High resolution of colour vision, but low contrast sensitivity in a diurnal raptor

Abstract

Animals are thought to use achromatic signals to detect small (or distant) objects and chromatic signals for large (or nearby) objects. While the spatial resolution of the achromatic channel has been widely studied, the spatial resolution of the chromatic channel has rarely been estimated. Using an operant conditioning method, we determined (i) the achromatic contrast sensitivity function and (ii) the spatial resolution of the chromatic channel of a diurnal raptor, the Harris's hawk Parabuteo unicinctus The maximal spatial resolution for achromatic gratings was 62.3 c deg-1, but the contrast sensitivity was relatively low (10.8-12.7). The spatial resolution for isoluminant red-green gratings was 21.6 c deg-1-lower than that of the achromatic channel, but the highest found in the animal kingdom to date. Our study reveals that Harris's hawks have high spatial resolving power for both achromatic and chromatic vision, suggesting the importance of colour vision for foraging. By contrast, similar to other bird species, Harris's hawks have low contrast sensitivity possibly suggesting a trade-off with chromatic sensitivity. The result is interesting in the light of the recent finding that double cones-thought to mediate high-resolution vision in birds-are absent in the central fovea of raptors.

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Research
Cite this article: Potier S, Mitkus M, Kelber A.
2018 High resolution of colour vision, but low
contrast sensitivity in a diurnal raptor.
Proc. R. Soc. B 285: 20181036.
http://dx.doi.org/10.1098/rspb.2018.1036
Received: 9 May 2018
Accepted: 1 August 2018
Subject Category:
Neuroscience and cognition
Subject Areas:
behaviour, neuroscience
Keywords:
colour vision, contrast sensitivity, foraging,
raptors, spatial resolution
Author for correspondence:
Simon Potier
e-mail: sim.potier@gmail.com
†
Present address: National Institute of Polar
Research, 10-3 Midori-cho, Tachikawa-shi,
Tokyo 190-8562, Japan.
Electronic supplementary material is available
online at https://dx.doi.org/10.6084/m9.
figshare.c.4193288.
High resolution of colour vision, but low
contrast sensitivity in a diurnal raptor
Simon Potier, Mindaugas Mitkus†and Almut Kelber
Department of Biology, Lund University, So
¨lvegatan 35, Lund 22362, Sweden
SP, 0000-0003-3156-7846; AK, 0000-0003-3937-2808
Animals are thought to use achromatic signals to detect small (or distant)
objects and chromatic signals for large (or nearby) objects. While the spatial
resolution of the achromatic channel has been widely studied, the spatial res-
olution of the chromatic channel has rarely been estimated. Using an operant
conditioning method, we determined (i) the achromatic contrast sensitivity
function and (ii) the spatial resolution of the chromatic channel of a diurnal
raptor, the Harris’s hawk Parabuteo unicinctus. The maximal spatial resol-
ution for achromatic gratings was 62.3 c deg
21
, but the contrast sensitivity
was relatively low (10.8–12.7). The spatial resolution for isoluminant red-
green gratings was 21.6 c deg
21
—lower than that of the achromatic channel,
but the highest found in the animal kingdom to date. Our study reveals that
Harris’s hawks have high spatial resolving power for both achromatic and
chromatic vision, suggesting the importance of colour vision for foraging.
By contrast, similar to other bird species, Harris’s hawks have low contrast
sensitivity possibly suggesting a trade-off with chromatic sensitivity. The
result is interesting in the light of the recent finding that double cones—
thought to mediate high-resolution vision in birds—are absent in the central
fovea of raptors.
1. Background
Vertebrate vision has been extensively studied and debated since the important
early works of Walls and Rochon-Duvigneaud [1,2]. One debated question is
whether animals analyse intensity and colour (i.e. achromatic and chromatic)
information of a visual scene combined or separately, and what each of them
is used for. It is now assumed that many animals use achromatic signals for
detection of small objects or fine details, and chromatic signals for large objects
or coarse features [3–5].
