Behavioral Ecology Vol. 10 No. 4: 391-395
© 1999 International Society for Behavioral Ecology
Intraflock variation in the speed of escape-flight response on attack by an avian predator
Ornithology Group, IBLS, University of Glasgow
Address correspondence to W. Cresswell, who is now at the Edward Grey Institute, Department of Zoology, South Parks Road, Oxford OX1 3PS, UK. E-mail: juniper{at}beetle.u-net.com
Received 30 October 1998; revised 14 December 1998; accepted 21 December 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The benefits of flocking to prey species, whether through collective vigilance, dilution of risk, or predator confusion, depend on flock members responding in a coordinated way to attack. We videotaped sparrowhawks attacking redshank flocks to determine if there were differences in the timing of escape flights between flock members and the factors that might affect any differences. Sparrowhawks are surprise short-chase predators, so variation in the time taken to take flight on attack is likely to be a good index of predation risk. Most birds in a flock flew within 0.25 s of the first bird flying, and all birds were flying within 0.7 s. Redshanks that were vigilant, that were closest to the approaching raptor, and that were close to their neighbors took flight earliest within a flock. Birds in larger flocks took longer, on average, to take flight, measured from the time that the first bird in the flock flew. Most birds took flight immediately after near neighbors took off, but later flying birds were more likely to fly immediately after more distant neighbors took flight. This result, along with the result that increased nearest neighbor distance increased flight delay, suggests that most redshanks flew in response to conspecifics flying. The results strongly suggest that there is significant individual variation in predation risk within flocks so that individuals within a flock will vary in benefits that they gain from flocking.
Key words: Accipiter nisus, collective detection, escape response, flocking, predation risk, reshanks, sparrowhawks, Tringa totanus.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Flocking in animals provides antipredation benefits in three main ways: through vigilance effects, the dilution effect, and the confusion effect. Vigilance benefits arise because, as flocks get larger, the probability of detecting an approaching predator can increase even as individual vigilance rates decline (Elgar, 1989
;
Pulliam, 1973; but see
Bednekoff and Lima, 1998).
Dilution benefits arise because the probability of an individual in a flock
being the victim will decrease as flock size increases
(Foster and Treherne, 1981;
Hamilton, 1971). Confusion
benefits arise because it is harder for predators to deal with multiple
targets. The benefits of each effect, however, depend on the degree of
coordination between the flock members
(Packer and Abrams, 1990;
Vine, 1971). Any benefits of
flocking that depend on vigilance depend on the rapid transmission of
information of the approach of a predator from those individuals that are
vigilant at the time to those that are not
(Lima, 1995b). The dilution
effect assumes that all individuals within a flock are at equal risk of
predation during an attack and therefore depends on all flock members behaving
in the same way (Foster and Treherne,
1981; Hamilton,
1971). The confusion effect relies on the flock remaining as a
coherent unit and so also depends on all flock members behaving in the same
way (Neill and Cullen, 1974).
Although the theoretical benefits of flocking depend on uniformity of
response, in reality it is unlikely that all flock members will respond in the
same way to an attack.
When a predator attacks a flock, it is unlikely that flock members will
escape at the same time. Vigilant individuals may make an escape response
immediately, but an individual engaged in an activity such as feeding that is
incompatible with an instant escape response may respond later
(Fitzgibbon, 1990;
Krause and Godin, 1996). Any
behavioral variation in response of flock members to attack by a predator will
lead to a reduction in flock cohesion. Therefore, variation in the speed of
escape response of flock members to attack is crucial to the benefits that
accrue from vigilance, dilution, or confusion, and the evolution of flocking
behavior (McNamara and Houston,
1992; Packer and Abrams,
1990). Although it may appear self-evident that a vigilant
individual is likely to respond sooner than a nonvigilant individual, for
example, it is the magnitude of the difference that is most important. Despite
the potential importance of individual variation in the speed of escape
response when attacked to the theoretical consideration of the benefits of
flocking, there are few quantitative data on the actual time taken to escape,
or on the factors affecting escape time
(Kenward, 1978;
Lazarus, 1979;
Lima, 1994b,
1995a,
b).
