Download Countershading enhances crypsis with some bird

Behavioral Ecology
doi:10.1093/beheco/arh166
Advance Access publication 17 November 2004
Countershading enhances crypsis with some
bird species but not others
Michael P. Speed,a,b David J. Kelly,b,c Andrew M. Davidson,b and Graeme D. Ruxtond
School of Biological Sciences, Liverpool University, Crown Street, Liverpool L69 7ZB, U.K.,
b
Biology, Liverpool Hope University College, Childwall, Liverpool L16 9JD, U.K., cDepartment of
Zoology, Trinity College Dublin, Dublin 2, Ireland, and dInstitute of Biomedical and Life Sciences,
Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, U.K.
a
Although the theory of self-shadow concealing countershading is over a century old, there are very few direct empirical tests to
substantiate the prediction that prey that are dorsally darkened and ventrally lightened (generally termed countershaded) suffer
lower rates of attack than other prey. In this paper, we report experiments designed to determine whether artificial,
countershaded prey are chosen by predators less often than those that are all light, all dark, or reverse shaded (i.e., dorsally
lightened and ventrally darkened). Artificial prey were presented in gardens and parks to free-living birds, either on white
backgrounds or on backgrounds with some degrees of color matching. In one experiment, birds were unmarked, and in the
other, they were individually identifiable. We found that in three experimental trials, countershaded baits were attacked at a rate
not significantly different from that of uniformly dark baits. In one experimental trial, countershaded baits were at some
advantage. When we examined the data set for this trial more closely, it was apparent that blackbirds were taking countershaded
baits least often, but blue tits and robins conferred no special advantage to countershaded baits. Hence, the efficacy of countershading may vary with species of predator. Key words: countershading, crypsis, predator, prey. [Behav Ecol 16:327–334 (2005)]
ould (1991: 231) notably described the light bellies of
countershaded animals as ‘‘perhaps the most universal
feature of animal coloration,’’ yet a definitive explanation for
dorsal darkening in countershaded prey animals remains
elusive (see review in Ruxton et al., 2004). Because countershading is seen most frequently in inconspicuous animals, it
has been widely assumed that it may add to the effectiveness
of an animal’s crypsis, somehow reducing detection by
predators. In the most famous and frequently applied theory
of countershaded crypsis (Thayer, 1896), the combination of
a dark dorsa and a light ventra is hypothesized to generate
a property now called ‘‘self-shadow concealment’’ (SSC, see
Edmunds and Dewhirst, 1994; Kiltie, 1988). Because illumination on prey is generally from above, shadows will be cast on
ventral surfaces, and the resultant variation in shading may be
used by predator’s visual systems to recognize and distinguish
solid objects from their backgrounds: there is evidence that
this is true for human vision (Ramachandran, 1988). Being
darkest on top may reduce variation in shading caused by
shadow and thus confound the ability of predators to
recognize that a prey item is indeed a three-dimensional
solid object when viewed from the side. This idea is generally
attributed to Thayer (1896), who wrote that ‘‘mimicry makes
an animal appear to be some other thing, whereas this newly
discovered law [of gradation in the coloring of animals]
makes him cease to appear at all.’’ Reporting Thayer’s work in
Nature, Poulton (1902) commented that ‘‘no discovery in the
wide field of animal coloration has been received with greater
interest’’ (although we note that Poulton himself invented the
idea some years earlier, see Poulton, 1888).
This theory of SSC has been widely accepted as a possible
explanation for countershading ever since (e.g., Braude et al.,
2001; Bretagnolle, 1993; Edmunds and Dewhirst, 1994;
G
Address correspondence to M.P. Speed. E-mail: [email protected].
Received 18 May 2004; revised 11 August 2004; accepted 3
September 2004.
Herring, 1994; Kiltie, 1988; Nagaishi et al., 1989; Phillips,
1962; Ruiter, 1956; Stauffer et al., 1999; Turner, 1961; Young
and Roper, 1976). However, there is little experimental
evidence that SSC really works in prey animals (see Ruxton
et al., 2004) and, furthermore, there is very little experimental
evidence that countershading enhances crypsis by this or any
other means. Notably, however, a recent and large-scale
comparative analysis concluded that countershading may
aid concealment in even-toed ungulates (Stoner et al., 2003b)
but that it is unlikely to do so in lagomorphs (Stoner et al.,
2003a).