While acuity is usually determined using achromatic gratings with high
contrast (e.g. black and white bars) [6], in natural situations, objects of interest
often differ in both contrast and colour to the background. Thus, the visual
acuity threshold provides only partial information about visual capabilities of
an animal as it reveals only the upper limit of spatial resolution for objects of
maximum contrast. The spatial resolution of the achromatic channel has been
estimated in numerous species, but contrast sensitivity remains poorly under-
stood [7], and the spatial resolution of the chromatic channel is known only
in three animal species: humans [8], honeybees Apis mellifera [3] and budgeri-
gars Melopsittacus undulatus [9]. In all three species, it is much lower than the
spatial resolution of the achromatic channel. Humans, for example, have been
shown to resolve achromatic gratings with 30–60 cycles per degree (c deg
21
),
but isoluminant red-green and blue-yellow gratings of less than 10 c deg
21
[8]. In budgerigars, the threshold was close to 4.5 c deg
21
for both red-green
and blue-green gratings [9].
Diurnal raptors (accipitriform and falconiform birds, hereafter called
raptors), renowned for their extraordinarily sharp eyesight, have fascinated
scientists for decades [6]. Among all animals studied to date, some raptors,
such as the wedge-tailed eagle Aquila audax [10], the Indian vulture Gyps
indicus [11] or the brown falcon Falco berigora [12], have the most acute
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vision. High-acuity vision, probably the most important
sensory modality for hunting raptors [13], results from the
large eye size and high cone density in their most acute
zone of vision, the central fovea. Yet, besides visual acuity,
very little is known about raptor vision. Contrast sensitivity
has been studied only in two species, the wedge-tailed
eagle [14] and the American kestrel Falco sparverius [15]
(and only in one individual of each species). Surprisingly,
while these two raptors have high spatial resolution
(142 c deg
21
for the wedge-tailed eagle and 42 c deg
21
for
the American kestrel) compared with non-raptorial birds,
such as the budgerigar (10 c deg
21
), their contrast sensitivity
is similarly low (e.g. 13.6 for the wedge-tailed eagle and 10.2
for the budgerigar) [9,14].
Raptors, like other birds, have four spectrally distinct
types of single cones (violet-sensitive, VS; short-wavelength-
sensitive, SWS; medium-wavelength-sensitive, MWS;
long-wavelength-sensitive, LWS) and one type of double cones
in their retinae, but several raptor species have been shown to
lack double cones in the central fovea [10,12,16]. These findings
challenge the common assumption that raptors, as other birds,
use double cones for achromatic vision and single cones for
chromatic vision [17,18]. Instead, these data suggest that raptors
may use single cones for high achromatic resolution, and that
they may possess highly resolved tetrachromatic vision [16].
However, the spatial resolution of the chromatic channel has
never been estimated in any raptor species.
In this study, we behaviourally determined (i) the achro-
matic contrast sensitivity function (CSF) and (ii) the spatial
resolution limit of the chromatic channel in a diurnal raptor,
the Harris’s hawk Parabuteo unicinctus. This species mainly
hunts live mammals, and high spatial resolution may be
important to detect prey at distance. Some recently studied
aspects of its vision suggest that Harris’s hawks are highly
visually specialized to their foraging demands [19,20]. They
have a broad binocular field (478), a deep centraland a shallow
temporal fovea, and high spatial resolution of achromatic
vision (the maximum visual acuity measured in one animal
was 43.7 c deg
21
) [19]. Thus, Harris’s hawks have a similar
achromatic acuity as humans [21] allowing for an interesting
comparison of the chromatic spatial resolution and the CSF.
2. Methods
(a) Experimental subjects
Experimental animals were three healthy adult female Harris’s
hawks (subjects A, B and C), belonging to the French falconry
park Les Ailes de l’Urga that were used in a previous study for
visual acuity estimation [19]. All three individuals were raised
in the raptor facility and used for public shows in the summer
season. During the period of this study (Experiment 1, contrast
sensitivity function: 25 April to 3 July 2017; Experiment 2, chro-
matic spatial resolution: 5 October to 26 November 2017), the
birds’ body weight was controlled every day and maintained
at about 90% of their free feeding weight. Water was provided
ad libitum, whereas food (chicken meat) was given only during
the experiments. If a bird did not perform well in a daily session,
it received more food for every correct choice the day after. Train-
ing and experimentation took place 5 days per week. The hawks
were housed together in an aviary and hand-fed by the falconer
when no experiments took place. During the experiment, they
were placed outside their aviaries and attached to an adapted
falconry perch.
