Biological Journal ofthe Linnean Society (1994),51: 433-446. With 5 figures
Selection by wild birds on artificial dimorphic
prey on varied backgrounds
J. M. COOPER* AND J. A. ALLEN
Department of Biology, University of Southampton, Southampton SO16 7PX
Received 7 December 1992, accepiedfor publication I8 M y 1993
Our aim was to test the effects of prey frequency and background composition on selection by
free-ranging birds. We did three series of experiments with populations of grey and orange pastry
prey scattered among coloured stones that made the prey either conspicuous or inconspicuous. Series
1 tested whether the predicted equilibrium frequency of the two prey types was influenced by the
frequency of matching grey and orange stones. Birds at a single site were given a random sequence of
combinations of prey frequency and stone frequency. Selection was dependent on background and
the effect of prey frequency also varied with background. In series 2, we explored the frequencyindependent effect of background: birds at five sites were given equal numbers of the two prey in
three frequencies of matching stones and two of non-matching. There was a higher risk of predation
for prey that matched rarer stones. In series 3 we attempted to measure, at a single site, the actual
equilibrium prey frequencies in three different backgrounds: two extreme stone frequencies and one
intermediate. Each experiment started with a population of equal numbers of grey and orange prey.
After half the prey had been eaten we calculated the frequencies of the survivors and presented a
new population of the original size but with the new prey frequencies; each experiment ran for 25
such ‘generations’. The results suggested that at equilibrium the commoner ‘morph’ was the one
that resembled the commoner colour of stone. Overall, our findings support the idea that visual
selection can result in morph frequencies becoming related to the proportions of their matching
background components and that this equilibrium will ‘track’ temporal or spatial changes in the
background.
ADDITIONAL KEY WORDS:-Frequency-dependent
predation - apostatic selection anti-apostatic selection - visual selection - crypsis - background tracking - pastry prey - colour
polymorphism.
C0NTENTS
Introduction . . . . . . . . . . . .
General methods . . . . . . . . . . .
Series 1: five prey frequencies, eight stone frequencies . .
Method . . . . . . . . . . . .
Results . . . . . . . . . . . .
Series 2: equal prey frequency, five stone frequencies . .
Method . . . . . . . . . . . .
Results . . . . . . . . . . . .
Series 3: ‘evolving’ prey frequencies in three stone frequencies
Method . . . . . . . . . . . .
Results . . . . . . . . . . . .
Discussion
. . . . . . . . . . . .
Acknowledgements . . . . . . . . . .
References . . . . . . . . . . . .
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*Present address: Department of Biology, Winchester College, Winchester SO23 9NA.
0024-4066/94/040433+ 14 $08.00/0
433
0 1994 The Linnean Society of London
434
J. M. COOPER AND J. A. ALLEN
INTRODUCTION
Some of the best known examples of natural selection occur when predators
choose conspicuous varieties of palatable prey in preference to inconspicuous
ones. Logically, we expect such directional selection to lead to a decrease in the
relative abundance of the conspicuous varieties (reviews: Edmunds, 1974;
Endler, 1986a). There is also evidence that predators often prefer varieties of
prey that are common and overlook varieties that are rare. Such ‘apostatic
selection’ may be responsible for the maintenance of colour polymorphisms
within prey species (Clarke, 1962; Greenwood, 1985; Allen, 1988a).
In complex backgrounds composed of innumerable patches varying in colour,
size, shape and other visual properties, selection against conspicuous morphs
may interact with apostatic selection. The possible forms of this interaction have
been discussed by Clarke ( 1962), Endler ( 1978, 1984, 198613, 1988), Greenwood
(1984) and Cook (1986). In particular, Endler (1978), has suggested that the
different colour morphs in a population may represent different ways of
matching the heterogeneity of background coloration.
Endler (1978) pointed out that a morph will be conspicuous when it is
abundant relative to the background patch (or combination of patches) that it
resembles; when this happens the morph will not be perceived as resembling a
‘random sample of the background’ and will have a disproportionately higher
risk of predation than when it is rare. Selective predation against conspicuous
morphs should therefore lead to a neutral equilibrium at a point related to the
relative abundance of the matching components in the background. Apostatic
selection is one of several mechanisms capable of stabilizing the equilibrium
(Endler, 1978, 1984, 198613, 1988; Cook, 1986), particularly when matching
patches are rare. If the relative frequencies of the different background patches
change, whether in space or time, then the equilibrium morph frequencies
should ‘track’ these changes (Endler, 1978).
