Download Predator versus prey: on aerial hunting and

Behavioral Ecology Vol. 12 No. 2: 150–156
Predator versus prey: on aerial hunting and
escape strategies in birds
Anders Hedenström and Mikael Rosén
Department of Animal Ecology, Lund University, Ecology Building, SE-223 62 Lund, Sweden
Predator and prey attack-escape performance is likely to be the outcome of an evolutionary arms race. Predatory birds are
typically larger than their prey, suggesting different flight performances. We analyze three idealized attack-escape situations
between predatory and prey birds: climbing flight escape, horizontal speeding, and turning and escape by diving. Generally a
smaller bird will outclimb a larger predator and hence outclimbing should be a common escape strategy. However, some
predators such as the Eleonora’s falcon (Falco eleonorae) has a very high rate of climb for its size. Prey species with an equal or
higher capacity to climb fast, such as the swift Apus apus, usually adopt climbing escape when attacked by Eleonora’s falcons.
To analyze the outcome of the turning gambit between predator and prey we use a Howland diagram, where the relative linear
top speeds and minimum turning radii of prey and predator define the escape and danger zones. Applied to the Eleonora’s
falcon and some potential prey species, this analysis indicates that the falcon usually wins against the example prey species; that
is, the prey will be captured. Level maneuvering hunting is the most common strategy seen in Eleonora’s falcons. To avoid
capture via use of this strategy by a predator, the prey should be able to initiate tight turns at high linear speed, which is
facilitated by a low wing loading (weight per unit of wing area). High diving speed is favored by large size. If close enough to
safe cover, a prey might still opt for a vertical dive to escape in spite of lower terminal diving speed than that of the predator.
On the basis of aerodynamic considerations we discuss escape flight strategies in birds in relation to morphological adaptations.
Key words: climbing flight, diving, Falco eleonorae, flight performance, Howland diagram, predation, turning gambit. [Behav
Ecol 12:150–156 (2001)]
D
epending on size and morphology predatory birds use
one or other preferred hunting technique, such as surprise attacks by the sparrowhawk (Accipiter nisus) or the legendary stoop by the perergine (Falco peregrinus) (Cresswell,
1996; Rudebeck, 1950–1951). Much recent work has focused
on fat load management under perceived or experienced predation risk (Gosler et al., 1995; Lilliendahl, 1997; van der
Veen, 1999). Another line of research has studied escape responses in relation to body mass of caged birds when attacked
by a simulated predator (e. g., Kullberg et al., 1996; Lee et
al., 1996; Lind et al., 1999; Veasey et al., 1998; Witter et al.,
1994). However, it remains unclear if the responses observed
in such experiments, usually a reduced take-off angle and
speed with increasing body mass, represent the effect of a
chosen strategy or a constraint on flight performance. This
article is not, however, concerned with such take-off escape
responses when a bird is attacked by a predator, but rather
with the relative flight performance between a predator and
its prey when both are already airborne. Lima (1993) reviewed
the literature on escape flight strategies in North American
birds when attacked by a predator.
Size, morphology, and hunting strategy have probably coevolved among predatory species to maximize success in hunting their most common prey. Prey species, on the other hand,
should evolve adaptations that maximize the chances of escaping a predator attack, leading to a co-evolutionary arms
race between predator and prey (Dawkins, 1982). In birds, the
predator is typically larger than the prey, and because size has
profound effects on aerodynamic performance, we could expect that the size difference is exploited by the prey when
selecting the best escape strategy. In this article we will con-
Address correspondence to A. Hedenström. E-mail: anders.
[email protected].
Received 15 March 2000; revised 14 June 2000; accepted 16 June
2000.
2001 International Society for Behavioral Ecology
sider the interaction between avian predator and prey involved in attack-escape interactions in open air space. When
attacked by a predator the prey bird only has one goal—to
survive by reaching a safe site before being seized by the predator. In aerial combat the available strategy set for the prey
consists mainly of three alternatives: (1) escape by outclimbing the predator (Cade, 1960), (2) escape by outmaneuvering
the predator in a turning gambit (Howland, 1974), and (3)
escape by diving away from the predator. From the prey’s
point of view the choice of the optimal escape behavior will
be context dependent. Factors likely to influence the choice
of escape strategy are predator (species, sex, size), the relative
position between prey and predator, speed vectors of prey and
predator when the prey discovers the predator and the state
of the prey (e.g., fuel load, muscle size, condition, etc.). A
general model combining all these factors is unlikely to generate any clear insights. We will focus on the aerodynamic
properties of birds during aerial attacks by considering the
three main escape options by simple scaling analysis of flight
performance. To improve realism and illustrate the general
principles we will calculate some relevant performance measures based on measured flight performance in the Eleonora’s
falcon (Falco eleonorae) (Hedenström et al., 1999), which
preys on migratory birds in the Mediterranean region during
their autumn migration (Rosén et al., 1999; Walter, 1979). For
comparison we selected some candidate prey species for
which the relevant measures of flight performance were available (Hedenström and Alerstam, 1992, 1994). Even though
our discussion will focus on the Eleonora’s falcon and its prey,
our results are generally applicable to any aerial predator-prey
interaction system where the relative locomotory performances of the predator and prey can be assessed using either biomechanical principles or experiments.