There are several factors that probably do affect speed of escape response,
such as the number and position of vigilant individuals and the overall
position and spacing of individuals within a flock. A nonfeeding and/or
vigilant individual is more likely to notice and escape immediately as a
predator approaches (Elgar et al.,
1986; Lima,
1994b). A flock member that is not vigilant at the time of the
attack probably responds to the escape flights of its near neighbors
(Davis, 1975;
Lima, 1995b). Although an
approaching but distant predator may not be visible to a feeding bird, the
rapid flight of a near neighbor is likely to be obvious, particularly if the
prey species has a conspicuous signal on flight
(Brooke, 1998). The likelihood,
and therefore speed, on average, of a flock member noticing a neighbor flying
off is probably dependent on the spacing within the flock. An individual with
only distant neighbors will be less likely to respond quickly. The overall
speed of the flock response should therefore increase as nearest neighbor
distance decreases (Lima and Zollner,
1996;
Pöysä,
1994). Where flocks are well spaced, individuals that are closest
to the approaching predator may also be more likely to respond quickest
because they are more likely to detect the predator's approach first. The time
taken for all of the flock to take flight, after initial predator detection,
should also increase with flock size because there will usually be relatively
fewer vigilant individuals within a larger flock
(Cresswell, 1994b;
Elgar, 1989;
Pulliam, 1973). Therefore, the
ratio of birds responding to the escape flights of conspecifics, rather than
responding to the predator, will increase with flock size.
In this study we measured individual variation in the time taken to fly on
attack by videotaping flocks of redshanks that were being attacked naturally
by sparrowhawks. In the study system, redshanks feed on an area of salt marsh
adjacent to a wood at average distances to cover of only 20-30 m (see
Cresswell, 1994a). The
redshanks are attacked by surprise by a sparrowhawk usually flying out of
cover (Cresswell, 1996) and
escape by flying away from the sparrowhawk and to cover
(Cresswell, 1993). The speed at
which the individual redshanks can get into the air and fly away from the
sparrowhawk determines the probability of capture
(Cresswell, 1994a;
Newton, 1986). Fast, coherent
escape responses are probably important because an individual redshank may
have around a 90% probability of being killed by a sparrowhawk at some time
during the winter period (Cresswell and
Whitfield, 1994). In this study we tested the hypotheses that
individuals closest to the approaching predator and individuals that were
vigilant at the time of attack would be more likely to be the first birds in a
flock to fly from the predator. We tested the hypothesis that as flock size
increased, more birds of the flock would fly later. We also tested the
hypothesis that birds with more distant neighbors would fly later than flock
members with close neighbors.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Data were collected from flocks of common redshanks (Tringa totanus) wintering at the Tyninghame estuary on the Firth of Forth, Scotland, during the first 9 weeks of, 1998. Full site details are given in Whitfield (1985
) and Cresswell
(1994a). Redshank flocks were
videotaped using a Sony Hi-8 video camera with a frame resolution of 0.02 s.
Flocks were videotaped feeding on an area of salt marsh from a distance of
30-300 m by a single observer (G.H.) sitting on the edge of the salt marsh.
Eurasian sparrowhawks (Accipiter nisus) attacked the redshank flocks
by flying out of the woods or bushes surrounding the salt marsh directly
toward the redshanks (see Cresswell,
1996). The camera was set to record a flock continuously, and an
attack and response sample was collected opportunistically each time a
sparrowhawk attacked the flock being videotaped. The direction of attack of
the sparrowhawk was recorded at the time by the observer, who was free to scan
the area constantly for attacking sparrowhawks. Attacks probably came from two
to three individual female sparrowhawks, and the redshanks attacked on the
salt marsh were probably the same individuals (see
Cresswell and Whitfield,
1994). Redshank flocks attacked ranged in size from 7 to 61 birds,
with a median flock size of 23.5 (16-30); between 200 and 400 redshanks feed
regularly on the salt marsh (Cresswell and
Whitfield, 1994).
We successfully videotaped 38 attacks where a sparrowhawk flew directly and
rapidly toward a flock of redshanks, and all of the flock members took flight
away from the sparrowhawk. Three of the attacks (8%) that were sampled
resulted in capture and death of a redshank. The success rate of attacks that
led to kills in this study was therefore similar to previous studies on the
site that determined that redshanks were at great risk from sparrowhawk
attacks (12%, n = 538 attacks in
Cresswell, 1996). Each attack
was analyzed using a frame-by-frame video player. The flight speed of a
sparrowhawk during an attack was estimated from attacks in which the raptor
was filmed flying past marker posts set at 20-m intervals on the salt marsh.