(b) Experimental room and aviary
The CSF (Experiment 1) was measured outdoors, in an aviary of
8 m width, 7.5 m length and 3 m height. A diffusing tarpaulin
was placed on the top of the aviary. The aviary wall behind
the monitors used to present the stimuli was covered with a
grey tarpaulin. The experiments were conducted from 10 to
13 h in order to avoid the birds facing the sun while flying.
No experiments were performed under very cloudy or rainy
conditions. Before every session, we measured the illuminance
at the starting perch, using an LCD Digital light meter (Tasi
HS1010). The average illuminance was 9400 +1200 lx (mean +
s.e.) and ranged from 3730 to 17780 lx, which corresponds to
full daylight (but without direct sun).
The chromatic spatial resolution measurements (Experiment
2) were conducted in a room of 7.5 m width, 6 m length and
3 m height. A neutral-white LED lamp (flicker frequency
100 Hz; Xanlite, France) was used to light up the room. The
illuminance at the starting perch was 210 lx.
In both experiments, two monitors for stimulus presentation
were positioned on one side of the room, at 5 m distance from
each other. Under each of the monitors, a perch was attached
to a feeding box, which had ten compartments with a piece of
chicken meat in each. Individual compartments could be
opened remotely using an electric motor to expose the meat as
a reward for a correct choice [19]. A starting perch was
positioned 5 m from the screens on the other side of the room.
(c) Stimuli
Stimuli were created in R v. 3.4.1 (R Development Core Team,
2017) and presented using Microsoft Office POWERPOINT 2016 on
two computer monitors (display size 476 266 mm; Samsung
S22C300H). The stimuli (238 133 mm) were presented in the
centre of the screens and subtended 2.7 1.5 degrees of visual
angle, when observed from the starting perch. We presented
the stimuli only in the central part of the monitor where the
luminance was most uniform (175 cd m
22
measured with
Hagner ScreenMaster, B. Hagner, Solna, Sweden).
Negative stimuli were achromatic square-wave gratings of
different spatial frequencies and contrasts (Experiment 1) or
red-green gratings of different spatial frequencies and fixed
colour contrast (Experiment 2). The positive stimulus was a
grating with very high spatial frequency (175.8 c deg
21
) of the
same achromatic (Experiment 1) or chromatic (Experiment 2)
contrast and mean luminance as the simultaneously presented
negative stimulus. Gratings of such high spatial frequency
should appear as uniform field for a Harris’s hawk, because
the maximum visual acuity determined previously in this species
was 43.7 c deg
21
(97% Michelson contrast [19]). The radiance
spectra of the red and green bars of the chromatic grating were
measured with a spectroradiometer RSP900-R (International
Light).
The chromatic stimuli (red-green gratings, Experiment 2)
were designed to have high chromatic and low achromatic
contrast. We assumed that chromatic vision is driven by signals
from single cones, while double cones mediate achromatic
vision [7,18]. Because no data on the Harris’s hawks retina
exist, the red-green gratings were created based on the relative
cone abundances and spectral sensitivities of the common
buzzard Buteo buteo [17], another closely related member of the
Accipitridae family, and the receptor noise-limited model of
colour discrimination [22].
The cone spectral sensitivities and achromatic contrasts of the
stimuli were modelled as described in detail by Lind et al. [17]
(see electronic supplementary material, table S1 and figure S1).
Briefly, the peak wavelength (
l
max
) of the sws1 pigment sensi-
tivity (405 nm in common buzzard [23]) was used to predict
l
max
of the pigments of other cone types and oil droplet
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transmittance spectra [24]; ocular media transmittance (OMT; t
50
at 375 nm), pigment absorption coefficient (0.035 mm
21
), cone
outer segment length (10 mm), the Weber fraction of the
LWS mechanism (0.1) and the cone abundance ratio of 1 : 2 : 2 : 4
(VS : SWS : MWS : LWS) were taken from Lind et al. [17]. The
photoreceptor spectral sensitivities were modelled using a
visual pigment template [25]. Based on this established
method, the chromatic contrast between the red and green bars
was 25 JNDs ( just noticeable differences; the discrimination
threshold is 1 JND). Spectral reflectances and quantum catches
of all cone types for these colours are given in the excel-file in
the electronic supplementary material.