METHODS
Information on flight performance in the Eleonora’s falcon
and seven potential prey species refers to published infor-
Hedenström and Rosén • Predator versus prey
151
Table 1
Morphological data of Eleonora’s falcon and seven potential prey species used to derive aerodynamic
properties
Species
m
(kg)
b
(m)
S
(m2)
Aspect
ratio
(b2/S)
Wing
loading
(N/m2)
Eleonora’s falcon Falco eleonorae
Knot Calidris canutus
Arctis tern Sterna paradiasaea
Song thrush Turdus philomelos
Dunlin Calidris alpina
Swift Apus apus
Chaffinch Fringilla coelebs
Siskin Carduelis spinus
0.35
0.205
0.11
0.066
0.050
0.043
0.022
0.011
0.95
0.51
0.80
0.34
0.40
0.40
0.26
0.21
0.104
0.0286
0.0571
0.0193
0.0146
0.0171
0.0128
0.0075
8.7
9.1
11.2
6.0
11.0
9.4
5.3
5.9
33.0
70.3
18.9
33.5
33.6
24.7
16.9
14.4
Sources: Hedenström and Alerstam (1992, 1994), Hedenström et al. (1999); m, body mass; b, wing
span; S, wing area.
mation of sustained climbing flight (Hedenström and Alerstam, 1992, 1994; Hedenström et al., 1999). Climbing flight
performance was measured by using tracking radar or an optical range finder. Track data were reduced in relation to wind
measurements obtained by tracking ascending helium filled
weather balloons. Sustained climbing flight was taken during
at least 240 s to represent the climb rate that a bird can maintain by aerobic muscle work, which in principle is for as long
as the fuel supply lasts. However, during very long climbs to
high altitudes the climb rate will decline because the air density declines with increasing altitude (Pennycuick, 1978). We
will assume that the birds exhibit their maximum power during these climbs or a constant proportion thereof (cf. Hedenström and Alerstam, 1992). Then we can estimate the maximum power (Pmax) as the sum of the aerodynamic power and
the rate of work required to raise the body against gravity at
speed Vz as:
Pmax ⫽ P(V) ⫹ mgVz,
(1)
where m is body mass, g is acceleration of a body in free fall
and P(V) is the mechanical power required to fly horizontally
at airspeed V. Mechanical power was calculated according to
the theory of Pennycuick (1989) with air density 1.23 kg/m3
representing sea level and standard atmospheric conditions,
but differing by using a value of 0.1 for the body drag coefficient (Pennycuick et al., 1996). The estimated Pmax from the
measured climbing flights was taken as the maximum available power from the flight muscles. Maximum horizontal airspeed (Vmax) was calculated by finding the speed where the
power required for horizontal flight equals Pmax. This estimate
of Vmax relies on current flight mechanical theory (Pennycuick, 1989), and possible future revision of this theory or
parameters used may change the estimates. However, changes
to the theory will affect the estimates approximately equally
and presumably the relative difference between the species
will remain largely unaffected. Hence, the general conclusions
will not be subject to features of the aerodynamic theory used.
In a steady horizontal turn a component of the lift force
(L) has to be directed upwards to balance the weight, which
determines the maximum bank angle by cos␾ ⫽ mg/L. The
remaining lift can be directed towards the center of rotation
giving a minimum turning radius at a given angle of bank as:
rmin ⫽
mV 2
,
Lsin ⌽
sible bank angle and a maximum lift coefficient CL ⫽ 0.5 at
the maximum speed. At low speeds birds can usually develop
a maximum lift coefficient around 1.6, but at high speeds lift
coefficients are in the range 0.3–0.5 (cf. Pennycuick, 1968).
Morphological data (body mass, wing span and wing area)
were taken from the original sources of flight performance
(Table 1). Measurements refer to the standard methods used
for aerodynamic calculations according to Pennycuick (1989),
hence the wing area includes the area of the body between
the wings. The prey species used as examples are not necessarily typical prey of the Eleonora’s falcon (cf. Walter, 1979),
but they were chosen because measures of flight performance
were available for these species. However, they do represent
similar sizes of typical prey that should have similar performance measures, and they or close relatives have all been
found among prey in breeding cliffs of Eleonora’s falcon (Spina et al., 1987; Walter, 1979).
