the highest food intake requirements (Figure 2). The analysis of the frequency distribution of intake rates however, reveals that this pattern is
nonsignificant (log-likelihood ratio: G ¼ 4.25, df ¼ 3, p , .25)
(Figure 3).
Wu and Giraldeau
•
Risk sensitivity in flocks of Lonchura punctulata
11
Figure 2
Probability of incurring an energy shortfall relative to the required
intake rate for producer (filled squares) and scrounger (open
squares) strategies (n ¼ 20).
EXPERIMENT 2: TESTING FOR
A RISK-SENSITIVE DECISION
Methods
Estimating daily food requirement
We estimated the daily food requirement (grams of seeds) of
eight L. punctulata randomly chosen from the same pool of 97
birds as used in experiment one. The birds were kept singly in
cages (30 3 30 cm, 34 cm high) during 14 days of measurement. The birds maintained visual and auditory contact with
others but fed from separate feeders hanging outside their
cages. Each feeder contained 10.00 g of white millet seeds,
and was changed daily 2 h after lights on. The used feeder was
cleared of its empty husks and weighed. The birds were also
weighed daily at the same time the feeders were changed.
Manipulation of energy budget
Two flocks of seven individuals were randomly selected from
the 68 birds of the colony that had not been used in other
parts of this study. They were habituated to an aviary for 14
days and trained to forage on a grid as in experiment 1. Flocks
were then given four trials per day. To modify their energy
budget, they were subjected to the following two controlled
feeding schedules. At the beginning of the second half (6 h)
of the day preceding a test, flocks were given either 50% (low
energy budget) or 100% (high energy budget) of their
estimated food intake for that period. They were then food
deprived overnight for 12 h plus 2 h after lights on before
testing. Testing always ended after 1.5 h, and birds always had
2 h of ad libitum feeding 30 min after the end of testing. Birds
were tested on consecutive days for each treatment, and the
treatment order was balanced between flocks. Birds were
allowed 7 days of ad libitum feeding and were subject to
another 3 days of training between the first and second
treatments.
Analysis
We selected four birds randomly in each flock as focal birds,
and recorded their behavior during the first 60 s of
observation in each trial. We obtained data for each bird by
averaging the measures of all trials for each treatment.
Repeated-measures ANOVAs tested for effects of energy
budget treatment on the birds’ foraging behavior, blocking
by flock. Proportions were arcsine-square-root transformed to
achieve normality and homoscedasticity (Zar, 1996). When no
transformation could achieve homoscedasticity between
Figure 3
Frequency distribution of intake rates for producer (filled bars) and
scrounger (open bars) strategies (n ¼ 20).
flocks, we analyzed them independently and combined the
probability tests if they were in the same direction (Sokal and
Rohlf, 1981). Again, all tests were two-tailed.
Results
General
The birds’ average (6SE, n ¼ 8) food requirement was 3.7 6
0.3g of millet per day and was not correlated to their weight
(13.7 6 0.2g). Results of flock foraging are based on 163 trials
(approximately 10 trials per bird per treatment), yielding
310.9 min of foraging for all eight birds. Flocks foraged as in
the previous experiment except that disruptions occurred
more frequently than in experiment 1. A total of 71 trials
(44%) included disruptions that lasted a total of 30.4 min.
Removing the disruptions left 280.5 min of observation time.
The birds flew down on the grid and foraged for 114 6 3 s per
trial. They spent 49.9 6 2.4% of their time feeding in patches,
37.4 6 2.7% hopping, and 12.7 6 2.3% stationary.
Effects of energy budget
Birds hopped at a significantly higher rate in the low energy
budget treatment (20 6 1 hops/s) than in the high energy
budget treatment (18 6 1 hops/s; combined probability of
paired t tests for both flocks: v24 ¼ 11.57, p ¼ .02) (Figure 4a).
Birds also consumed more seeds per trial under low energy
budget (20 6 1 seeds) than under high energy budget (18 6 1
seeds; repeated-measures ANOVA: F1,6 ¼ 7.64, p ¼ .03) (Figure
4b). There was no significant interaction between factors. All
but one bird searched with the head down proportionally more
in the low energy budget than in the high energy budget
treatment (binomial probability: p ¼ .03). Nevertheless, the
mean proportion of time they had the head down while
searching (producer) did not increase significantly from high
energy budget (0.73 6 0.05) to low energy budget (0.82 6 0.03;
combined probability of paired t tests for each flock on arcsine
square-root transformed data: v24 ¼ 7.38, p ¼ .12) (Figure 4c).