The achromatic contrast was calculated as Michelson contrast
[26] for the double cones. Because pigmentation of the oil droplet
of raptor double cones is unknown and cannot be predicted by a
model [24], we calculated a range of achromatic contrasts by
varying the cut-off wavelength of the double cone oil droplet
l
cut
from 400 to 500 nm (see electronic supplementary material,
figure S1). The double cone contrast between red and green
bars (varying from 8.6% to 2.7%, respectively) was lower than
or very similar to the minimum achromatic contrast threshold
(see results of Experiment 1).
As the use of only the double cones for achromatic vision is
hypothetical and other raptors have been shown to lack them
in the fovea [16], we also calculated the Michelson contrast
between red and green bar colours, for each single cone type
(see electronic supplementary material, table S1).
(d) Behavioural experiment
The CSF (contrast sensitivity refers to the inverse of Michelson
Contrast) and the spatial resolution of the chromatic channel of
the Harris’s hawks were measured using an operant conditioning
technique, involving two phases as described below.
(i) Conditioning
Sitting on the starting perch, the birds were required to choose
between the positive (rewarded) and a negative (unrewarded)
stimulus. As negative stimuli, gratings were used with low
spatial frequency (either 1.1 or 2.9 c deg
21
) and high achromatic
(69% Michelson contrast; Experiment 1) or high chromatic
contrast (25 JND; Experiment 2).
The side of the positive and negative stimuli was changed in
a pseudo-random order (i.e. the positive stimulus was not pre-
sented on the same side for more than three consecutive trials).
A session consisted of 40 trials, and the positive stimulus was
presented 20 times on each side.
When the bird opened the wings to leave the starting perch,
the monitors were switched off to ensure that the bird could not
change the decision on its way. If the bird chose the positive
stimulus, a compartment with meat was opened after the bird
landed on the perch. The experimenter was hiding in a cabin
to avoid any visual contact and influence on the bird’s choice.
Two training sessions were conducted daily. When a bird
reached 80% correct choices in two consecutive sessions, the
training phase ended and the test phase began.
(ii) Testing
As in the conditioning phase, two sessions of 40 trials were
conducted with each bird every day, and the side of the positive
stimulus was varied pseudo-randomly. Before each test
session, we presented five low-frequency gratings (either 1.1 or
2.9 c deg
21
) to ensure that the bird was still conditioned.
For Experiment 1, achromatic gratings of six spatial frequen-
cies (1.1, 2.9, 5.9, 11.7, 22.0, 35.2 c deg
21
) were used. Each
frequency was tested with six to nine different Michelson
contrasts (from 69, 53, 29, 25, 20, 18, 15, 9, 6 and 3%). High-
frequency gratings were tested with fewer different contrasts.
During a single session, only one spatial frequency was pre-
sented, but with all contrasts. Tests were repeated until each
bird had completed 40 choices for each combination of spatial
frequency and contrast needed to establish the CSF.
For Experiment 2, eight spatial frequencies (1.1, 2.9, 5.9, 7.3,
11.7, 22.0, 35.2 and 44.0 c deg
21
) of the red-green gratings
were used and tested in each session. The tests were repeated
until each bird had completed 40 choices for each spatial
frequency.
(e) Data analysis
All analyses were performed with R v. 3.4.1 using fpsyphyg[27]
and fggplot2g[28] packages. Psychometric functions were fitted
to the choice frequencies from each bird in each test. From
these functions, the detection threshold (72.5% correct choices,
binomial test, n¼40, p,0.01) was determined. A double-
exponential function was fitted to the contrast sensitivity data
using a method of least squares [29].
3. Results
Three individuals were used in both experiments, but while
Harris’s hawk B performed in both experiments, we obtained
only the CSF for Harris’s hawk A, and only the chromatic
spatial resolution for Harris’s hawk C.
To build the CSF, the contrast sensitivity threshold was
interpolated for each spatial frequency using psychometric
functions (figure 1a,b for examples). Contrast sensitivity is
given as the inverse of the stimulus contrast, at which dis-
crimination performance was at threshold level (72.5%;
figure 1c). We found maximum contrast sensitivities of 10.8
and 12.7 at spatial frequencies of 7.9 and 5.3 c deg
21
for
Harris’s hawk A and B, respectively. These sensitivities
correspond to Michelson contrasts of 9.3% and 7.9%. The
extrapolated spatial resolution at highest contrast (contrast
sensitivity ¼1) was 39.5 c deg
21
for Harris’s hawk A and
62.3 c deg
21
for Harris’s hawk B.