Most tests of apostatic selection have used prey that are conspicuous (review:
Allen, 1988a). Results from birds (Bond, 1983; Cooper, 1984; Reid &
Shettleworth, 1992) and humans (Tucker & Allen, 1988, 1993) searching for
artificial ‘prey’ suggest that apostatic selection also occurs when prey match the
background. Similar results have been recorded for marine predators, probably
fish, feeding on artificial populations of two morphs of the snail Littorariajlosa on
mangrove trees (Reid, 1987). In fact, the data from experiments in which prey
were presented on several backgrounds suggest that apostatic selection on a
given set of prey types is stronger when they are inconspicuous rather than
conspicuous (Bond, 1983; Cooper, 1984; Reid, 1987; Tucker & Allen, 1988).
Predators presumably attend more strongly to common forms of inconspicuous
prey because they have more opportunity to learn to distinguish them from the
background.
Cooper ( 1984) used free-ranging wild birds foraging on ‘populations’ of
artificial dimorphic prey dispersed among backgrounds of stones. His design was
closer to the system modelled by Cook (1986), in which morphs are assumed to
match single colour patches in the background rather than the more complex
combinations of patches proposed by Endler (1978, 1984, 1986b, 1988). Cooper
(1984) found that selection was strongly apostatic when the prey matched the
colours of the stones and less so when they did not. Here we describe three series
SELECTION ON VARIED BACKGROUNDS
435
of experiments which explore further the effects of selective predation by birds on
the frequencies of artificial morphs in matching and non-matching backgrounds.
GENERAL METHODS
We used the hessian, stones and pastry prey of Cooper (1984). ‘Populations’ of
50 or 100 grey and orange pastry ‘prey’ (cylindrical ‘baits’, 7 mm long x 6.5 mm
diameter) were presented among 600 or 1200 matching grey and orange stones
scattered over sheets of hessian sackcloth. Densities were approximately 107 m-‘
for the stones and 9 m-* for the prey. The grey stones were basalt and the orange
stones flint (size range of both types: 5-35 mm). Background colour composition
was altered by varying the proportions of the two colours of stone. T o our eyes,
the two prey types were a poor match to their corresponding stones in factors
such as size, shape and texture, but in colour the match was good. As a control,
we also measured selection on the prey when they were on backgrounds that
made them conspicuous: either green stones or mixtures of equal numbers of lilac
and yellow. Munsell colour estimates for the two types of prey and the five types
of stone are given by Cooper (1984).
At the start of each set of experiments the appropriate numbers of stones were
mixed together in a bucket and then strewn haphazardly over the hessian. Trials
were started by scattering 50 or 100 prey (depending on the area of hessian) in
the appropriate proportions among the stones. We tried to record predation after
approximately half the prey had been eaten (thus defining the end of a trial)
because this minimizes the problems of bias in the estimation of selection
coefficients (see below) at extreme prey frequencies (Manly, 1974; Greenwood &
Elton, 1979). We were careful to search the backgrounds systematically for
uneaten baits because it was essential to ensure that we were not responsible for
any apparent selection. The spatial distributions of the stones and prey were
changed at the end of every trial.
The predators were common species of British garden birds. Those seen were:
blackbirds ( Turdus merula L.), songthrushes ( T. philomelos Brehm.), starlings
(Sturnus vulgaris L . ) , blue tits (Parus caeruleus L.), house sparrows (Passer domesticus
(L.)) and robins (Erithacus rubecula Hart.).
We used the selection coefficient /3 (Manly, 1973, 1974) to measure selection
against grey prey in each trial. After arcsine transformation /3 ranges from 0 to
90, with a value of 45 indicating no selection, a value above 45 selection against
grey, and a value below 45 selection against orange. Thus when selection is
regressed on prey frequency, a positive slope crossing the ‘no selection line’
indicates apostatic selection and, when the slope is positive but does not cross the
‘no selection line’, ‘potentially’ apostatic selection (Greenwood, 1985). A
negative slope indicates ‘anti-apostatic selection’ (Greenwood, 1985) which, in
real populations, should lead to monomorphism.