(2)
where V is speed, L is lift and ⌽ is the bank angle (e.g., Thomas, 1996). For calculations we will assume the maximum pos-
Escape by climbing flight
If two birds, predator and prey, are on the same level when
the prey discovers the predator, then a good strategy should
be vertical escape upwards, that is, by climbing flight, if the
prey possesses a capacity to climb at a faster rate than the
predator. Pennycuick (1978) derived a formula for the climbing capacity in birds as:
Vz ⫽
2.16mm f
1.92m 2/3
⫺ 1/2 3/2 ,
m
␳ b
(3)
where mm is the mass of the flight muscles, m is body mass, f
is wingbeat frequency, ␳ is air density and b is wing span. We
can use this formula to calculate how climb rate scales with
body mass by substituting the body mass dependent parameters with their respective scaling relationship. Greenewalt
(1962) found that flight muscle mass is relatively independent
of body size at 17%, that is, mm ⫽ 0.17m. In isometrically
scaled birds maximum wingbeat frequency scales as f⬁m–1/3
(Pennycuick, 1975) and wing span scales as b⬁m1/3. By substituting these relations into Equation 2 we get:
Vz ⫽ a0m⫺1/3 ⫺ a1m1/6
(4)
where a0 and a1 include physical constants independent of
body mass. From this equation it is clear that the rate of climb
should decline with increasing body mass in a series of isometrically scaled birds. If climbing flight is the selected escape
strategy, then we might expect selection for smaller size in the
prey species. From Equation 3 it is also clear that birds climbing performance is enhanced by increased flight muscle frac-
Behavioral Ecology Vol. 12 No. 2
152
Table 2
Observed airspeed (Vh) and rate of climb (Vz) in the Eleonora’s falcon and seven potential prey species, and derived aerodynamic properties
used for comparing relative flight performance between predator and prey
Species
N
Vh
(m/s ⫾ SD)
Eleonora’s falcon
Knot
Arctic tern
Song thrush
Dunlin
Swift
Chaffinch
Siskin
13
33
15
10
10
7
24
7
13.1
13.8
9.9
12.4
13.9
10.0
11.2
13.4
⫾
⫾
⫾
⫾
⫾
⫾
⫾
⫾
2.35
1.9
1.4
1.5
0.41
0.8
1.2
1.2
Vz
(m/s ⫾ SD)
1.4
1.10
1.24
1.00
1.63
1.34
1.02
0.84
⫾
⫾
⫾
⫾
⫾
⫾
⫾
⫾
0.31
0.34
0.22
0.21
0.41
0.30
0.33
0.23
P(Vh)
(W)
mgVz
(W)
Ptot
(W)
Vmax
(m/s)
⌽max
(⬚)
rmin
(m)
2.45
2.48
0.46
0.70
0.43
0.27
0.18
0.11
4.81
2.21
1.34
0.65
0.80
0.57
0.22
0.091
7.26
4.69
1.80
1.35
1.23
0.84
0.40
0.20
28.4
25.8
23.6
22.1
24.6
22.1
19.4
18.3
82
70
84
77
80
81
82
82
11.0
24.8
6.3
11.4
11.3
8.3
5.6
4.8
Sources: Hedenström and Alerstam (1992, 1994), Hedenström et al. (1999). N, number of observations; P(Vh), mechanical power required
for level flight; mgVz, the power expended to climb at speed Vz; Ptot, the total mechanical power (P(Vh)⫹mgVz), Vmax is the estimated
maximum horizontal airspeed; ⌽max, the maximum angle of bank; and rmin, the calculated horizontal minimum turn radius. P(Vh) was
calculated according to Pennycuick (1989) using a body drag coefficient CD,par ⫽ 0.1 and air density 1.23 kg/m3, and Vmax was calculated
under the same assumptions; rmin was calculated for a lift coefficient CL ⫽ 0.5.
tion, maximum wingbeat frequency and wing span. An increase in wingspan inevitably leads to a reduced maximum
wingbeat frequency (Pennycuick, 1975, 1996), and so there is
a trade-off between the two traits. However, wing span (b) is
raised to 3/2 and wingbeat frequency is raised to one in Equation 3, and therefore we might still expect rather long and
high aspect ratio wings in birds adapted for high climbing
performance. Selection pressure on size and morphology
should be in the same direction for a predator where climbing
flight pursuit is an important hunting strategy.
Real birds are not isometrically scaled, but wing span tends
to increase faster with increasing body mass (Rayner, 1988),
which partly compensates the adverse effects of size on climb
rate. This is particularly obvious in the Eleonora’s falcon,
which has an extreme climb rate for its size (Table 2; Hedenström et al., 1999). Comparing the prey species with Eleonora’s falcon, it is only the dunlin (Calidris alpina) that surpasses the predator, and allowing for the variation around the
means, possibly also the arctic tern (Sterna paradisaea) and
the swift (Apus apus) would escape successfully from the fal-
con by climbing (Table 2). If the prey species has a lower
climb rate than its predator, then escape climbing is a bad
option, even if starting with an altitude advantage, because
the predator will eventually close the gap in a sustained climb
gambit. When attacked by Eleonora’s falcons small passerines
such as chaffinch (Fringilla coelebs) and siskin (Carduelis spinus) should not try climbing flight escapes (Table 2).
If a prey is attacked by a predator coming from above, that
is, the prey has a lower initial position than the predator (Figure 1), it may still be advantageous to escape by climbing. If
we assume that power available from the flight muscles is independent of forward speed (Pennycuick, 1968), then the
maximum rate of climb will be associated with the minimum
power speed (Vmp). If power available is speed dependent
then maximum rate of climb will be at a forward speed greater than Vmp (Thomas and Hedenström, 1998). The escape
should be directed away from the attacking predator to maximize the flight distance for the predator (Figure 1). If the
prey reaches the same level as the predator before the predator has closed the distance, then climbing flight escape is a
viable strategy when the horizontal distance to the predator
(D) satisfies the inequality:
D⬎
z
Vz,prey
(Vpred ⫺ Vmp,prey ),
(5)
where the variables are defined in Figure 1. This rather simplistic model assumes that the predator is already flying at its
maximum speed when discovered and that the prey is flying
at Vmp and can accelerate to its maximum rate of climb instantly. This is not true in the real world, but the model illustrates the point that climbing escape might be an option even
with an initial height disadvantage to the prey and that the
decision to climb or not should be distance dependent.