Alternative explanations for countershading of course exist
(see reviews in Kiltie, 1988; Ruxton et al., 2004). One
alternative general explanation for some instances of countershading is that it is an epiphenomenon resulting from
different demands applied to the dorsum and ventrum of an
animal rather than a primarily adaptive antipredator trait. For
example, in some terrestrial quadrupedal species with short
limbs, the ventrum may be barely visible when the animal is
viewed from above or from the side (see Braude et al., 2001).
We might then expect such animals only to manifest
camouflage pigmentation on the dorsum rather than on
both the dorsum and the ventrum especially, if pigmentation
incurs costs (see Kiltie, 1988; Ruxton et al., 2004).
Of the relatively few experiments conducted to test the
general prediction that countershading enhances crypsis
(e.g., Edmunds and Dewhirst, 1994; Ruiter, 1956; Turner,
1961), Edmunds and Dewhirst’s (1994) is in our view the most
rigorous. Edmunds and Dewhirst presented artificial prey
on lawns to freely foraging birds (house sparrows, Passer
domesticus; chaffinches, Fringilla coelebs; starlings, Sturnus
vulgaris; blackbirds, Turdus merula; song thrushes, Turdus
philomelos; robins, Erithacus rubecula; dunnocks, Prunella
modularis; blue tits, Parus caeruleus; and great tits, Parus major).
Prey were small green pastry cylinders that were uniformly
light, uniformly dark, countershaded, or reverse shaded.
Counter- and reverse-shaded baits were two-toned, being
made from a thin strip of dark pastry laid on light pastry and
Behavioral Ecology vol. 16 no. 2 International Society for Behavioral Ecology 2004; all rights reserved.
Behavioral Ecology
328
Table 1
Summary of sites and experimental conditions for the two experiments (days with rain were avoided in both experiments)
Experiment,
trial
Experiment 1,
garden 1
Experiment 1,
garden 2
Experiment 2,
trial 1
Experiment 2,
trial 2
Dates
Condition
in first
period of
experiment
Condition in
second
period of
experiment
Visiting
birds
Color of
pastry
Site 1: Whitehaven,
Cumbria,
rural garden
Site 2: Whitehaven,
Cumbria, rural
garden (2 miles
from garden 1)
Archbishop
Ryan Park,
Dublin
B, ST, TH,
SP, CD, GT,
CH, BT
B, ST, TH,
SP, GT
Green
26 June 2002 to
25 July 2002
Card present
(14 days)
Card absent
(14 days)
Green
26 June 2002 to
25 July 2002
Card absent
(14 days)
Card present
(14 days)
B, BT, R
Brown
11 March 2002 to
30 May 2002
Archbishop
Ryan Park,
Dublin
B, BT, R
Brown
5 November 2003 to
1 December 2003
Brown pastry
on brown
background
(11 March 2002
to 1 May 2002)
Brown pastry on white
background (5 November
2003 to 19 November 2003)
Brown pastry
on white
background
(15 May 2002
to 30 May 2002)
Brown pastry
on brown
background
(23 November 2003
to 1 December 2003)
Site
Key to abbreviations: B ¼ blackbird (Turdus merula), ST ¼ starling (Sturnus vulgaris), TH ¼ thrush (Turdus philomelos), SP ¼ sparrow (Passer
domesticus), BT ¼ blue tit (Parus caeruleus), CD ¼ collared dove (Streptopelia decaocto), GT ¼ great tit (Parus major), R ¼ robin (Erithacus rubecula).
presented with either the dark or the light area upperside.
Edmunds and Dewhirst reported a significant advantage to
countershaded baits over the uniformly dark forms.
However, on its own, Edmunds and Dewhirst’s experiment
does not constitute a definitive test of the prediction that
countershading enhances crypsis for at least two reasons. First,
Edmunds and Dewhirst’s data set is small (they report 9
sampling days), and even though they showed statistical
significance, there is a good case for repeating this work.
Second, Edmunds and Dewhirst were unable to consider
whether different bird species responded to countershading
in prey in different ways.