SERIES 1: FIVE PREY FREQUENCIES, EIGHT STONE FREQUENCIES
Cooper (1984) demonstrated apostatic selection when a range of prey
frequencies was presented on backgrounds with equal numbers of matching
stones. In this new series of experiments we varied stone frequency as well as prey
frequency. Our aim was to test the prediction that the estimated equilibrium
436
J. M. COOPER AND J. A. ALLEN
frequencies of the ‘morphs’ should be related to the relative abundance of their
respective matching elements in the background (Endler, 1978; Cook, 1986).
Method
We did the experiments between June 4 and December 5, 1980, in a garden at
Compton, near Winchester, Hampshire. The hessian sheet was 1.4 m x 4 m and
bore a population of 50 prey among 600 stones. During the first four weeks we
familiarized the local birds by feeding them twice daily on 25 grey and 25 orange
baits scattered among 600 green stones on the hessian. The main predators were
blackbirds (four individuals) and starlings (at least four); robins, blue tits and
songthrushes also visited occasionally.
We ran a random order of 45 experiments (combinations of background and
prey frequency). In 35 of them, five frequencies of grey prey (0.1, 0.3, 0.5, 0.7,
0.9) were each presented in seven frequencies of grey stones (0.1, 0.2, 0.3, 0.5,
0.7, 0.8, 0.9). The remaining ten experiments consisted of two replicates of each
of the five prey frequencies presented in a background of non-matching green
stones. Each of the 45 experiments consisted of a succession of five identical trials
run consecutively during a single day. These experimental days were sporadic
throughout the summer, autumn and winter of 1980.
If selection in a given background is apostatic, the expected equilibrium
frequency can be estimated from the regression of selection on prey frequency (or
more strictly, frequency on selection) as the frequency for which the value of
selection is 45. From the ideas of Endler (1978) and the results of Cooper (1984),
we predicted that selection on the matching backgrounds would be more
strongly apostatic than on the non-matching green background, and that the
equilibrium frequency of grey prey would be highest in the 0.9 grey background
and progressively lower in the 0.8, 0.7, 0.5, 0.3, 0.2 and 0.1 backgrounds.
Figure 1 provides further explanation.
Note that the five trials a t each combination of background and prey
frequency cannot be considered as independent trials, since they were done in
succession at the same site. We therefore used the mean results of the five trials in
the regression analyses.
Results
I n Fig. 2 we have regressed selection (arcsine transformation of fl) on the
frequency of grey prey in the seven matching backgrounds and one nonmatching (green) background. The slopes of the regression lines for the results
from the matching backgrounds are significantly heterogeneous (F6,2,= 3.04,
P < 0.05). Four are positive and three are negative, although the departure from
a gradient of zero is statistically significant for the 0.3 grey background alone
(Table 1). Thus, in contrast to Cooper (1984), we failed to obtain consistent
evidence for apostatic selection in the matching backgrounds, although it may be
indicative that positive (though non-significant) slopes were obtained for both
extremes of matching stone frequency (0.1 and 0.9).