With the red-green gratings, we obtained the spatial
resolution of the chromatic channel for Harris’s hawks B
and C. The threshold was 21.6 c deg
21
for Harris’s hawk
B and 16.4 c deg
21
for Harris’s hawk C (figure 2).
4. Discussion
We determined the achromatic CSF function and the spatial
resolution of the chromatic (red-green) channel of Harris’s
hawks, an actively hunting diurnal raptor species. While
the highest achromatic spatial resolution of Harris’s hawks
(40–60 c deg
21
) is in a similar range as in humans [21], the
highest contrast sensitivity (11– 12) is approximately ten
times lower than that in humans [21], and the resolution for
red-green gratings (16– 22 c deg
21
) is twice as high ( figure 3).
(a) Achromatic contrast sensitivity function
The shape of the CSF in Harris’s hawks is similar to that of
other raptors [14,15] and other vertebrates tested so far
[9,29,30,32,33]. The maximum contrast sensitivity of 12.7 is
close to the CS found in the most closely related species
studied to date, the wedge-tailed eagle (13.6) [14], but lower
than in the American kestrel (30) [15]. While the maximum
contrast sensitivity of these birds occurred at a spatial resol-
ution of 10 c deg
21
[14,15], the maximum contrast
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sensitivity of Harris’s hawks was found at 5.3 and
7.9 c deg
21
. This suggests that maximum contrast sensitivity
and visual acuity are not directly related in raptors. It is
unclear why raptors—and generally all birds tested so far—
have such low contrast sensitivity, but it has been suggested
that birds may trade contrast sensitivity for other visual
0.4
0.6
0.8
1.0
0.4
0.6
0.8
1.0
0 10 20 30 0 10 20 30
fraction of correct responses
contrast sensitivity
11.72 (c deg–1) 21.97 (c deg–1)
contrast sensitivity
0.5 1.0 2.0 5.0 10 20 50 100
1
2
5
10
spatial frequenc
y
(c de
g
–1)
contrast sensitivity
(b)(a)
(c)
Figure 1. The behavioural contrast sensitivity function of Harris’s hawks. (a,b) Examples of two psychometric functions from contrast threshold tests of (a) Harris’s
hawk A and (b) Harris’s hawk B with different spatial frequencies. Each circle represents 40 choices made by one bird. Vertical lines are threshold values interpolated
from logistic functions that were fitted to the data. All curves are given in the electronic supplementary material, figure S2. (c) Contrast sensitivity, defined as the
inverse of contrast threshold, as a function of spatial frequency. Sensitivity values were fitted to a double exponential function (see methods). Red, Harris’s hawk A;
blue, Harris’s hawk B; black, the pooled data. Filled squares at the baseline represent the spatial resolution threshold extrapolated from the contrast sensitivity
function. Triangles represent the spatial resolution threshold of the same two individuals determined in the study of Potier et al. [19]. (Online version in colour.)
Harris’s hawk B
0.4
0.6
0.8
1.0
fraction of correct responses
Harris’s hawk C
0.4
0.6
0.8
1.0
0 1020304050
spatial frequency (c deg–1)
01020304050
spatial frequency (c deg–1)
(b)(a)
Figure 2. Psychometric functions used to determine the chromatic spatial resolution of (a) Harris’s hawk B and (b) Harris’s hawk C. Each circle represents 40 choices
made by one bird. Vertical segments are threshold values, which were interpolated from logistic functions that were fitted to the data. (Online version in colour.)
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abilities, such as chromatic sensitivity [33], which would be in
agreement with the high chromatic spatial resolution found
in this study.
From the CSF, we extrapolated the maximum resolving
power of Harris’s hawks. The visual acuity of the same two
individuals has also been determined in a previous study
[19]. The spatial resolution of 40 to 60 c deg
21
agrees well
with an anatomical estimation based on eye size alone [19]
or presumed focal length and a hexagonal cone mosaic
with cone centre-to-centre distances of 2 to 2.5 mm, which is
slightly larger than the 1.6 mm cone centre-to-centre distances
determined anatomically in the deep fovea of the wedge-
tailed eagle [11]. If all cone types contributed to achromatic
vision and no spatial summation took place in Harris’s
hawks’ fovea, this would indicate relatively moderate
maximum densities of 200 000 cones mm
22
.