We therefore report two experiments designed to test
whether countershading enhances protection by diminishing
the probability of detection by predators. We modified
Edmunds and Dewhirst’s basic experimental design to
incorporate a ‘‘cryptic condition’’ (in which prey more or
less match their background color) and a ‘‘conspicuous
condition’’ (in which all prey are presented on a white
background). In our initial experiment we used gardens as
arenas and unmarked birds as predators; in our second
experiment we used individually identifiable blackbirds (T.
merula) and robins (E. rubecula) in a single park, whose
behavior was monitored throughout. If countershading does
reduce the likelihood of detection in the artificial prey, then
we would expect that in the cryptic condition countershaded
baits are taken less often than the other forms. Furthermore,
if the primary cause of prey choice is ease of visual detection, then in the conspicuous condition we expect prey to
be taken at similar rates. We show that although countershading cannot always be demonstrated to enhance crypsis,
there is some evidence in our data set to support Edmunds
Table 2
Results of GLM analysis of bird-feeding data in experiment 1
Source
Type III sum
of squares
df
Mean square
F
Significance
a. Whitehaven, garden 1
Day
Background
Prey
Background 3 prey
Error
Total
Corrected total
30.958
36.262
1.529
1.576
68.205
937.000
108.051
1
1
3
3
103
112
111
30.958
36.262
0.510
0.525
0.662
46.752
54.761
0.770
0.794
,.001
,.001
.514
.500
b. Whitehaven, garden 2
Day
Background
Prey
Background 3 prey
Error
Total
Corrected total
23.630
3.103
4.398
3.224
34.467
1032.000
89.844
1
1
3
3
103
112
111
23.630
3.103
1.466
1.075
0.335
70.616
9.272
4.381
3.211
,.001
.003
.006
.026
Countershading enhancement of crypsis
and Dewhirst’s results. Crucially though, countershading
may be effective with some species of predators but not
others.
EXPERIMENT 1: UNMARKED INDIVIDUALS
Methods
The design of experiments with unmarked birds closely
followed the method of Edmunds and Dewhirst (1994), in
which pastry prey were made from a 3:1 mixture of plain white
flour and lard. To make pastry of a light hue, 25 ml of green
‘‘Supercook’’ dye and 50 ml of water were added to 600 g of
pastry; for pastry of a dark hue, 75 ml of dye was added to
a second 600-g batch of pastry. Edmunds and Dewhirst’s
recipe generates a large difference (to human eyes) in
contrast between the light and dark pastries.
The prey were created by molding the pastry into approximately 3 mm-diam cylinders and then cutting them into 10 mm
lengths. Four prey types were made using this method;
light and dark prey were cut directly from rolled pastry and
rolled into cylinders. For the countershaded and reverseshaded prey the pastry was first rolled until it was approximately 1.5 mm thick and then the light and dark pastries were
laid on top of one another to produce a two-toned prey.
Countershaded prey were placed with the dark pastry on the
uppermost side and the light pastry on the underside; reverse
shaded were placed with light pastry uppermost and the dark
pastry on the underside. This produces a contrast boundary
between light and dark sections of the bait. Following
Edmunds and Dewhirst (1994), we used 25 of each prey
type randomly distributed throughout a 10 by 10 matrix so
that each bait was 0.5 m from the nearest other baits (note this
was 1 m in Edmunds and Dewhirst’s original experiment).
Prey were distributed at 0830 h and collected when
approximately 50–60% of the baits had been taken or at
around 1600 h on each day, whichever came first. We split the
experimental trials into two phases, one in which prey were
placed directly onto grass (‘‘card absent’’) and the other in
which they were placed on 1.5 3 1.5-cm squares of white card
(‘‘card present’’). Because all prey types would be clearly
visible against the white card, the card-present condition was
included to control for the possible existence of preferences
that operate after detection and are unrelated to crypsis. Any
differences in predation rates in the card-present treatment
are therefore likely to reflect postdetection preferences rather
than difference in crypsis. We ran this experiment simultaneously between 26 June 2002 and 28 July 2002 in two similar
gardens in Whitehaven, Cumbria, U.K., that were 2 miles
apart. In garden 1, card present was the first condition and
card absent the second condition, both conditions lasting for
14 days. In garden 2, this order was reversed (see summary
in Table 1). Because water degrades the coloration of the
artificial prey, we did not collect data on rainy days.
Statistical analysis
Data for each garden were analyzed separately using the
GLM ANOVA procedure in SPSS v.11.0. Prey and background
were fixed factors, and day of experiment was included as
a covariate. The square root transform of the number of each
prey type attacked per day had a good match to a normal
distribution and was the dependent variable in each case. In
all GLM analyses described in this paper, we used planned
Bonferroni post hoc tests in the estimated marginal means
procedure of SPSS. In most cases, we compared mean
numbers of different bait types attacked within but not
between an experimental condition (i.e., within the background-matching or white background conditions).