We tested for frequency independence by estimating the expected selection at
a prey frequency of 0.5. In practice, we transformed the prey frequencies before
SELECTION ON VARIED BACKGROUNDS
437
10 -
carrying out regression by subtracting 0.5 from each of them. The frequency of
0.5 then becomes zero on the transformed scale, so that the value of a obtained in
the analysis is the value of selection predicted by the regression for this equal
prey frequency. T h e values for the seven matching backgrounds were
significantly different from one another (F6,27= 5.834, P < 0.001) and we
therefore tested the deviation of each one from a ‘no selection’ expectation of 45
(Table 1). Selection was above 45 for all three backgrounds composed mainly of
TABLE
I . Series 1: regression statistics and significance tests (single mean value ofselection for each
value of prey frequency). Regression equations are in the form Y = a + bX; first t is for deviation of
the slope b from zero (matching backgrounds, d.f. = 3; pooled data for green background,
d.f. = 8). Selectioq,, is the estimated selection at prey frequency of 0.5; second t is for deviation
from 45 (matching backgrounds, d.f. = 3; green background, d.f. = 8). ns, non significant
Background
Regression
equation
+
0.1 grey
0.2 grey
0.3 grey
0.5 grey
0.7 grey
0.8 grey
0.9 grey
34.73 38.41X
64.89- 19.64X
61.72- 11.35X
35.88+ 10.31X
46.36- 14.30X
35.27+0.54X
23.33+ 18.82X
Green
41.77+9.46X
t
2.95
- 1.53
- 22.46
1.89
-0.94
0.04
1.26
1.83
P
Selection,,5
t
P
ns
ns
< 0.001
ns
ns
ns
ns
53.94
55.07
56.04
46.19
39.2 1
35.54
32.74
0.66
2.77
77.26
0.77
- 1.34
-2.58
-2.90
ns
ns
< 0.001
ns
ns
ns
ns
ns
46.50
1.02
ns
J. M. COOPER AND J. A. ALLEN
438
90
1
80
0.2 grey stones
l o
:
I
0
0
0
lot
=
90
-
I
1
0.3 grey stones
I
0.5 grey stones
i
80
t
t
10
90
E 60-
* 30
a
a
I
0.7 grey stones
0.8 grey stones
t
80
c
a
1
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70
a
t
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0
8
.
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-
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LA-1--- - - - -3-- - - ;
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20 -
:
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I
t
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t
0.9 grey stones
80
70t
Green stones
10
0
0.3
0.5
0.7
Grey prey frequency
0.9
0.1
0.3
0.5
0.7
Grey prey frequency
0.9
SELECTION ON VARIED BACKGROUNDS
90 ,
439
1
2ol
10
O
1
04
I
I
I
I
!
I
I
;
I
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
~
Grey stone frequency
Figure 3. Series 1: selection against grey prey relative to frequency of grey stones in the seven
0.9
matching backgrounds. 0 0. I grey prey, A 0.3 grey prey, x 0.5 grey prey, A 0.7 grey prey,
grey prey. Solid line is the pooled regression Y = 60.8-30.52X; broken line is relationship expected
in absence of selection.
orange stones (0.1, 0.2 and 0.3 grey) and below 45 for all three ‘grey’
backgrounds (0.7, 0.8 and 0.9 grey). Overall, this tendency for the birds to
remove conspicuous prey was statistically significant (method of combining
probabilities, Sokal & Rohlf (1981): ‘orange’ backgrounds, - 2 1 In P = 25.00,
P < 0.001; ‘grey’ backgrounds, -2c In P = 13.14, P < 0.05). Selection was
closest to random in the 0.5 grey and the green backgrounds, suggesting that the
two prey types were equally conspicuous when on these two backgrounds.
The results from the 0.1 and 0.9 backgrounds are in the directions predicted
from Endler’s hypothesis of background tracking: from the intersections of the
regression lines with the ‘no selection’ lines, the predicted equilibrium frequency
is lower for the 0.1 grey background than for the 0.9 grey background. To test
further for background tracking, we regressed selection on the frequency of stones
within each of the five prey frequencies (Fig. 3). The five slopes do not differ
significantly from one another (F4,25= 1.231) and neither do the values of
= 0.14). We have therefore fitted a pooled
selection at stone frequency 0.5 (F4,29
regression (Y = 60.8 - 30.25X)’ the slope of which is highly significantly
different from zero (t33= -6.06, P < 0.001, implying that selection depends on
stone frequency in a regular way. From the pooled regression line, selection at a
frequency of 0.5 grey stones is estimated as 45.53, which is not significantly
different from 45 (t33 = 0.37). This confirms the earlier analysis that predation
appeared to be random when the two colours were presented on equal numbers
of matching stones.
Figure 2. Series I: selection against grey prey (p, arcsine-transformed) relative to frequency of grey
prey in seven matching backgrounds and one green background (solid points, first green replicate;
open points, second replicate). Solid lines are regression lines and broken lines indicate relationship
expected in absence of selection.