DISCUSSION
The present study provides evidence for risk sensitivity in the
PS game in socially foraging nutmeg mannikins. More
precisely, results from the first experiment show that producer
12
constitutes a riskier foraging alternative than does scrounger
as generally assumed by stochastic PS models. The second
experiment reveals that the birds increase their relative use of
the producer strategy in response to a decrease in energy
budget. We discuss the implications of the two experiments
in turn.
Our conclusions rest on the assumption that a bird’s head
position indicates its foraging strategy. This assumption is
based on results provided by Coolen et al. (2001) using the
same species of birds foraging in the same experimental
apparatus. Moreover, our current results support those of
Coolen et al. (2001) because we observed a strong correlation
between the proportion of patches that a bird joined and the
proportion of time that it had its head up while hopping. In
addition, we found that our birds hopped at a higher rate
when they had the head up than when they had the head
down. The slower hopping with the head down may reflect
that seeds are more difficult to detect than a feeding
conspecific. It follows that nutmeg mannikins may need to
slow down their hopping rate when playing producer and
even more so when prey crypticity increases (see Gendron and
Staddon, 1983; Pyke, 1981; Speakman, 1986). Thus, our
results suggest that an individual’s hopping rate may ultimately be used as another indicator of strategy use by nutmeg
mannikins. Our estimates of intake rate and risk may not be
accurate if the birds could also find food patches or feeding
conspecific by using other behaviors. Conceivably, an individual may have been able to detect a feeding conspecific by
looking up while remaining in one place. However, we feel
this is unlikely given that Coolen and Giraldeau (2003) found
a correlation between stationary behaviors with the head up
and simulated predation threat but not joining frequency.
We are therefore confident that our measure of head position while hopping was an effective indicator of foraging
strategy use.
The analyses of producer and scrounger intake rates in
experiment 1 show that producer is a riskier foraging strategy
than is scrounger in nutmeg mannikins. When playing
producer, the birds have a lower patch encounter rate than
when playing scrounger, so it follows that they run a higher
chance of not obtaining any food at all by playing producer.
Our results allow us to go further and show for the first time,
that a bird has a higher variability (CV) of intake rate when
playing producer than scrounger in this species. This difference in variability constitutes the basis for risk-sensitive
foraging (Caraco, 1980; McNamara and Houston, 1992;
Stephens, 1981) and is consistent with the common assumption of stochastic PS games (Barta and Giraldeau, 2000;
Caraco and Giraldeau, 1991). A study of socially foraging
starlings (Koops and Giraldeau, 1996) previously showed that
an individual’s intake within a patch is more variable when the
patch is discovered than joined. The latter however is not
sufficient because it did not take into account the effort
required to obtain each feeding opportunity, hence the net
intake rate. Although the higher variability in producer intake
rate in the present study strongly suggests that it is a riskier
foraging strategy than is scrounger, it may not be the case if
mean intake rates differ greatly. We did not find a significant
difference in the mean payoff obtained from using either of
the two strategies as predicted by rate-maximizing games for
foragers at the SEF (Barnard and Sibly, 1981; Vickery et al.,
1991). The observed power of the test (1-b ¼ 0.32), however,
does not totally exclude this possibility. A small difference in
mean intake rate however, is expected because producer and
scrounger birds are predicted to have equal probabilities of
falling bellow their requirement, not equal mean intake rates
(Barta and Giraldeau, 2000; Caraco and Giraldeau, 1991).
The frequency distribution of intake rates also suggests that
Behavioral Ecology
Figure 4
Mean þ SE (n ¼ 8–11) hopping rate (a), number of seeds eaten in
a trial (b), and proportion of time searching as scrounger (c) in the
high (blank) and low (filled) energy budget treatments.
producer is riskier than is scrounger, but the two distributions did not differ significantly. Overall, our results indicate a
potential for a risk-sensitive PS game in our system. The small
difference in risk that we observed may not be biologically
significant, especially at high required intake rates, at which
the differences between strategies are minimal. This may lead
to risk-insensitive decisions (Shafir and Trivaks, 2000) or to
effects that may be too small to be detectable (Barta and
Giraldeau, 2000). In such cases, deterministic rate-maximizing
models would appear sufficient to predict the animal’s
foraging decision.
Despite the small difference in risk noted in the first experiment, the second experiment reveals a limited but consistent
increase of producer use with a decrease in energy budget. We
discuss possible causes for the small amplitude of the birds’
response to energy budgets and the implications of the result
Wu and Giraldeau
•
Risk sensitivity in flocks of Lonchura punctulata
for risk-sensitive PS games as well as for the energy budget
rule.