For Harris’s hawk A, the extrapolated resolving power is
similar to the value from an earlier direct measurement of
resolution (39.5 versus 42.8 c deg
21
[19]), as has been found
by similar extrapolations in other bird species [9,30,34]. By
contrast, the results for Harris’s hawk B differ markedly
(62.3 versus 35.3 c deg
21
[19]), which is surprising. In the pre-
vious experiment [19], individuals that made more horizontal
head movements before choosing a stimulus showed a higher
visual acuity. In that study, Harris’s hawk B made very few
head movements before each choice (1.6 +0.2; mean +s.e.),
suggesting that its visual acuity may have been underesti-
mated. In the present study, Harris’s hawk B was more
attentive and made more head movements (S.P. 2017, per-
sonal observation), which may explain the higher visual
acuity threshold. This suggests that readers should rely
more on the maximum, not the average of behaviourally
determined visual acuity for a species, because indivi-
duals differ in attention not only between conditioning
experiments, but even from session to session.
Finally, all these values and interpretations need to be
taken with caution. Using stimuli with a luminance of
175 cd m
22
, we may have slightly underestimated the
American kestrel
human
barn owl
wedge-tailed
eagle
Harris’s
hawk
spatial resolution (c de
g
–1)
contrast sensitivity
0.1 1 10
1
10
100
rock dove
budgerigar
cat
achromatic threshold :
chromatic threshold :
budgerigar
human
Harris’s hawk
Harris’s
hawk
contrast sensitivity
0.1 1 10
1
10
100
(a)
(b)
(c)
Figure 3. Comparison of the vision of Harris’s hawks and other animals. (a) Contrast sensitivity of Harris’s hawks (average of two birds). (b) Comparison of the
contrast sensitivity function of Harris’s hawks (red-brown) and other animals (diurnal raptors in blue, nocturnal raptor in green, non-raptorial birds in pink and
human in black). The spatial resolution thresholds of achromatic (filled symbols) vision are represented for budgerigars, humans and Harris’s hawks. (c) Spatial
resolution thresholds of chromatic vision of budgerigars, humans and Harris’s hawks (open symbols). References: humans [8,21], American kestrel [15], wedge-tailed
eagle [14], barn owl [30] rock dove [31] and budgerigar [9]. (Online version in colour.)
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absolute maximum of resolution. We do not, however, think
the difference could be large. In the wedge-tailed eagle, the
resolution determined at 200 cd m
22
was 128 c deg
21
, com-
pared with 136 c deg
21
at 2000 cd m
22
, thus an increase of
less than 10% with a 10-fold increase in luminance [11].
(b) Chromatic spatial resolution
In Harris’s hawks, similar to budgerigars [9], the spatial
resolution of the chromatic channel is lower than that
of the achromatic channel. This indicates that they can
detect prey providing maximum achromatic contrast to
the background from a larger distance than prey only pro-
viding chromatic contrast. The chromatic spatial resolution
of Harris’s hawks for red-green stimuli with high colour
contrast is the highest found to date among animals,
twiceashighasmeasuredinhumans(below10cdeg
21
)
[8] and five times higher than in budgerigars (4cdeg
21
)
[9]. Both previous studies found the same resolution
threshold for red-green gratings as for other colour
gratings, blue-green for budgerigars [9] and blue-yellow
for humans [8]. Although we cannot be sure, we are there-
fore rather confident that our result is not specific for this
particular colour combination, either. Because raptors lack
double cones in their fovea, it has recently been suggested
that they may have high chromatic spatial resolution [16].
Our study provides the first evidence that this is true for
one raptor species.
With the eye the size of Harris’s hawks [11], the resolution of
20 c deg
21
requires a cone centre-to-centre distance of 6mm.
