ArticlePDF Available

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

  • Institute of Biosciences, Life Sciences Center, Vilnius University

Abstract and Figures

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.
Content may be subject to copyright.
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.
Received: 9 May 2018
Accepted: 1 August 2018
Subject Category:
Neuroscience and cognition
Subject Areas:
behaviour, neuroscience
colour vision, contrast sensitivity, foraging,
raptors, spatial resolution
Author for correspondence:
Simon Potier
Present address: National Institute of Polar
Research, 10-3 Midori-cho, Tachikawa-shi,
Tokyo 190-8562, Japan.
Electronic supplementary material is available
online at
High resolution of colour vision, but low
contrast sensitivity in a diurnal raptor
Simon Potier, Mindaugas Mitkusand 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
, but the contrast sensitivity
was relatively low (10.8–12.7). The spatial resolution for isoluminant red-
green gratings was 21.6 c deg
—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
but isoluminant red-green and blue-yellow gratings of less than 10 c deg
[8]. In budgerigars, the threshold was close to 4.5 c deg
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
&2018 The Author(s) Published by the Royal Society. All rights reserved.
on August 29, 2018 from
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
for the wedge-tailed eagle and 42 c deg
the American kestrel) compared with non-raptorial birds,
such as the budgerigar (10 c deg
), 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
) [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
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
) 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
(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
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 (
) of the sws1 pigment sensi-
tivity (405 nm in common buzzard [23]) was used to predict
of the pigments of other cone types and oil droplet Proc. R. Soc. B 285: 20181036
on August 29, 2018 from
transmittance spectra [24]; ocular media transmittance (OMT; t
at 375 nm), pigment absorption coefficient (0.035 mm
), 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
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
) 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
) 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
) 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
) 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
(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
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
for Harris’s hawk A and
62.3 c deg
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
for Harris’s hawk
B and 16.4 c deg
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
) 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
) 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
[14,15], the maximum contrast Proc. R. Soc. B 285: 20181036
on August 29, 2018 from
sensitivity of Harris’s hawks was found at 5.3 and
7.9 c deg
. 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 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
spatial frequenc
(c de
contrast sensitivity
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
fraction of correct responses
Harris’s hawk C
0 1020304050
spatial frequency (c deg–1)
spatial frequency (c deg–1)
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.) Proc. R. Soc. B 285: 20181036
on August 29, 2018 from
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
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
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
[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
[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
, we may have slightly underestimated the
American kestrel
barn owl
spatial resolution (c de
contrast sensitivity
0.1 1 10
rock dove
achromatic threshold :
chromatic threshold :
Harris’s hawk
contrast sensitivity
0.1 1 10
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.) Proc. R. Soc. B 285: 20181036
on August 29, 2018 from
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
was 128 c deg
, com-
pared with 136 c deg
at 2000 cd m
, 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,
[8] and five times higher than in budgerigars (4cdeg
[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
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
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 (
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. Proc. R. Soc. B 285: 20181036
on August 29, 2018 from
1. Rochon-Duvigneaud A. 1943 Les yeux et la vision
des verte
´s. Paris, France: Masson.
2. Walls GL. 1942 The vertebrate eye and its adaptive
radiation. New York, NY: Hafner Publishing Co
(fascimile of 1942 edition).
3. Giurfa M, Vorobyev M, Brandt R, Posner B, Menzel
R. 1997 Discrimination of coloured stimuli by
honeybees: alternative use of achromatic and
chromatic signals. J. Comp. Physiol. A 180,
235–243. (doi:10.1007/s003590050044)
4. Osorio D, Miklo
´si A, Gonda Z. 1999 Visual ecology
and perception of coloration patterns by domestic
chicks. Evol. Ecol. 13, 673– 689. (doi:10.1023/
5. Spaethe J, Tautz J, Chittka L. 2001 Visual constraints
in foraging bumblebees: flower size and color affect
search time and flight behavior. Proc. Natl Acad. Sci.
USA 98, 3898–3903. (doi:10.1073/pnas.
6. Mitkus M, Potier S, Martin GR, Duriez O, Kelber A.
2018 Raptors vision. In Oxford research encyclopedia
of neuroscience. Oxford, UK: Oxford University Press.
7. Olsson P, Lind O, Kelber A. 2018 Chromatic and
achromatic vision: parameter choice and limitations
for reliable model predictions. Behav. Ecol. 29,
273–282. (doi:10.1093/beheco/arx133)
8. Mullen KT. 1985 The contrast sensitivity of human
colour vision to red-green and blue-yellow
chromatic gratings. J. Physiol. 359, 381–400.
9. Lind O, Kelber A. 2011 The spatial tuning of
achromatic and chromatic vision in budgerigars.
J. Vision 11, 1–9. (doi:10.1167/11.7.2)
10. Reymond L. 1985 Spatial visual acuity of the eagle
Aquila audax: a behavioural, optical and anatomical
investigation. Vision Res. 25, 1477–1491. (doi:10.
11. Fischer AB. 1969 Laboruntersuchungen und
Freilandbeobachtungen Zum Sehvermo
¨gen und
Verhalten Von Altweltgeiern. Zool. Jahrb. Syst.