Escape by horizontal turning gambit
Figure 1
A simple model for a criterion of climbing flight escape with an
initial height disadvantage. The horizontal distance to the predator
at start of the climb is D. The predator has to cover the distance
D⫹z/Vz,prey·Vmp, prey at horizontal speed Vpred, where z is the initial
height difference between the predator and prey, Vz,prey is maximum
climb rate of prey, and Vmp,prey its minimum power speed.
A useful escape tactic to a prey is to initiate a turn before
predator closure and rely on a tight turn radius for escape.
The classical example is the cheetah and gazelle, where the
cheetah has the highest top speed but the gazelle can execute
tight turns that are often life-saving maneuvers. Howland
(1974) analyzed the condition of a two dimensional turning
gambit between predator and prey with respect to maximum
linear speed and turn radii. The turning gambit starts with a
linear escape away from the predator, but because the predator has the highest maximum speed it will close in on the
Hedenström and Rosén • Predator versus prey
153
Figure 2 are calculated on the mean performances of the falcon and prey, but there is individual variation in these and so
the border between escape and no escape should be considered as a band around the curve. Species or individuals falling
close to the curve of Figure 2 can escape with some probability, depending on the relative individual flight performances of predator and prey. Three of the species (knot, dunlin
and song thrush) even have greater turning radii than the
predator (Table 2), and they should avoid getting involved in
a turning gambit with Eleonora’s falcons altogether.
Escape by diving
Diving or stooping is a typical attack strategy by large falcons,
famous by the performance of the peregrine (Falco peregrinus) (Alerstam, 1987; Peter and Kestenholz, 1998; Tucker,
1998). In a gliding dive inclined at an angle ␣ to the horizontal the bird must keep the wings partly open to provide the
lift needed to maintain a constant glide angle. Using simple
fixed wing theory of gliding flight the vertical speed (Vz) is:
Vz ⫽
Figure 2
A Howland diagram showing the escape and no escape zones of a
turning gambit between relative maximum linear speed (v) of prey
and predator and minimum relative turning radius (r). The
function describing the borderline between escape and no escape is
v ⫽ 兹r (Howland, 1974). Also shown are the relative v and r for
the species listed in Tables 1 and 2, using estimated maximum
speeds and turning radii. The only species falling outside the no
escape zone is the arctic tern. The three data points plotted on the
right ordinate represent points of r ⬎ 1 and are actually further
away from the escape demarcation than indicated in the diagram.
The species are knot (Kn), arctic tern (At), song thrush (St),
dunlin (Du), swift (Sw), chaffinch (Ch) and siskin (Si).
prey. There is, however, a chance to escape if the prey has a
smaller turning radius than the predator and there is an optimal moment (or distance) to execute the turn (Howland,
1974). The border between the danger and safe zones in a
Howland diagram is defined by:
v ⫽ 兹r ,
(6)
where v is the ratio of maximum speeds of prey and predator
(Vmax,prey/Vmax,pred) and r is the ratio between the minimum
turning radii (rmin,prey/rmin,pred). Hence, knowing maximum
speeds and turning radii it is possible to predict the outcome
of a turning gambit.
We used available data on flight performance in the Eleonora’s falcon and seven potential prey species representing
different size and morphology to estimate maximum sustained horizontal flight speed and the minimum horizontal
turning radius when initiated at the maximum speed (Table
2). During circular horizontal turns at the calculated minimum radii these birds would experience forces between 2.7g
(knot) and 9g (arctic tern), which is of the same magnitude
as the vertical force measured in quail (Coturnix coturnix)
during take-off (Earls, 2000). The falcon has the highest maximum speed and hence would overtake all the prey species in
a straight level escape flight. We have plotted relative speeds
and turning radii for the species in Table 2 in a Howland
diagram (Figure 2), which indicates that only one species, the
arctic tern, would escape from a turning gambit with Eleonora’s falcon. The other species would be taken by the predator. However, the three smallest species (swift, chaffinch, and
siskin; Table 2) fall near the border between the escape and
no escape zones (Figure 2). The points in the (v,r)-plane of
k 1 mg
k SV 3
⫹ 2
,
2
b V
mg
(7)
where V is forward speed along the glide path, b is wing span,
S is wing area, and k1 and k2 include physical constants. At the
terminal speed the vertical speed is Vsin␣ and Equation 7
becomes:
Vmg sin␣ ⫽
k 1 (mg)2
⫹ k 1 SV 3 ,
b 2V
(8)
which after substitution of b and S and rearrangement gives
the condition for terminal gliding speed as:
V 4 ⫺ c1m1/3V ⫹ c2m2/3 ⫽ 0,
(9)
where c1 and c2 are new constants independent of body mass.
Solving Equation 9 for terminal speed in a gliding dive yields:
V ⬀ m1/6,
(10)
which shows that speed increases with increasing body size (cf.