The small amplitude of the effect of energy budget on
producer use is not likely owing to an ineffective treatment.
Although the birds may have increased their food intake
during the ad libitum feeding period that preceded the 6 h of
low food availability, they were not likely to compensate fully
for the following treatment, as these birds ingest approximately 45% of their daily intake in the first half of a 12-h
photoperiod (Trudeau LE, unpublished data). In addition,
the birds are also not likely to accumulate large food or fat
reserves early in the day because the consequent mass gain
can impair locomotion and result in an increased vulnerability to predators (see Burns and Ydenberg, 2002; Metcalfe and
Ure, 1995). Our birds responded to the low energy budget
treatment by hopping at a higher rate and by eating more,
indicating that they were hungrier. Instead, the small
amplitude of the change in producer use may be owing to
the negative frequency dependence of the payoffs in a PS
game (Barnard and Sibly, 1981). As an individual increases its
use of one strategy, the other strategy will become relatively
more profitable. Thus an individual can only shift its use of
foraging strategies slightly without a significant trade-off in
expected intake rate, which in all cases is a significant factor in
survival probability (Barnard et al., 1985). Nonetheless, even
small differences in risk may be biologically significant
because an energy deficit can have important consequences
for the animals, such as the failure to migrate (Bednekoff and
Houston, 1994), decreased reproduction (McNamara et al.,
1991; Schmitz, 1992), or starvation (Barkan, 1990; McNamara
and Houston, 1986). Because our small birds had been food
deprived for 14 h in addition to a reduced intake the previous
day in the low energy budget treatment, the perceived risk of
starvation was likely considerable. Furthermore, small differences in survival probability on a short time scale become
significant over an animal’s reproductive lifetime (McNamara
and Houston, 1982).
The observed increase in preference for risk or producer
use with a decreasing energy budget in our small nutmeg
mannikins has implications for a number of theories. It is
consistent with the energy budget rule and other tests of the
model done on small animals choosing between two prey
types (Bautista et al., 2001; Kacelnik and Bateson, 1996 and
references therein). Our result therefore adds to other studies
suggesting that small homeothermic animals respond to
energy budget manipulations in a shortfall minimizing manner. In addition, our results indicate that the prediction of the
energy budget rule with solitary foragers in mind extends to
the choice of producer and scrounger strategies in feeding
groups of nutmeg mannikins, as hypothesized by risk-sensitive
PS games (Barta and Giraldeau, 2000; Caraco and Giraldeau,
1991). The stochastic PS model (Caraco and Giraldeau, 1991)
predicts that a change in the energy budget of group members will affect their use of producer and scrounger strategies
depending on group size and the producer’s competitive
efficiency, the proportion of a food patch that goes to its
finder. For the present study, with a group size of seven and
a competitive efficiency of 0.59, the model predicts a small
decrease of producer use with a decreasing energy budget.
Our birds’ response was the reverse, but we cannot reject the
model because certain assumptions of the model such as
sequential patch discoveries and long search times relative to
patch time were not met. Nevertheless, it may be that the
former model is too simplistic. A dynamic stochastic PS model
(Barta and Giraldeau, 2000) assumes that foragers maximize
their survival probability throughout the day, and predicts an
increase in producer use with a decreasing energy budget
when they are very close to immediate starvation. For diurnal
13
animals, this is more likely to occur in the morning, because
they cannot feed during night. Our birds foraged during the
morning and their response to increased food deprivation is
consistent with the prediction of the model. Nevertheless, an
explicit test of both risk-sensitive PS models is required to
determine which theory is more applicable to socially foraging
nutmeg mannikins and to ground feeding birds in general.
We thank Zoltan Barta, Thomas Caraco, and two anonymous reviewers for useful comments on a previous version of the manuscript.
This research was conducted in partial fulfillment of the degree of
masters in Biology of Concordia University and was financially
supported by a Natural Sciences and Engineering Research Council
of Canada research grant, as well as by a Fonds pour la Formation de
Chercheurs et l’Aide à la Recherche du Québec to L.A.G. G.M.W.
received financial support through teaching assistantships provided
by the Department of Biology of Concordia University as well as from
National Environment Research Council Discovery, FQRNT Team,
and PAFARC (UQÀM) research grants to L.A.G. All experiments
reported here were conducted under the guidelines of the Canadian
Council for Animal Care and were approved by the Concordia University Animal Care Committee.
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