The number of frames taken to travel 20 m could be accurately determined for
four attacks.
For each attack, the redshank that flew first was identified, and the frame when that bird flew was defined as frame zero. Every other flock member was then scored for the frame number when it first took flight relative to the frame when the first bird of the flock took off. The distance of the bird's nearest neighbor (in body lengths) and the distance between the bird and its nearest neighbor to fly in the last frame (i.e., the closest bird to fly previously) was also recorded. We also recorded whether the bird had its head up during the frame immediately before frame zero (just before the attack). Finally, the position of the bird within the flock was recorded with respect to the direction of the approaching sparrowhawk. The flock was split into quarters so that approximately one-quarter of birds were scored as being closest to the approaching sparrowhawk and one-quarter were scored as being farthest from the raptor. The quarters were defined by equal numbers of birds in each quadrant because the flocks were reasonably evenly spread; each quadrant therefore also represents approximately a quarter of the area of the flock.
We analyzed data using the SPSS statistical programs
(Norusis, 1990). All
probabilities quoted are two-tailed. Where means are given, they are in the
form of mean ± standard error; where medians are given they are in the
form median and 95% confidence limits (see
Campbell, 1989).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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General pattern of response times
Half of the flock members flew on average 0.18 s after the first bird had flown (Figure 1). The time taken for all flock members to take flight after the first bird had flown was approximately 0.7 s (Figure 1). Sparrowhawks approached the redshank flocks during an attack at an average speed of 25 m/s (range 20-28, n = 4 attacks).
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Individual variation in response times
Redshanks that were closest to the approaching raptor took flight on
average sooner than those birds at the back of the flock
(Figure 2). The overall median
difference in response time comparing individuals in the closest quarter of
the flock with those in the farthest quarter was a median of 0.09 s
(0.02-0.12; Wilcoxon signed-ranks test, matched pairs from n = 37
attacks, z = -3.2, p = 0.002). The analysis was limited to
37 cases because with 1 flock it was impossible to determine the approach
direction of the raptor accurately. Redshanks that had their heads up just
before the first flight in response to the attack flew earlier on average,
with a median of 0.07 s (0.05-0.12) than those redshanks that had their heads
down within the same flock (Wilcoxon signed-ranks test, matched pairs from
n = 15 attacks, z = -3.3, p =.001). The analysis
was limited to 15 cases because only 15 flocks were videotaped close enough to
discern head position accurately for each flock member. Those birds that had
their heads up just before the attack were distributed randomly with respect
to the direction of the approaching raptor (Kruskall-Wallis nonparametric
ANOVA of head-up frequency by flock quarter, 
23 =
1.3, p =.73). Redshanks that had close nearest neighbors (
5 bird
lengths away) took flight more quickly on average than those redshanks with
distant nearest neighbors (>5 bird lengths away). The overall median
difference in response time comparing individuals with near neighbors with
those with far neighbors in the same flock was 0.07 s (0.02-0.12; Wilcoxon
signed-ranks test, matched pairs from n = 29 attacks, z = -
3.0, p =.003). The analysis was limited to 29 cases because only 34
flocks were videotaped close enough so that nearest neighbor distance could be
determined accurately, and of these flocks only 29 had birds within both
classes.
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The mean time taken for all the flock to take flight (measured from the time that the first bird of a flock flew) was dependent on flock size. This result was confounded by the relationship between flock size and nearest neighbor distance. As flock size increased, the nearest neighbor distance decreased (Spearman's rank correlation, rs = -.44, n = 34 flocks, p =.009). The analysis was restricted to 34 flocks because nearest neighbor distance could not be determined accurately for four flocks videotaped at a distance. When mean nearest neighbor distance was controlled for using partial correlation, there was a significant increase in the time taken for a bird to fly as flock size increased. The time taken for the entire flock to take flight was greatest for larger flocks (Kendall's partial correlation coefficient of mean flock size with time of the last bird in the flock to fly, controlling for nearest neighbor distance = 0.45, n = 34 attacks, p =.008). The mean time taken for a bird in the flock to take flight was also greatest for larger flocks (Kendall's partial correlation coefficient of mean flock size with mean time of the birds in the flock to fly, controlling for nearest neighbor distance = 0.38, n = 34 attacks, p =.03).
Transmission of the flock response
The majority of birds flew immediately after one of their near neighbors
took flight (Figure 3).