Andersson and Norberg, 1981). A similar analysis for terminal
speed in a vertical dive with completely folded wings gives the
same scaling relationship as Equation 10. Hence, this explains
why large falcons may adopt this attack strategy since they
have a speed advantage with respect to a usually smaller prey
bird. However, depending on the starting positions a prey may
escape, and reach a safe site before being seized, by diving
even with a lower terminal speed than the attacking predator.
In a very simple setting, the prey dives to cover with a vertical
dive and the predator attack by an inclined gliding dive from
a horizontal distance D to the prey. Starting at the same level,
the prey escapes if the vertical distance to the ground (h) is:
h⬍
DVz,prey
2
兹V 2 ⫺ V z,pred
,
(11)
where V is the terminal speed of the predator and Vz is the
birds’ respective vertical speeds. Again, this criterion assumes
that both birds can accelerate instantaneously to their maximum speeds. Equation 11 shows that the prospects of escaping an attack by diving away from the predator increases with
horizontal distance to prey and the terminal speed of the prey.
This is perhaps not a very startling result, but the model could
easily be modified to account for a more realistic situation,
including time of accelerating to maximum speed and different relative altitudes when the hunt starts.
Small passerines are often seen trying to escape by vertical
dives at high altitudes over sea, even when Eleonora’s falcons
are very close to them (Walter, 1979; Hedenström and Rosén,
Behavioral Ecology Vol. 12 No. 2
154
unpublished observations). But often such escape dives are
combined with a sharp pull-up, i.e. initiating of a loop. This
is again an application of the turning gambit. Assuming that
the prey bird reaches its terminal speed velocity in a dive with
completely folded wings, then
V⫽
冢
冣
2mg
␳Sb CD,par
1/2
,
(12)
where ␳ is air density, Sb is body frontal area and CD,par is the
body drag coefficient. If the bird opens its wings they will
create a lift force that can be used to create a centripetal
acceleration in a turn away from the dive path. Initially all
that lift is used to turn, but later along the loop path the same
amount of lift also has to support the weight. The initial turning radius is:
r⫽
2m
,
␳SCL
(13)
where m is body mass, S is wing area and CL is the lift coefficient. The morphology and aerodynamic properties of the
bird determine the relative speed and the turn radius to be
plotted in a Howland diagram. For the species in Table 1 we
need information about body mass, frontal area, wing area,
body drag and lift coefficients to estimate the outcome of a
vertical dive turning gambit. Such data are lacking for these
species, but by assuming CD,par ⫽ 0.1, CL ⫽ 0.5 and otherwise
the default values in Pennycuick (1989), we get a similar outcome as that of the horizontal flight turning gambit (cf. Figure 2).
DISCUSSION
Predator and prey interactions often have a great influence
on the life of organisms, such as habitat selection, selection
of feeding sites, sociality and group living and vigilance (Lima
and Dill, 1990). They can also generate morphological adaptations and counter adaptations in the predator and prey species to enhance performance of capturing and escaping, respectively. We have focused our analysis on the flight performance in birds escaping by one of three main strategies:
climbing away from the predator, outmaneuvering the predator in a horizontal turning gambit, or diving to safety. The
general principles should however be applicable also to other
situations and animals.
In climbing flight escape, performance is enhanced by
small size, long wings, large flight muscles and high wingbeat
frequency. When encountering attacks from Eleonora’s falcons, a predator with an exceptional capacity to climb fast for
its relatively large size (Hedenström et al., 1999), only the
dunlin and possibly also the swift should escape by climbing
(Table 2). In fact, this is the main escape tactic observed in
swifts (Hedenström et al., 1999; Hedenström A, and Rosén M,
unpublished observations). The dunlin is usually not a prey
of Eleonora’s falcons, but when attacked by other predators
climbing escapes have been observed (Lima, 1993). The wing
morphology of both the swift and the dunlin is characterized
by rather high aspect ratio wings, in line with the prediction
for birds adopting climbing escapes (cf. Table 1). The skylark
(Alauda arvensis) is another species escaping by climbing
(song) flight on attacks by the merlin (Falco columbarius)
(Cresswell, 1994). Skylarks are known to have capacity for fast
climbs (Hedenström, 1995b). Morphologically the skylark has
shorter wings than the swift and dunlin, but it has larger flight
muscles than birds in general (about 25% of total body mass;
Rayner, 1988). Lima (1993) also reports escape by climbing
flight in the short-billed dowitcher (Limnodromus griseus),
American crow (Corvus brachyrhynchos) and water pipit (An-
thus rubescens), and Hedenström (1995a) reports an observation of a flock of white-winged black terns (Chlidonias leucopterus) escaping by climbing away from a pursuing peregrine. Some large species, such as the sage grouse (Centrocercus urophasianus), which is a typical quarry to large falcons,
rely on acceleration and high maximum horizontal speed
achieved by large flight muscles and small wings (Pennycuick
et al., 1994). The maximum speed of the grouse is higher than
that of the falcon, but the grouse would not be able to fly at
this speed with aerobic muscle work, and it is questionable if
it can fly at any speed without incurring an oxygen debt (Pennycuick et al., 1994). Hence, it needs to find cover soon after
having out-speeded a pursuing falcon.