96, 81–132.
12. Reymond L. 1987 Spatial visual acuity of the
falcon, Falco berigora: a behavioural, optical and
anatomical investigation. Vision Res. 27,
1859–1874. (doi:10.1016/0042-6989(87)90114-3)
13. Jones MP, Pierce KE, Ward D. 2007 Avian vision: a
review of form and function with special
consideration to birds of prey. J. Exo. Pet. Med.
16, 69–87. (doi:10.1053/j.jepm.2007.03.012)
14. Reymond L, Wolfe J. 1981 Behavioural
determination of the contrast sensitivity function of
the eagle Aquila audax.Vision Res. 21, 263–271.
15. Hirsch J. 1982 Falcon visual sensitivity to grating
contrast. Nature 300, 57– 58. (doi:10.1038/
16. Mitkus M, Olsson P, Toomey MB, Corbo JC, Kelber A.
2017 Specialized photoreceptor composition in the
raptor fovea. J. Comp. Neurol. 525, 2152–2163.
17. Lind O, Mitkus M, Olsson P, Kelber A. 2013
Ultraviolet sensitivity and colour vision in raptor
foraging. J. Exp. Biol. 216, 1819–1826. (doi:10.
18. Martin G, Osorio D. 2008 Vision in birds. In The
senses: a comprehensive reference, vol. 1 (eds AI
Basbaum, A Kaneko, GM Shepherd, G Westheimer),
pp. 25–52. Amsterdam, The Netherlands: Elsevier.
19. Potier S, Bonadonna F, Kelber A, Martin GR, Isard
P-F, Dulaurent T, Duriez O. 2016 Visual abilities in
two raptors with different ecology. J. Exp. Biol. 291,
2639–2649. (doi:10.1242/jeb.142083)
20. Potier S, Mitkus M, Bonadonna F, Duriez O, Isard
P-F, Dulaurent T, Mentek M, Kelber A. 2017 Eye
size, fovea, and foraging ecology in accipitriform
raptors. Brain Behav. Evol. 90, 232– 242. (doi:10.
21. Berkley M. 1976 Cat visual psychophysics: Neural
correlates and comparison with man. In Progress
in psychobiology and physiological psychology, vol. 6
(eds J Sprague, A Epsteine), pp. 63– 119. London,
UK: Academic Press.
22. Vorobyev M, Osorio D. 1998 Receptor noise as a
determinant of colour thresholds. Proc. R. Soc. Lond.
B265, 351–358. (doi:10.1098/rspb.1998.0302)
23. O
¨deen A, Ha
˚stad O. 2003 Complex distribution of
avian color vision systems revealed by sequencing
the SWS1 opsin from total DNA. Mol. Biol. Evol. 20,
855–861. (doi:10.1093/molbev/msg108)
24. Hart NS, Vorobyev M. 2005 Modelling oil droplet
absorption spectra and spectral sensitivities of bird
cone photoreceptors. J. Comp. Physiol. A 191,
381–392. (doi:10.1007/s00359-004-0595-3)
25. Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG,
Donner K. 2000 In search of the visual pigment
template. Vis. Neurosci. 17, 509– 528. (doi:10.1017/
26. Michelson A. 1927 Studies in optics. Chicago, IL:
University of Chicago Press.
27. Knoblauch K. 2007 psyphy: Functions for analyzing
psychophysical data in R. R package version 00– 5.
See http://cran/R-project org/package¼psyphy.
28. Wickham H, Chang W. 2014 ggplot2: an
implementation of the grammar of graphics. See
29. Uhlrich DJ, Essock EA, Lehmkuhle S. 1981
Cross-species correspondence of spatial contrast
sensitivity functions. Behav. Brain Res. 2, 291– 299.
30. Harmening WM, Nikolay P, Orlowski J, Wagner H.
2009 Spatial contrast sensitivity and grating acuity
of barn owls. J. Vision 9, 13. (doi:10.1167/9.7.13)
31. Hodos W, Ghim MM, Potocki A, Fields JN, Storm T.
2002 Contrast sensitivity in pigeons: a comparison
of behavioral and pattern ERG methods. Doc.
Ophthalmol. 104, 107–118. (doi:10.1023/
32. De Valois RL, De Valois KK. 1990 Spatial vision.
New York, NY: Oxford University Press.
33. Ghim MM, Hodos W. 2006 Spatial contrast
sensitivity of birds. J. Comp. Physiol. A 192,
523–534. (doi:10.1007/s00359-005-0090-5)
34. Lind O, Sunesson T, Mitkus M, Kelber A. 2012
Luminance-dependence of spatial vision in
budgerigars (Melopsittacus undulatus) and Bourke’s
parrots (Neopsephotus bourkii). J. Comp. Physiol. A
198, 69–77. (doi:10.1007/s00359-011-0689-7)
35. Hart NS. 2004 Microspectrophotometry of visual
pigments and oil droplets in a marine bird, the
wedge-tailed shearwater Puffinus pacificus:
topographic variations in photoreceptor spectral
characteristics. J. Exp. Biol. 207, 1229– 1240.