329
a
16
14
Mean number attacked
•
12
10
8
6
4
2
0
L
D
C
R
C
R
Prey type
b
16
14
Mean number attacked
Speed et al.
12
10
8
6
4
2
0
L
D
Prey type
Figure 1
Mean numbers of each prey type attacked in experiment 1 in the
presence/absence of card. Shaded bars represent presentations
without white card; unshaded bars represent presentations with card.
L ¼ light, D ¼ dark, C ¼ countershaded, R ¼ reverse shaded. Error
bars represent 2 SEM (solid lines connect means significantly
different, p , .01; dashed line, p , .05). (a) Whitehaven site 1: card
used in first presentation. (b) Whitehaven site 2: card absent in first
presentation.
Results
There was a significant effect of day as a covariate in data sets
from both gardens, in which there was a positive correlation
of total number of prey attacked and day of experiment (see
Table 2 and Figure 1). In both gardens background was recorded as a significant factor; a higher mean number of prey
were attacked in the presence of card.
In garden 1, in which baits were presented first on card,
there were no significant effects of prey or prey 3 background
interaction. In contrast, in garden 2 with card absent as the
first condition, all factors and the prey 3 background interaction were significant. With card present, the Bonferroniadjusted post hoc test showed no significant differences
between mean numbers of each prey attacked (p . .98 in all
comparisons); with card absent, comparisons of light and dark
(p ¼ .03) and light and countershaded were significant (p ,
.01; in all other comparisons p . .05). Hence, countershaded
baits were taken at a rate not significantly different from that
of dark or reverse-shaded baits.
Behavioral Ecology
330
Table 3
Output of GLM for first experiment with individually marked Dublin birds
Source
Type III sum
of squares
df
Mean square
a. First experiment in which brown board was presented first
Trial
3.662
1
3.662
Prey
19.552
3
6.517
Background
0.075
1
0.075
Species
203.326
1
203.326
Prey 3 background
17.298
3
5.766
Prey 3 species
7.835
3
2.612
Background 3 species
5.213
1
5.213
Prey 3 background 3 species
8.713
3
2.904
Error
573.359
1723
0.333
Total
4564.000
1740
Corrected total
866.177
1739
b. Second experiment in which white board was presented first
Trial
0.038
1
0.038
Prey
0.136
3
0.045
Background
1.544
1
1.544
Species
212.380
2
106.190
Prey 3 background
6.716
3
2.239
Prey 3 species
2.265
6
0.377
Background 3 species
4.087
2
2.043
Prey 3 background 3 species
8.599
6
1.433
Error
436.663
1783
0.245
Total
2766
1808
Corrected total
691.300408
1807
One argument that can be made against the quality of data
generated with unmarked free-living birds is that the
individuals participating may change during the course of
an experiment. We therefore decided to follow-up this
experiment with a second experiment in which a group of
individually ringed birds was presented with baits in a similar
experimental setup. Here we were able to check that all the
identified individuals were present throughout the duration
of the experimental trials.
EXPERIMENT 2: INDIVIDUALLY RINGED BIRDS
Methods
The trials were conducted in Archbishop Ryan Park in
Merrion Square, Dublin, Ireland (Table 1). We performed
two experiments, one between 11 March 2002 and 30 May
2002 and the other between 5 November 2003 and 1
December 2003. All presentations were made on boards.
Some years earlier (1998), green baits had been presented to
birds as part of an early-feeding experiment; hence, we used
brown baits and brown-painted boards here.
To color the baits, a brown dye was manufactured by
combining 20 parts of Green (90) with 1 part of Christmas
Red (4R) (both from J E O’Brien & Sons Ltd., Dublin,
Ireland). To produce the dark brown color, we mixed 37.5 ml
of dye with 37.5 ml of water and added this to 600 g of pastry.
To produce the light brown coloration, we mixed 7.5 ml of
dye with 68.5 ml of water and again added this to 600 g of
pastry. This recipe generates a large difference (to human
eyes) in contrast between the light and dark pastries.
Countershaded and reverse-shaded baits were then produced
as in Edmunds and Dewhirst (1994), with the dark and light
forms providing a conspicuous contrast boundary. The board
used was a plain white Corriboard square (5-mm thick 3 50
cm 3 50 cm). For color-matching conditions, we painted the
board with a dark brown paint (Dulux Weathershield—Bitter
F
Significance
11.005
19.585
0.225
611.014
17.327
7.848
15.665
8.728
.001
,.001
.635
,.001
,.001
,.001
,.001
,.001
0.154
0.185
6.305
433.599
9.141
1.541
8.344
5.852
.695
.906
.012
,.001
,.001
.161
,.001
,.001
Chocolate) to match the dark brown bait color used,
otherwise the board was presented unpainted.