In the turning gambit a prey will outmaneuver a predator
by a combination of high relative linear top speed and a small
turning radius (Figure 2; Equation 6). Of our example species
only one, the arctic tern, would outperform the Eleonora’s
falcon, while two (or possibly three) species were borderline
cases (Figure 2). A small turning radius is achieved by a low
wing loading (large relative wing area) and fast flight is facilitated by a streamlined body shape, low wing drag (i.e., small
wings), and high power available from the flight muscles
(large muscle fraction). Generally, wing loading increases with
increasing body size and so a small turning radius is obtained
by small birds with relatively large, but short, wings. These
features represent a typical passerine, but apparently also
terns are adapted for this sort of gambit by low wing loading
and relatively high top speed (Tables 1 and 2). The Eleonora’s
falcon mainly hunts by chasing prey by active maneuvering
flight (Rosén et al., 1999), perhaps because their main prey
(small passerines) most often try to escape by maneuvering
flight. The Howland diagram (Figure 2) indicates that this
predator should do well by this strategy when compared with
some potential prey species. Field observations show however
that success rate is quite low per attack (11%; Walter, 1979),
but once a bird is attacked when passing a colony of Eleonora’s falcons, many falcons will attack in rapid succession
resulting in rather low survival chances for the prey (Rosén
et al., 1999; Walter, 1979). The survey by Lima (1993) shows
that escape by a last moment dodge is a very common strategy.
Hence, the Howland diagram is a useful tool for assessing the
likely outcome of an attack-escape gambit between predator
and prey in birds. The only condition is that the prey has the
opportunity to first move away from the predator and the ability to execute turns with minimum radii (Howland, 1974).
This generally requires open spaces, such as the aerial hunting of Eleonora’s falcons, which usually takes place at great
altitudes where migrants cruise when passing the Mediterranean sea on autumn migration (Rosén et al., 1999). Howland
diagrams are also applicable to other situations, such as birds
hawking insects in the air (cf. Warrick, 1998), bats hunting
moths (Roeder and Treat, 1961), fish hunting in open water
(Arnott et al., 1999) and cheetah and other terrestrial carnivores hunting on open plains.
Extra lift and still more reduced turning radius may be
achieved by spreading the tail and hence augmenting the lifting surfaces when turning (Thomas, 1996). Also the prey can
do this, thereby reducing its turning radius by the same
amount as the falcon, provided the relative tail surfaces are
the same, in which case the relative radii will remain unchanged with respect to those calculated in Table 2. Some
species, however, such as dunlin and knot (Calidris canutus),
have relatively small tails and would not be able to increase
lift to the same degree as the falcon, which has a normal tail
size, and consequently do even worse in a turning gambit than
indicated in Figure 2.
In escape by diving the predator has an advantage from its
size and will reach higher maximum terminal speeds than the
Hedenström and Rosén • Predator versus prey
smaller prey. Birds will maximize the diving speed by having
streamlined bodies and small wings. Many water birds escape
by plunge diving (Lima, 1993), and especially ducks seem to
fulfil the requirements for this. Alerstam (1987), using tracking radar, reports that his highest measured speed of birds
refers to red-breasted mergansers (Mergus serrator) reaching
43 m/s in a shallow gliding dive. Passerines also dive when
attacked by Eleonora’s falcons, in combination with pull-ups,
hence executing a vertical turning gambit. Small birds should
be able to execute relatively tighter turns when initiated at a
very high speed, as during a vertical dive with completely folded wings, where the larger predator might not be able to
achieve its theoretical minimum turning radius for structural
safety reasons (cf. Howland, 1974). Swifts were never observed
diving when escaping from Eleonora’s falcons, perhaps because their long wings generate too much drag even when
folded.
In this article we have focused on how aerodynamic theory
may be used to analyze attack-escape performance in birds by
indicating the direction of selection on morphology for improved flight performance. Our analyses show that depending
on escape strategy, there may be partly diverging selection
pressures on morphology. This, in turn, suggests that a species
should be generally best adapted for escaping by a certain
method, that is, ‘‘escape specialists’’ rather than ‘‘escape generalists.’’ The swift is an example of a species that invariably
escape by climbing flight when attacked by Eleonora’s falcons.
Lima’s (1993) survey indicated that many species seem to prefer one main strategy, but several species may select one of
the alternative strategies. However, our analyses also show that
the relative performances of the prey and predator should
influence the escape strategy selected. Also, the relative positions between the predator and prey birds, such as vertical
and horizontal distances, decide the escape strategy selected.
By always maximizing the distance and trajectory to the predator, a prey will inflict the maximum energy cost to the predator (Weihs and Webb, 1984), which eventually can force the
predator to abort the attack. In line with the life-dinner principle (Dawkins, 1982) the predator should consider energy
costs associated with prey capture, while the prey should pay
little attention to energy costs per se (Hedenström and Alerstam, 1995). Studying sparrowhawk attacks on birds, Cresswell
(1995) found that the hawks preferred prey in the size range
101–150 g. This could be due to the relative maneuverability
of this size class in relation to small prey (ⱕ50 g) that may
escape more easily. It may also be that large prey was preferred because they are more profitable than small prey. In
another study, Cresswell (1993) found that redshanks (Tringa
totanus) responded differently on attacks by three different
bird predators, supporting our flight mechanics results.