Approximately 46% of individuals, on average, flew immediately after a
neighbor within three body lengths took off. Those birds that flew early
during an attack were much more likely to fly immediately after a near
neighbor took flight. Birds that flew later during an attack were more likely
to fly immediately after birds much farther away took flight, even when
controlling for the effects of nearest neighbor distance
(Figure 4). The median
difference in the distance between a bird taking flight and the closest bird
to take flight previously, in the first 0.1 s, compared to later flying birds,
was 5.2 (1-8.7) bird lengths (Wilcoxon signed-ranks test, matched pairs from
n = 11 attacks, z = -2.9, p =.003). The previous
analysis was restricted to birds of the same nearest neighbor distance (no
more than one body length) within the same flock to control for the
confounding effects of those birds with far neighbors being more likely to fly
later. Data were only available from 11 flocks under these conditions.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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In general, although the relative time of escape flight depended on vigilance state, position with respect to the approaching raptor, distance from neighbors, and flock size, differences in response time due to these factors might be considered small (see also Lima, 1994b
). The maximum
effect of any of the factors acting singly was to reduce escape flight time on
average by a maximum of approximately 0.1 s. This would translate to a less
than 3 m decrease in the distance that a sparrowhawk could approach toward a
flock (using the estimate of 25 m/s approach speed from this study). During
the study, redshanks frequently fed at distances of less than 10 m to cover,
and it is possible therefore that even the small delays in initiating an
escape flight in this study make a real difference to capture probability. The
effect of any decreases in the distance between the sparrowhawk and a redshank
before it flies will also be multiplied in the sparrowhawk's favor because a
sparrowhawk will typically be flying close to maximum velocity before a
response, while a redshank will have to accelerate from zero. It was not statistically possible to analyze the interaction between the various factors because of small sample sizes. It was likely, however, that a nonvigilant individual with no near neighbors would fly later than 0.1 s after the first bird in the flock flew. A few birds flew after 0.5 s (see Figure 1), although none flew later than 0.7 s. A 0.5-s delay in initiating an escape flight might allow a sparrowhawk to approach approximately 12.5 m closer, a distance likely to increase capture probability within the study system. Delays in flight caused by position with respect to the approaching raptor may have not have had any detrimental effects, however. Birds farther back in the flock flew on average about 0.09 s later than those in the front did. If a sparrowhawk travels at 25 m/s, then it will only decrease its distance toward the front of the flock by 2.25 m. Most redshank flocks were spread over at least 10 m, and so those birds at the back will have actually taken flight farther away from the sparrowhawk than early flying birds. Delays in initiating escape flight might be especially disadvantageous, however, if the attacking sparrowhawk preferentially targets late-flying birds.
Birds in larger flocks took longer on average to take flight upon attack.
It is important to note that the variable measured in this study was the time
taken for individuals within a flock to take flight relative to the time when
the first bird took flight. No measurement could be taken of how far the
sparrowhawk was from the flock at the instant when detection occurs, if there
was a lag between detection and flight. Although larger flocks took longer on
average to take flight, they may have detected the sparrowhawk earlier than
smaller flocks because of the vigilance characteristics of larger flocks. The
first bird to take flight in a large flock may then have taken flight much
sooner than the first bird in a small flock. The fact that larger flocks took
longer on average to take flight may then be explained because individuals in
larger flocks do not have to respond as quickly, being protected by increased
approach time of the predator and increased dilution and confusion effects.
Advantages of delaying an escape flight could be the prevention of false
alarms (Lima, 1995b) and
identification of the approaching predator so that the correct escape response
is made (see Cresswell, 1993).
Alternatively, larger flocks would have had fewer vigilant individuals (see
Elgar, 1989;
Pulliam, 1973). The number of
birds initially sighting and taking off in response to the approaching raptor
in larger flocks would then be relatively small. Any effects of increasing
flock size on overall response time should be small, however, because when
each bird has several near neighbors then the flight response should propagate
exponentially.