Presentations were made at 25 different locations around
the park that were chosen to be well within any given bird’s
territory. No individual was allowed more than three
presentations at any given site during a day’s data collection,
and presentations at a location ceased when approximately
50% of baits had been taken or when 15 min had passed,
whichever came sooner. The experimenter (D.K.) had greater
knowledge of the numbers of baits taken in this experiment
and was better able to stop a presentation when the 50%
criterion had been met than was possible in experiment 1.
As several birds could visit and remove prey items quickly, it
was not feasible to randomly distribute the prey items in
a manner that ensured correct identification of every prey
taken. Therefore, the presentation was divided into four equal
sectors (25 3 25 cm), and each of the four treatments (light
brown, dark brown, countershaded, and reverse shaded) was
placed in a different sector. The treatments were always placed
in the same order on the board, but the board was rotated
through 90 with respect to the observer between consecutive
presentations. This system corrected for any distance from
cover considerations, as well as favored perches. At the start of
each presentation, there were 10 of each bait type spaced
evenly across the relevant sector. This was the minimum
number of baits that ensured a period of uninterrupted
feeding by the birds. The observer stood close to the board to
record both the number of baits eaten and the order in which
they were eaten. This ensured that all baits eaten were
attributable to individual birds.
In the first phase of the first experimental trial (from 11
March 2002 to 1 May 2002), the board initially was brown;
subsequently we changed the board color to white (unpainted) (fully conspicuous condition from 15 May 2002 to
30 May 2002). In the second experimental trial (from 5
November 2003 to 1 December 2003), we reversed this order
of presentation (Table 1).
•
Countershading enhancement of crypsis
Five identified blackbirds and eight identified robins took
part in the first experimental trial for its entire duration.
These birds had been previously marked (by mist netting and
color ringing) and trained to associate the experimenter with
food. In addition a number of unidentified individuals of
both species and unidentified blue tits, P. caeruleus, visited the
feeding boards.
Between experimental trials, a new set of birds was marked to
replace individuals that had moved or died in the interim.
Fifteen robins took part in all the second experimental trial,
and only four were identified as individuals present in the first
experimental trial. Four blackbirds took part in the second
experimental trial; two of which were identified as having
previously encountered the baits. As in the first experimental trial, a number of unringed blue tits also fed from the boards.
331
a
3.0
2.5
Mean numbers attacked
Speed et al.
2.0
1.5
1.0
0.5
0.0
L
Statistical analysis
C
R
C
R
Prey type
b
1.8
1.6
1.4
Mean numbers attacked
We used the GLM analysis in SPSS v. 11.0 on square root
transformed numbers of baits taken per presentation with
bird species, prey, and background as fixed factors and
presentation number as covariate. Planned Bonferroni post
hoc tests were again used to compare mean attack rates within
experimental conditions.
In the white-board presentation of the first experimental
trial, blue tits made only 7 visits compared to 119 in the
preceding part of this experimental trial. Blue tits were
therefore excluded from the overall GLM analysis and were
examined separately. In the second experimental trial, all
three species made similar numbers of visits between
experimental conditions and hence, all three were included
in the GLM.
D
1.2
1.0
0.8
0.6
0.4
Results
0.2
In the first experimental trial in which baits were initially
presented against a brown background, all main factors
(except background) and all interactions were significant
(Table 3, Figure 2). We consider two levels of analysis from
this point: first, the prey 3 background interaction, looking at
the total effect of avian predation on the baits, and second,
the species 3 prey interactions for both backgrounds. Blue
tits were excluded from the main GLM analysis for reasons
stated (however, we confirmed that their exclusion did not
affect the conclusions for the brown-board presentation by
running a similar GLM with the blue tits present and the
‘‘white-board’’ condition excluded; see Appendix).
When the background was brown, only mean numbers of
dark and countershaded prey were not significantly different
(p ¼ .697, otherwise all other mean comparisons were
significant, Figure 2a). When the background was subsequently changed to white, no means were significantly
different (p ranged from .980 to 1). Thus, even though there
is no main effect of background in the number of baits taken
(in a large part because the experimenter determined when
to stop a presentation), there is strong evidence of differential
choice when the baits matched the background but no
evidence of differential choice when they contrast with the
background. This is consistent with our expectation that the
white background would diminish any differences in detection rates between baits.