Hence, when possible, the prey should obtain information
such as species, distance, speed, and flight direction about the
attacking predator for appropriate choice of escape response
that maximizes the survival chances. When facing surprise attacks this might not be possible, and the prey bird might rather chose a standard escape response. This situation could be
what cage escape flight experiments represent (e.g., Lind et
al., 1999; Veasey et al., 1998; Witter et al., 1994). However,
Kullberg et al. (1998) found that the escape trajectory of great
tits (Parus major) depended on the attack angle of a model
predator.
It is of course naı̈ve to believe that selection for efficient
escape performance is the only factor that matters to shape a
bird’s morphology. Selection for efficient foraging, migration
and display should also be important selective agents. Predation may, however, be such an important selective force that
it results in significant features in the prey species’ size and
morphology. Some typical prey species to the Eleonora’s fal-
155
con, for example swifts, swallows and flycatchers, are themselves aerial predators, which could involve selection on size
and morphology in the same direction as selection for efficient escape from an aerial predator. But depending on the
escape response of invertebrate prey, small birds may face conflicting selective demands for their own foraging efficiency
and escape flight performance.
Finally, even if the aerodynamic theory used is revised in
the future, we think that the general conclusions will remain
valid. Measuring the maximum flight performance of birds is
a challenge (cf. Chai and Dudley, 1999; Marden, 1987), but
such data can be used to assess the relative flight performance
of predator and prey by using Howland diagrams. They can
also help us understand why birds are designed as they are.
It is extremely difficult to measure the flight trajectories of
two birds during attack-escape maneuvers in the wild. However, such measurements and high-speed films of these interactions would be most welcome.
We thank Fernanda Diana for inviting us to work with the Lega Italiana Protezione Uccelli (LIPU) project as a base and for her support
during our stays. We are also grateful to Alberto Badami, Nicola Fara,
Franco Fadda, Maurizio Medda, Fernando Spina, and Susanne Åkesson for assistance during fieldwork that inspired our thinking on aerial predation. Erik Svensson and S. Åkesson gave much appreciated
comments on the manuscript. This research was supported by the
Swedish Natural Science Research Council (given to A.H.).
REFERENCES
Alerstam T, 1987. Radar observations of the stoop of the peregrine
falcon Falco peregrinus and the goshawk Accipiter gentilis. Ibis 129:
267–273.
Andersson M, Norberg RÅ, 1981. Evolution of reversed sexual size
dimorphism and role partitioning among predatory birds, with a
size scaling of flight performance. Biol J Linn Soc 15:105–130.
Arnott SA, Neil DM, Ansell AD, 1999. Escape trajectories of the brown
shrimp Crangon crangon, and a theoretical consideration of initial
escape angles from predators. J Exp Biol 202:193–209.
Cade TJ, 1960. Ecology of the peregrine and gyrfalcon populations
in Alaska. Berkeley, California: University of California Press.
Chai P, Dudley R, 1999. Maximum flight performance of hummingbirds: capacities, constraints, and trade-offs. Am Nat 153:398–411.
Cresswell W, 1993. Escape response by redshanks, Tringa totanus, on
attack by avian predators. Anim Behav 46:609–611.
Cresswell W, 1994. Song as a pursuit-deterrent signal, and its occurrence relative to other anti-predation behaviours of skylark (Alauda
arvensis) on attack by merlins (Falco columbarius). Behav Ecol Sociobiol 34:217–223.
Cresswell W, 1995. Selection of avian prey by wintering sparrowhawks
Accipiter nisus in southern Scotland. Ardea 83:281–389.
Cresswell W, 1996. Surprise as a winter hunting strategy in sparrowhawks Accipiter nisus, peregrines Falco peregrinus and merlins F. columbarius. Ibis 138:684–692.
Dawkins R, 1982. The extended phenotype. Oxford: Oxford University Press.
Earls KD, 2000. Kinematics and mechanics of ground take-off in the
starling Sturnus vulgaris and the quail Coturnix coturnix. J Exp Biol
203:725–739.
Gosler AG, Greenwood JJD, Perrins C, 1995. Predation risk and the
cost of being fat. Nature 377:621–623.
Greenewalt CH, 1962. Dimensional relationships for flying animals.
Smithsonian Misc Coll 144(2):1–46.
Hedenström A, 1995a. Ecology of avian flight (PhD dissertation).
Lund: Lund University.
Hedenström A, 1995b. Song flight performance in the skylark Alauda
arvensis. J Avian Biol 26:337–342.
Hedenström A, Alerstam T, 1992. Climbing performance of migrating
birds as a basis for estimating limits for fuel-carrying capacity and
muscle work. J Exp Biol 164:19–38.
Hedenström A, Alerstam T, 1994. Optimal climbing flight in migrating birds: predictions and observations of knots and turnstones.
Anim Behav 48:47–54.
156
Hedenström A, Alerstam T, 1995. Optimal flight speed of birds. Phil
Trans R Soc Lond B 348:471–487.