440
J. M. COOPER AND J. A. ALLEN
SERIES 2: EQUAL PREY FREQUENCY, FIVE STONE FREQUENCIES
This set of experiments (12 November to 19 December 1981) was designed to
test whether the frequency-independent effect of stone frequency observed in
series 1 was repeatable with birds a t new sites.
Method
We again used backgrounds of 1.4 m x 4 m hessian sheets each holding 600
stones. T h e prey were presented at equal frequency (25 grey and 25 orange
prey). Stone frequency was varied in five different backgrounds (three grey and
orange stone frequencies: 0.1, 0.5, 0.9; one lilac and yellow, 0.5; one all green).
The experiments were run concurrently at five sites in Southampton (minimum
distance between any two: 550 m). At all sites the five backgrounds were
presented three times and each trial lasted several hours per day. T h e fifteen
trials were done in a different random order at each site.
T o ensure that the birds learned to associate the backgrounds with food, we
fed them on white (undyed) pastry baits daily for three weeks and on 25 grey
and 25 orange prey on each of the two days immediately before the experiments.
It was impractical to monitor closely five simultaneous experiments, and
exploitation varied from the normal 50% target. Predators observed were
blackbirds (all five sites), songthrushes (two sites), starlings (two sites), blue tits
(two sites), house sparrows (two sites) and robins (all sites).
Results
Selection was affected by background composition (F4,50= 53.08, P < 0.05)
and was in the direction predicted from the hypothesis that prey which match
their background are more protected. Selection against grey prey was thus
greatest in the 0.1 grey background, least in the 0.9 grey background and close
to random (45) in the 0.5 grey background and the two controls (Table 2).
There was no effect of site on selection (F4,50 = 2.24, ns) and no significant
interaction between the effects of site and background (F,,,,, = 1.15, ns).
The selection observed in this series did not differ significantly from selection
on the equivalent 0.5 grey prey populations presented in series 1 (Table 2).
TABLE2. Series 1 and series 2: mean values of selection
(j& standard errors, arcsine-transformed) against grey prey in
0.5 grey prey populations on five different sorts of background.
t-tests (dX = 18) compare the data from the two series, (ns, not
significant)
Background
0.1 grey
0.5 grey
0.9 grey
Green
Lilac/yellow
Selection5 s.e.
Series 1
Series 2
61.01k3.33
48.23k2.07
29.91 f1.08
45.00k2.92
43.84f2.15
-
59.27f2.10
44.07f1.05
29.42f 1.51
44.01 f 1.67
44.01 f 1.67
44.95f 1.36
t
P
0.55
1.91
0.18
0.30
0.05
ns
ns
ns
ns
ns
-
SELECTION O N VARIED BACKGROUNDS
44I
SERIES 3: ‘EVOLVING’ PREY FREQUENCIES IN T H R E E STONE FREQUENCIES
This series (5 May to 19 July 1982) tested whether selection by birds can
actively drive morph frequencies towards equilibria that are related to the
frequencies of matching stones. We therefore used populations of prey in which
the morph frequencies were allowed to ‘evolve’ in response to visual selection
(method of Allen, 1972, see also Clarke, 1979 and Allen et a/., 1993).
Method
We used a lawn outside the Biology Department of the University of
Southampton, where the birds had experienced pastry and stones twelve months
earlier in the experiments described by Cooper (1984).The prey density (9 m-*)
was the same as in the previous two series but the background was twice as large
and the prey twice as numerous (hessian: 1.4 m x 8 m, number of stones: 1200,
prey population: 100). We trained the birds to visit by feeding them undyed
pastry baits on bare hessian for two weeks immediately before the start.
In each experiment we simulated 25 successive ‘generations’, starting from a
population of 100 prey with a frequency of 0.5 grey (generation 0). We recorded
the number of surviving prey when about half had been eaten and then cleared
the background of uneaten baits and redistributed the stones. We then presented
a new generation of 100 prey in the same frequencies as had survived predation.
We used three backgrounds with different frequencies of grey stones and did the
experiments in the (random) order: 0.9, 0.1, 0.5. The experiments were run on
71 consecutive days; the 0.9 grey stone experiment lasted 20 days, the 0.1 grey 25
days a.nd the 0.5 grey 26 days. Thus each generation was exposed to predation
for about one day. Predators were blackbirds (two pairs), blue tits (probably
four) and robins (one pair).