If we look at each species (Figure 3a,b), we see marked
differences in bait choices when the background is brown.
While the blue tits showed no differences in bait choices at all
(one-way ANOVA, F3,476 ¼ 0.873, p ¼ .455), the robins took
light baits over all others and the blackbirds showed more
complex order of choice: L(ight) . R(everse shaded) .
C(ounter shaded) ¼ D(ark). In contrast, when the back-
0.0
L
D
Prey type
Figure 2
Mean numbers of prey attacked by all predators at Archbishop Ryan
Park, Dublin. Shaded bars represent data for brown boards; unshaded
bars represent data for white boards (solid lines connect means
significantly different, p , .01; dashed line, p , .05). (a) First
experimental trial in which brown backgrounds are used first. (b)
Second experimental trial in which white backgrounds are used first.
ground was white, all significant effects of color difference on
choice rates disappear.
In the second experimental trial, in which baits were initially
presented against a white background, trial number, prey, and
the prey 3 species interaction were nonsignificant; all other
components of the ANOVA were significant (Figure 2b, Table 3,
b). Overall, more baits were taken in the second part of the
experiment when brown boards were presented. This is
explained in part by a larger number of total visits made by
the birds (215 in the first half of the trial and 241 in the second),
which may reflect growing demand for food as the winter
progressed during the experiment. When the background was
white, there were overall no significant differences between bait
types; however, when the background was changed to brown,
countershaded baits were taken at a significantly lower rate than
light baits, and there were no other significant differences
noted. Hence, there is some advantage to countershaded prey
in this part of the experiment.
This level of analysis, however, hides important differences
between species (Figure 3c,d). When the background was
white, the blackbirds took countershaded baits more often
Behavioral Ecology
332
b
10
10
8
8
Mean numbers attacked
Mean numbers attacked
a
6
4
L D C R
Blue tits
n=119
L D C R
Robins
n=227
0
L D C R
Blackbirds
n=88
L D C R
Blue tits
n=7
L D C R
Robins
n=41
L D C R
Blackbirds
n=79
d
10
10
8
8
Mean numbers attacked
Mean numbers attacked
c
4
2
2
0
6
6
4
4
2
2
0
6
L D C R
Blue tits
n=45
L D C R
Robins
n=156
L D C R
Blackbirds
n=12
0
L D C R
Blue tits
n=54
L D C R
Robins
n=167
L D C R
Blackbirds
n=18
Figure 3
Results for experiment 2 by bird species; experimental trials 1 (brown board first) and 2 (white board first). (a) Trial 1, brown board. (b) Trial 1,
white board. (c) Trial 2, white board. (d) Trial 2, brown board. Post hoc tests: ---- ¼ 0.1%; — ¼ 1%; ...... ¼ 5%. ‘‘n’’ refers to the number of
presentations in which birds of each species visited the boards during each trial.
than light and dark baits, but when the background was
changed to brown, they took the countershaded baits
significantly less often than the others (we note that the
number of visits by blackbirds in this second experimental
trial is lower than in the first). In contrast, the blue tits never
took baits at significantly different rates, whereas the robins
took the light baits over the others, when the background was
brown (Figure 3) but not when it was white.
DISCUSSION
Though SSC is often viewed as the correct explanation for
countershading (e.g., Gould, 1991, and see review in Ruxton
et al., 2004), Edmunds and Dewhirst’s (1994) study stands out
as the only good direct experimental demonstration that
countershading can enhance crypsis. In this paper, we have
attempted to replicate and extend important features of
Edmunds and Dewhirst’s experiment.
We draw a number of conclusions from the first experiment
performed with unringed birds on two neighboring lawns.
First, when presented on a lawn initially without cards (in
garden 2), the birds chose some types of bait at different rates,
but there was no special advantage to countershading, in that
the countershaded baits were taken at a rate not significantly
different from that of dark or reverse-shaded baits. When
subsequently placed on white cards, these preferences
disappeared altogether, indicating that the observed patterns
of predation were based on detection rather than on some
postdetection preference (such as visual familiarity or bait
taste). We therefore were unable to replicate Edmunds and
Dewhirst’s demonstration that countershading enhances
crypsis (compared to uniform dark baits) but were able to
show that observed choices were not likely to be due to
postdetection preferences. Second, order of presentation has
an important though not unexpected effect on behavior; if
birds find the baits on a white background first (garden 1),
they do not significantly discriminate between baits even when
Speed et al.