Hedenström A, Rosén M, Åkesson S, Spina F, 1999. Flight performance during hunting excursions in Eleonora’s falcon Falco eleonorae. J Exp Biol 202:2029–2039.
Howland HC, 1974. Optimal strategies for predator avoidance: the
relative importance of speed and manoeuvrability. J Theor Biol 47:
333–350.
Kullberg C, Fransson T, Jakobsson S, 1996. Impaired predator evasion
in fat blackcaps. Proc R Soc Lond B 263:1671–1675.
Kullberg C, Jakobsson S, Fransson T, 1998. Predator induced take-off
strategy in great tits (Parus major). Proc R Soc Lond B 265:1659–
1664.
Lee SJ, Witter MS, Cuthill IC, Goldsmith AR, 1996. Reduction in escape performance as a cost of reproduction in gravid starlings Sturnus vulgaris. Proc R Soc Lond B 263:619–624.
Lilliendahl K, 1997. The effect of predator presence on body mass in
captive greenfinches. Anim Behav 53:75–81.
Lima SL, 1993. Ecological and evolutionary perspectives on escape
from predatory attacks: a survey of North American birds. Wilson
Bull 105:1–47.
Lima SL, Dill LM, 1990. Behavioral decisions made under the risk of
predation: a review and prospectus. Can J Zool 68:619–640.
Lind J, Fransson T, Jakobsson S, Kullberg C, 1999. Reduced take-off
ability in robins (Erithacus rubecula) due to migratory fuel load.
Behav Ecol Sociobiol 46:65–70.
Marden JH, 1987. Maximum lift production during takeoff in flying
animals. J Exp Biol 130:235–258.
Pennycuick CJ, 1968. Power requirements for horizontal flight in the
pigeon Columba livia. J Exp Biol 49:527–555.
Pennycuick CJ, 1975. Mechanics of flight. In: Avian biology (Farner
DS, King JR, eds). New York: Academic Press; 1–75.
Pennycuick CJ, 1978. Fifteen testable predictions about bird flight.
Oikos 30:165–176.
Pennycuick CJ, 1989. Bird flight performance: a practical calculation
manual. Oxford: Oxford University Press.
Pennycuick CJ, 1996. Wingbeat frequency of birds in steady cruising
flight: new data and improved predictions. J Exp Biol 199:1613–
1618.
Pennycuick CJ, Fuller MR, Oar JJ, Kirkpatrick SJ, 1994. Falcon versus
prey: flight adaptations of a predator and its prey. J Avian Biol 25:
39–49.
Behavioral Ecology Vol. 12 No. 2
Pennycuick CJ, Klaassen M, Kvist A, Lindström Å, 1996. Wingbeat
frequency and the body drag anomaly: wind-tunnel observations on
a thrush nightingale (Luscinia luscinia) and a teal (Anas crecca). J
Exp Biol 199:2757–2765.
Peter D, Kestenholz M, 1998. Sturzflüge von Wanderfalke Falco peregrinus und Wüstenfalke F. pelegrinoides. Orn Beob 95:107–112.
Rayner JMV, 1988. Form and function in avian flight. Curr Ornithol
5:1–66.
Roeder KD, Treat AE, 1961. The detection and evasion of bats by
moths. Amer Sci 49:135–148.
Rosén M, Hedenström A, Badami A, Spina F, Åkesson S, 1999. Hunting flight behaviour of the Eleonora’s falcon Falco eleonorae. J Avian
Biol 30:342–350.
Rudebeck G, 1950–1951. The choice of prey and modes of hunting
of predatory birds with special reference to their selective effect.
Oikos 2:65–88, 3:200–231.
Spina F, Scappi A, Berthemy B, Pinna G, 1987. The diet of Eleonora’s
falcon Falco eleonorae in a colony of the western coast of Sardinia
with some remarks on the migration of small passerines through
the Mediterranean. Suppl Ric Biol Selvaggina 12:235–254.
Thomas ALR, 1996. The flight of birds that have wings and tail: variable geometry expands the envelope of flight performance. J
Theor Biol 183:237–245.
Thomas ALR, Hedenström A, 1998. The optimum flight speeds of
flying animals. J Avian Biol 29:469–477.
Tucker VA, 1998. Gliding flight: speed and acceleration of ideal falcons during diving and pull out. J Exp Biol 201:403–414.
van der Veen IT, 1999. Effects of predation risk on diurnal mass dynamics and foraging routines of yellowhammers (Emberiza citrinella). Behav Ecol 10:545–551.
Veasey JS, Metcalfe N, Houston DC, 1998. A reassessment of the effect
of body mass upon flight speed and predation risk in birds. Anim
Behav 56:883–889.
Walter H, 1979. Adaptations to prey and habitat in a social raptor.
Chicago: University of Chicago Press.
Warrick DR, 1998. The turning- and linear-maneuvering performance
of birds: the cost of efficiency for coursing insectivores. Can J Zool
76:1063–1079.
Weihs D, Webb PW, 1984. Optimal avoidance tactics in predator prey
interactions. J Theor Biol 106:189–206.
Witter MS, Cuthill IC, Bonser RHC, 1994. Experimental investigations
of mass-dependent predation risk in the European starling, Sturnus
vulgaris. Anim Behav 48:201–222.