A cone abundance ratio of 1 : 2 : 2 : 4 (VS : SWS : MWS : LWS)
and the estimated total density of 200 000 cones mm
22
contributing the achromatic resolution would mean that the
rarest cone type (VS) would have cone centre-to-centre dis-
tances of 6mm and thus determine the chromatic
resolution limit. This estimation is rather conservative. As
nothing is known about the specific opponent channels
underlying bird colour vision, it assumes that resolution of
the chromatic channel is limited by the cone type with
lowest density in the retina. The red-green gratings did
have high contrast for the SWS, MWS and LWS cone types;
therefore, we cannot completely exclude the possibility that
the threshold is set by some achromatic mechanism involving
only single cones.
We used red-green gratings that were isoluminant for
the double cones, assuming receptor properties reported in
the literature for another accipitriform bird, the common
buzzard. However, these assumptions come with some
uncertainty. For example, in the visual streak of the wedge-
tailed shearwater Puffinus pacificus, the oil droplet coloration
is greatly reduced and no yellow or red oil droplets are
present [35]. It is unknown whether anything similar is the
case in the fovea of raptors. However, even if all oil droplets
were transparent (
l
cut
at 300 nm), our stimulus would still
generate a high chromatic contrast (10.93 JNDs) and sub-
threshold achromatic contrast (8.6%). Therefore, we consider
that the red-green grating used in this study is isoluminant
for the double cones.
(c) Vision and foraging ecology of Harris’s hawks
How do spatial resolution and CS relate to the ecological
needs of Harris’s hawks? Harris’s hawks live mainly in dry
environments and forage mainly on mammals [36]. From a
foraging perspective, the contrast between prey and back-
ground may be important and while the maximum contrast
sensitivity of the birds is relatively low, it is certainly suffi-
cient to detect and catch the prey. In addition, while it has
been shown that raptors cannot use UV cues for prey detec-
tion [17], the high spatial resolution of chromatic vision found
in our study suggests a potentially important role of colour
vision for foraging. Furthermore, it is possible that contrast
sensitivity is higher for moving stimuli, as found in budger-
igars [37]. In another raptor species, the American kestrel,
prey motion has been found to be a better predictor of prey
detection than prey size [38].
Finally, it is important to note that all three species of
raptors studied so far for CSF live in open habitats, where–
at least on a sunny day—achromatic contrasts, caused for
instance by sharp shadows, are higher and thus may be
more important than in closed environments (such as dense
forest; Dan-E. Nilsson 2018, personal communication). It
would be interesting to estimate the CSF of a raptor that
lives in a closed habitat to see whether living in a different
environment leads to higher contrast sensitivities.
5. Conclusion
Because raptors are considered to be mainly visually guided
foragers, and some species have high visual acuity [13], it has
long been suggested that raptors have generally superior
visual abilities compared to other animals. In this study, we
showed that Harris’s hawks have the highest chromatic
visual acuity threshold found to date, suggesting that they
can discriminate an object (e.g. a prey) that is isoluminant
but differs in colour from the background at long distance.
However, while its achromatic visual acuity is indeed high
for its body size, the maximum contrast sensitivity is similar
to that of other birds (figure 3; and see [30] for a review). This
illustrates that the perfect eye is not necessarily an eye with
high performance in every domain, but an eye adapted to
the behaviour and ecology of a species [39,40]. For Harris’s
hawks, this involves having high chromatic and achromatic
spatial resolution and relatively low contrast sensitivity.
Ethics. The study was conducted under a formal agreement between
the animal rearing facility Les Ailes de l’Urga (France) and Lund
University (Sweden). In agreement with French law, the birds were
handled by their usual trainers under the permit of Les Ailes de
l’Urga (national certificate to maintain birds ‘Certificat de capacite’
delivered to the director of the falconry, Patrice Potier, on 20
June 2006).
Data accessibility. The datasets supporting this article have been
uploaded electronic supplementary material.
Authors’ contributions. S.P., M.M. and A.K. designed the study. S.P. per-
formed the experiments, analysed the data and wrote the manuscript
with contributions by all authors.
Competing interests. We have no competing interests.
Funding. This study was financially support by the Swedish Research
Council (2016-03298) and the K. & A. Wallenberg Foundation
(Ultimate Vision).
Acknowledgements. We thank P. Potier and N. Descarsin from Les Ailes
de l’Urga for allowing to perform experiments with their birds. We
also thank M. Lieuvin for her help with the fieldwork. Thanks to
O. Lind and P. Olsson for the help with modelling, stimulus
preparation and fitting of the contrast sensitivity function.
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