Some of the delay in initiating flight was probably due to transmission of
the escape response information through the flock rather than due to
individuals delaying flight after they had detected the approaching
sparrowhawk. This is shown by the result that birds with only far neighbors
were much more likely to fly later. Birds without near neighbors would benefit
less from the dilution effect (Hamilton,
1971) and probably also the confusion effect
(Neill and Cullen, 1974). It
seems unlikely, therefore, that birds with far nearest neighbors would delay
flight relative to conspecifics within the same flock on the grounds of
reduced risk. The delay in initiating flight may therefore have simply been
because any visual stimulus will be smaller as its distance away from the
receiver increases (see Lima and Zollner,
1996). This may also have been demonstrated in this study by the
result that those birds nearest to the approaching raptor responded before
those farther away. It also seems most likely that individuals in a flock were
responding to the escape flights of their near neighbors because the pattern
of response changed with time (see Figure 6). Initially an individual may have
spotted an attacking sparrowhawk and then flown, followed rapidly by its near
neighbors. Later flying birds were, however, more likely to fly immediately
after more distant birds flew. This would be expected because as more birds
flew, the size of the visual stimulus increased and the response became
increasingly more detectable to distant birds. The effect of decreasing
nearest neighbor distance increasing the probability of a rapid escape
response has important consequences for flock spacing. In any flock, there
will be a trade-off between the benefits of close spacing to maximize flocking
benefits, and the benefits of feeding well away from conspecifics to maximize
feeding rates (Barta et al.,
1997). The results from this study suggest that any assessment of
the costs of dense flocking must be considered with the potential benefits of
rapid and coordinated responses.
There was no evidence from this study of any significant ambiguity or
uncertainty within the process of collective detection as reported from
studies by Lima (1995b). In
dark eyed juncos Junco hyemalis not all birds responded to the escape
flights of conspecifics, and the proportion of birds responding was context
specific. In Lima's study, however, threats were artificially provided, and it
is possible that flights by detectors in response to the experimental threat
were in some way different from "real" escape flights. Lima
(1994a) suggests that an
increase in attack rate should lead to greater responsiveness to departures in
nondetectors. Given a particularly high rate of attack (and the system in our
study probably fits here), it is then conceivable that nondetectors might
initiate escape upon detecting a single bird departing the flock, leading to
our observation of little ambiguity in collective detection. However, flight
responses that are apparently mistakes occur frequently in redshanks
(Cresswell, unpublished data), and in some of these not all flock members fly.
These observations, along with the data from this study, suggest that there
may be some unambiguous information of perceived threat within a flight
response to an approaching predator. It seems likely that efficient collective
detection would benefit all flock members because a successful predator is
probably more likely to return to the same area in the future. This probably
applies particularly to Accipiter hawks that are generalist predators
that readily adopt local prey specializations
(Cresswell, 1995;
Cresswell and Whitfield, 1994;
Newton, 1986).
Measuring predation risk directly is difficult because observations of
successful attacks are rare. The response times in the study are, however,
probably a good index of relative predation risk because sparrowhawks are
surprise short-chase hunters that give up quickly if they do not get close to
their prey (Cresswell, 1996).
This study may then provide reasonable evidence for variation in predation
risk within a flock (see also Fitzgibbon,
1989; Krause,
1994). Significant variation in predation risk within a flock has
important consequences for the benefits of flocking. All flock members are
clearly not equal, and flock members will each have different costs and
benefits, dependent on their vigilance rate, position in the flock, and
nearest neighbor distance.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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This work was funded by grants to W.C. by the Leverhulme Trust and to G.D.R. by the British Ecological Society. We thank Andrew Ferguson, Stewart Bearhop, Bob Furness, and Sue Holt for technical help and the loan of equipment, Philip Whitfield for supporting the project, and Bobby Anderson, ranger at Tyninghame, for his continuing support of fieldwork there. The manuscript was considerably improved by the incisive comments of three anonymous referees.
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C. L. Devereux, M. J. Whittingham, E. Fernandez-Juricic, J. A. Vickery, and J. R. Krebs Predator detection and avoidance by starlings under differing scenarios of predation risk Behav. Ecol., March 1, 2006; 17(2): 303 - 309. [Abstract] [Full Text] [PDF]
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C. A. D. Semeniuk and L. M. Dill Cost/benefit analysis of group and solitary resting in the cowtail stingray, Pastinachus sephen Behav. Ecol., March 1, 2005; 16(2): 417 - 426. [Abstract] [Full Text] [PDF]
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E. Fernandez-Juricic, B. Kerr, P. A. Bednekoff, and D. W. Stephens When are two heads better than one? Visual perception and information transfer affect vigilance coordination in foraging groups Behav. Ecol., November 1, 2004; 15(6): 898 - 906. [Abstract] [Full Text] [PDF]
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