Results
Prey frequency (Fig. 4) was clearly influenced by the composition of the
background (independence of the three proportions in the final generations:
G = 69.10, d.f. = 2, P < 0.001). The frequency of grey prey decreased when the
background was mainly orange (0.1 grey) and increased when the background
was mainly grey (0.9). The rise in the frequency of orange in the 0.1 grey
background was not significantly different from the rise in the frequency of grey
in the 0.9 grey background (T = 60.5, n = 21, P > 0.05, Wilcoxon
matched-pairs signed-ranks test), suggesting that there was little difference in
the strength of selection against the two colours. This is supported by the data
from the background with equal numbers of grey and orange stones; the prey
frequencies stay close to the starting value of 0.5 (departure from 0.5 not
significant: T = 114.6, n = 21, Wilcoxon test). Using the values for the last 13
generations in each experiment (Fig. 4), we find that the equilibrium grey prey
frequencies (mean fstandard error) are: 0.1 grey stones, 0.2 1 f 1.08; 0.5 grey
stones, 0.53f 1.53; 0.9 grey stones, 0.77f 1.94.
Figure 5 shows the changes in selection with generation number. At first,
selection was consistently against grey prey in the 0.1 grey background (the first
nine points all represent selection against grey; P < 0.02, binomial test) and
J. M. COOPER AND J. A. ALLEN
442
4
o.9 0.1 grey stones
I
0.8
1 .o
0.5 grey stones
0.9
0.8-.
h
2
0.7-.
>r
4
," 0.3
CJ
10.9grey stones
I
0.9
q,,
i
,
,
,
; ,
,
,
i
,
,
, ; .
,
,
i
0.0
0
4
8
12
16
20
,
,
,I
24
Generation number
Figure 4. Series 3: frequencies of grey prey over 24 generations of selection by wild birds feeding on
populations on backgrounds of 0.1, 0.5 and 0.9 grey stones. Broken lines indicate initial prey
frequencies. Note that the experiments ran in the order 0.9, 0.1, 0.5.
SELECTION O N VARIED BACKGROUNDS
70
60
i
I
10.5arev
" . stones
8o
70
443
i
i
I
0.9 grey stones
60
50
40
2oi
30
10
04"';
0
"
4
.
i
"
0
'
i
"
12
'
i
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'
i
16
Generation number
Figure 5. Series 3: selection against grey prey (p, arcsine-transformed)
20
' " 1
24
in generations 0-24. Broken
lines (selection = 45) are relationships expected in absence of selection.
444
J. M. COOPER AND J. A. ALLEN
against orange in the 0.9 grey background (in the first 16 generations there is
only one case of selection against grey; P < 0.002, binomial test). For the second
half of the generations in these two backgrounds, selection fluctuated around the
null value of 45. Selection in the 0.5 background was close to 45, which is to be
expected if the starting frequency of 0.5 grey prey represents the equilibrium
value.
Visual inspection of Fig. 5 suggests that selection might have been more
variable in the second half of each experiment than in the first half. T o test this,
we fitted a three-point running mean and then calculated the absolute values of
the departures of each generation from the appropriate value of the running
mean. Variability, so defined, was indeed significantly greater in the second
halves of the experiments in the 0.1 and 0.5 grey backgrounds (0.1 grey: mean
variability+ standard error in first half 1.53 f 0.47, in second half 4.2 1 0.80,
t = -2.90, d.f. = 22, P < 0.01; 0.5 grey: mean variability in first half
0.88f0.22, in second half 2.65f0.58, t = -2.85, d.f. = 22, P < 0.01). For the
0.9 grey background, variability was in fact greater in the first half of the
experiment but the difference was statistically non-significant (mean variability
in first half 2.99f0.52, in second half 2.23f0.27, t = 1.30, d.f. = 22, P > 0.05).