•
Countershading enhancement of crypsis
they are subsequently placed against the green backgrounds
of the lawn. One explanation for this is that in the initial
presentation with the cards, the birds had time to learn that
all squares in the matrix were likely to contain a bait. Hence,
when baits were presented without cards, it may be that the
birds simply return to places where they previously found food
rewards and choose them in a manner unrelated to their
underlying relative conspicuousness. An implication is that in
factorial, ordered experiments performed using a matrix such
as this, we cannot rely on bait choices from the ‘‘cards-first’’
garden to tell us much about crypsis and the efficacy of
countershading when the background is changed to the colormatching condition.
It could be argued that in this sort of experiment the birds
might approach and view the baits from above, in which case
countershading and reverse shading could not be expected to
have effects. However, it is clear that baits were not exclusively
viewed from above because, for example, the light and
reverse-shaded baits were generally treated differently in
relation to the other baits, even though their upper surfaces
were identical (Figures 1b and 2). Hence, we must conclude that
when countershaded and dark baits are treated as equivalent,
as they were in most experimental trials, it is not primarily
because the birds viewed the baits exclusively from above.
Having marked individuals in the second experiment
enabled us to learn about the different contributions of bird
species to the overall levels of predation seen on each bait.
The first experimental trial of the second experiment, with
individually marked birds, produces similar results to those
seen in garden 1. Overall, the birds chose the baits at different
rates when placed on a color-matching background and
showed no differences on a white background. Again, there
was no significant benefit to countershading in relation to
uniformly dark baits that matched the brown board most
closely. However, consideration of the data at the level of bird
species revealed a hierarchy of choosiness; the blackbirds were
most discriminating (taking the baits in an order of
preference L . R . D ¼ C), robins next (L . D ¼ C ¼ R),
and finally blue tits (no preferences at all). It follows that if we
had rerun the experiment at a different site, with a different
composition of individuals from these species, we might find
quite different results.
One reason that the blackbirds may show higher levels of
prey discrimination is that during feeding they stand on the
board as dominant predators taking multiple baits, whereas
the robins and blue tits flew in from neighboring perches and
generally took one or two baits at a time, with limited time for
visual inspection and perhaps different viewing angles. It is
possible that the blue tits simply followed a spatial rule, flying to the nearest part of the board rather than focusing on
the most conspicuous baits, as the robins appear to have done.
In addition, we cannot rule out the differences in perceptual
system between the bird species as a contributory factor; nor
can we rule out the possibility that the color of the substrate
on which these species normally forage differs and affects
their behavior at the feeding board in complex ways.
Most notably perhaps, in the second trial of this experiment, the blackbirds took countershaded baits more often
than the others when they were placed against a white
background and least often when they were placed against the
brown background. This strongly suggests that for these birds
at this point in the experiment, countershaded baits really
were least readily detected when placed against a colormatching substrate. Furthermore, we can discount the
possibility that the birds are averse to countershaded prey
because they favored them in the contrasting background
condition. Hence, we appear to have evidence that countershading may work to diminish detection rates with some
333
species and not others, which could go some way to explaining why we failed to replicate all components of Edmunds and
Dewhirst’s original results in the first experiment with
unmarked birds.
Conclusions
In one of our four experimental trials, countershading did
enhance protection. Most notably perhaps, when we examined the data for this experimental trial at the species level, it
was clear that only the blackbirds were taking the other baits
at higher rates than countershaded baits. Furthermore, the
three focal bird species took the baits in very different ways in
this experiment, ranging from no selection by color to a high
level of choosiness. If such high levels of predator heterogeneity have some generality, then cryptic appearances of prey
animals may be optimized to minimize overall predation levels
from a suite of different predators.
We have supporting evidence for the hypothesis that
countershading enhances crypsis, but we also have a number
of data sets in which countershading provided no enhancement to crypsis compared to plain dark baits. It may be that
countershading varies in its effectiveness at enhancing crypsis
in visual conditions other than those used in this experiment.
In future experiments, we intend therefore to vary lighting
conditions and the degree of contrast and sharpness of the
contrast boundary between dorsum and ventrum.
Our results do show, however, that in most instances (i.e.,
three of four experiments in color-matching conditions), our
countershaded baits were on average not more or less
vulnerable to predation than the simple, dark ‘‘phenotype,’’
despite having a relatively large area of light pigment.
An important conclusion is that SSC could still apply here
even if the net effect of countershading is to maintain but not
to actually enhance crypsis. If defensive pigmentation incurs
costs, then countershading may be a good way of maintaining
cost-effective crypsis.
APPENDIX
Demonstration that the inclusion/exclusion of the blue tits
does not affect overall conclusions in experiment 2, experimental trial 1. Here we included the blue tits but excluded the
white-board section of the experiment in which the blue tits
were barely represented. Table A1 shows the results from
GLM analysis; Figure A1 shows data for all bird species for this
experimental trial. Overall conclusions about the pattern of
predation are unchanged by removing the blue tits from the
analysis.
Table A1
Results from GLM analysis in which all three bird species are
represented, but white-board data are excluded (experiment 2, trial 1)
Source
Type III
sum of
squares
df
Trial
Prey
Species
Prey 3 species
Error
Total
Corrected total
2.664
40.885
150.729
34.680
388.268
3697.000
610.186
1
3
2
6
1723
1736
1735
Mean
square
2.664
13.628
75.365
5.780
0.225
F
Significance
11.822
60.477
334.443
25.650
.001
,.001
,.001
,.001
Behavioral Ecology
334
3.0
Mean numbers attacked
2.5
2.0
1.5
1.0
0.5
0.0
L
D
C
Prey type
R
Figure A1
Data for experiment 2, experimental trial 2 with all bird species
present.
We thank Tim Caro, Candy Rowe, Ian Harvey, Katherine Allen,
Malcom Edmunds, and an anonymous referee for their help. Technical support was provided by D. Sennett, Liverpool Hope University
College, and D.K. was funded by the Liverpool Hope research fund.
REFERENCES
Braude S, Ciszek D, Berg NE, Shefferly N, 2001. The ontogeny and
distribution of countershading in colonies of the naked mole-rat
(Heterocephalus glaber). J Zool 253:351–357.
Bretagnolle V, 1993. Adaptive significance of seabird coloration: the
case of procellariiforms. Am Nat 142:141–173.
Edmunds M, Dewhirst RA, 1994. The survival value of countershading
with wild birds as predators. Biol J Linn Soc 51:447–452.
Gould SJ, 1991. Bully for brontosaurus. London: Penguin.
Herring PJ, 1994. Reflective systems in aquatic animals. Comp
Biochem Physiol 109A:513–546.
Kiltie RA, 1988. Countershading: universally deceptive or deceptively
universal. Trends Ecol Evol 3:21–33.
Nagaishi H, Nishi H, Fujii R, Oshima N, 1989. Correlation between
body colour and behaviour in the upside-down catfish, Synodontis
nigriventis. Comp Biochem Physiol 92A:323–326.
Phillips GC, 1962. Survival value of the white coloration of gulls and
other seabirds. University of Oxford.
Poulton EB, 1888. Notes in 1887 upon lepidopterus larvae &c. Trans
Entomol Soc Lond 1888:595–596.
Poulton EB, 1902. The meaning of the white undersides of animals.
Nature: 596.
Ramachandran VS, 1988. Perception of shape from shading. Nature
331:163–166.
Ruiter LD, 1956. Countershading in caterpillars: an analysis of its
adaptive significance. Arch Neerl Zool 11:285–341.
Ruxton GD, Speed M, Kelly DJ, 2004. What, if anything, is the adaptive
function of countershading? Anim Behav 68:445–451.
Stauffer JAJ, Hale EA, Seltzer R, 1999. Hunting strategies of a Lake
Malawi Cichlid with reverse countershading. Copeia 1999:1108–
1111.
Stoner CJ, Bininda-Emonds ORP, Caro T, 2003a. The adaptive
significance of coloration in lagomorphs. Biol J Linn Soc 79:309–
328.
Stoner CJ, Caro TM, Graham CM, 2003b. Ecological and behavioral
correlates of coloration in artiodactyls: systematic analyses of
conventional hypotheses. Behav Ecol 14:823–840.
Thayer AH, 1896. The law which underlies protective coloration. Auk
13:124–129.
Turner ERA, 1961. Survival value of different methods of camouflage
as shown in a model population. Proc Zool Soc Lond 136:273–284.
Young RE, Roper CFE, 1976. Intensity regulation of bioluminescence
during countershading in living animals. Fish Bull 75:239–252.