DISCUSSION
In summary, all three series of experiments demonstrated that selection on the
grey and orange prey was affected by the frequencies of matching background
stones, and in series 3 this selection appeared to have a direct effect on
equilibrium frequencies. There is some consistency in the strength of frequencyindependent selection, not only among the different sites in series 2 but also
between the equivalent 0.5 grey prey populations presented in series 1 and 2.
There was no evidence for frequency-independent selection when the two prey
types were equally conspicuous.
With regard to frequency-dependent selection, the data from series 1 were
inconsistent. Selection may have been apostatic in the two extreme matching
backgrounds of 0.1 and 0.9 grey stones and the predicted equilibrium
frequencies in these two backgrounds were in the same direction as observed
later in series 3. For the intermediate frequencies, however, no clear picture
emerges (apart from the frequency-independent influence of background
composition). One explanation could be that selection at a given combination of
prey and stone frequency was affected by the experiences of the birds in
previous, often very different combinations. This sort of interaction between
trials has been shown to occur in experiments with conspicuous prey (Allen,
1976; Horsley et al., 1979), but it was impractical to use separate sites for each
combination of stone and prey frequency, ideal though this might have been
(Greenwood, 1985).
By contrast, the results from series 3 were more consistent with the hypothesis
of background tracking and it is perhaps no coincidence that the birds were
exposed to smaller temporal fluctuations in prey frequency. I n the two extreme
backgrounds the birds at first appeared to select in a frequency-independent
manner against prey that resembled the least common background colour
component. The direction of selection then appeared to fluctuate around an
equilibrium. One interpretation of this result is that frequency-independent
SELECTION ON VARIED BACKGROUNDS
445
selection against the more conspicuous morph gave rise to a neutral equilibrium
which was then stabilized by apostatic selection (Endler, 1978; Cook, 1986).
Since the three experiments in series 3 were run consecutively at a single site,
the same group of birds were sufficiently labile in their behaviour to generate
different equilibrium frequencies in response to changes in background
composition. A longer experiment with more generations would of course be
needed to measure the degree of stability of the equilibria and to see whether
they converge more closely on the proportions of stones in the backgrounds.
More replicates are also needed. If the constancy of selection on inconspicuous
morphs proves to be a general result, and if naturally occurring polymorphic
prey usually match the background (Endler, 1978, though see Clarke, 1962),
then apostatic selection could be a less variable (and consequently a more
predictable) force for maintaining polymorphism than some theoretical models
have suggested (Cook, 1965; Jarvinen, 1976).
Our work gives no direct clues about the behavioural mechanisms underlying
the observed selection. We saw nothing to suggest that the birds learned to avoid
the stones through negative reinforcement, and so an explanation based on
conventional Batesian mimicry seems unlikely. Selection could have resulted
from development of search images for common cryptic prey (Guilford &
Dawkins, 1987; Tucker & Allen, 1993) or could reflect a behavioural trade-off
between the probability of detecting prey versus non-prey (Staddon & Gendron,
1983; Greenwood, 1986; Getty, 1987). Whatever the explanation, the results
imply that colour was an important cue in detection even though the prey
differed markedly from the stones in, for example, size and shape.
Note that we have been careful to avoid the use of the term ‘crypsis’. This is
because we are unsure whether the birds overlooked the prey because their
outlines were less obvious against the backdrop of matching stones (‘crypsis’), or
because they were actually seen but perceived as stones (‘masquerade’) (Endler,
1981).
Finally, we wonder whether apostatic selection can protect polymorphism
when one of the background patches is very rare or even absent (Endler, 1978).
An experiment to test this could throw light on how apparently conspicuous
morphs of prey species such as landsnails of the genus Cepaea Held. can survive in
places where selection against conspicuous forms might be expected to promote
monomorphism (Cain & Sheppard, 1954). Apostatic selection might even be
strong enough to override the directional effects of crypsis (Clarke, 1962; Allen,
1988b).
ACKNOWLEDGEMENTS
We thank Jeremy Greenwood and Laurence Cook for comments on some very
early drafts. Later versions were reviewed by Jeremy Greenwood, Rebecca Knill,
Stuart Church and an anonymous referee. We thank Keef Anderson for
technical assistance at all stages in the work. Financial support to JMC was
provided by a Postgraduate Studentship from the States of Guernsey Education
Council.
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