36. Del Hoyo J, Elliot A, Sargatal J (eds). 1994 Handbook
of the birds of the world. vol. 2: New world vulturesto
Guineafowl. Barcelona, Spain: Lynx Editions.
37. Haller NK, Lind O, Steinlechner S, Kelber A. 2014
Stimulus motion improves spatial contrast
sensitivity in budgerigars (Melopsittacus undulatus).
Vision Res. 102, 19– 25. (doi:10.1016/j.visres.2014.
38. Sarno R, Gubanich A. 1995 Prey selection by Wild
American Kestrels-the influence of prey size and
activity. J. Rapt. Res. 29, 123– 126.
39. Land MF, Nilsson D-E. 2012 Animal eyes. Oxford, UK:
Oxford University Press.
40. Martin GR. 2017 The sensory ecology of birds.
Oxford, UK: Oxford University Press. Proc. R. Soc. B 285: 20181036
on August 29, 2018 from
... Contrast sensitivity, or spatial resolution regarding two adjacent objects, is highly dependent on the luminance and achromatic contrast of stimuli (Potier et al. 2020a). Without enough contrast between adjacent objects, spatial resolution is severely impaired (wedge-tailed eagles can only resolve 10 cycles/degree at 7% contrast) (Potier et al. 2018a;Harmening et al. 2009;Hirsch 1982;Reymond and Wolfe 1981;Ghim and Hodos 2006). Humans are more sensitive at all frequencies compared to the wedge-tailed eagle, and up to 100 times more sensitive at low frequencies, surely due to the tradeoff for eagles to achieve higher resolution in high luminance and high contrast conditions (Reymond and Wolfe 1981). ...
... A good example is Harris's hawk, which has lower contrast sensitivity but is able to resolve at twice the frequency (over 20 cycles/degree) of humans when pure chromatic patterns are provided (Potier et al. 2018a;Mullen 1985). Although only a third that of the spatial resolution of Harris's hawks in an achromatic setting, it is still the highest chromatic contrast sensitivity measured to date (Potier et al. 2018a). ...
... A good example is Harris's hawk, which has lower contrast sensitivity but is able to resolve at twice the frequency (over 20 cycles/degree) of humans when pure chromatic patterns are provided (Potier et al. 2018a;Mullen 1985). Although only a third that of the spatial resolution of Harris's hawks in an achromatic setting, it is still the highest chromatic contrast sensitivity measured to date (Potier et al. 2018a). Achromatic signals are considered to be preferred for visualization of small/distant objects, while chromatic signals are used for large/near objects (Potier et al. 2018a). ...
Birds of prey, also collectively known as raptors, consist of the Falconiformes (falcons and caracaras), Accipitriformes (eagles, buzzards, hawks, kites, and Old World vultures), Cathartiformes (New World vultures), Cariamiformes (seriemas), and Strigiformes (true owls Strigidae, and barn owls Tytonidae) (del Hoyo et al. 1999; Jarvis et al. 2014; McClure et al. 2019). Although grouped together as key apex predators, raptors are phylogenetically heterogenous assimilation with many morphological and ecological differences. Perhaps a most obvious example is revealed in their activity patterns, where most raptors are considered diurnal, except the owls, which are considered nocturnal, a habit they share with two other avian orders for which we have genome sequences (Caprimulgiformes and Apterygiformes) (Martin 1990; Mikkola 1983; Martin 2017; Zhan et al. 2013). However, the ferruginous pygmy owl Glaucidium brasilianum maintains some activity during the day and the snowy owl Bubo scandiacus hunts during the daytime, the American barn owl Tyto furcate is most active in twilight, the burrowing owl Athene cunicularia is cathemeral, and the stripped owl Asio clamator is crepuscular and nocturnal (del Hoyo et al. 1999; Martins and Egler 1990; Motta-Junior 2006; Motta-Junior et al. 2004; Sarasola and Santillan 2014; Martin 1986). Overall, as a group, owls actually exhibit a broad range of activity patterns and habitats (Bowmaker and Martin 1978; Braga 2006). Additionally, nearly one-third of falconiform species, as well as some accipitriformes species, maintain activity during the crepuscular period (Mitkus et al. 2018).
... Colour vision enables many birds to differentiate between lights of very similar wavelengths, perhaps giving some species the highest levels of spectral resolution among vertebrates (Wright 1972;Wright 1979). However, even with high spectral resolution the ability to resolve spatial detail using coloured light is below that of spatial resolution involving achromatic patterns (Potier et al. 2018). ...
... Although particular colours may have salience for particular species in the mediation of specific behaviours (Endler et al. 2005;Endler et al. 2014) acuity for coloured patterns have been shown to be significantly lower than for black and white patterns. This, this has been demonstrated in budgerigars Melopsittacus undulatus (Lind and Kelber 2011) and in Harris's hawks Parabuteo unicinctus (Potier et al. 2018). Given the phylogenetic distance between these species and their marked differences in ecology, lower acuity for chromatic stimuli is likely to be a feature of the vision of all bird species, probably a feature of all visual systems. ...
Full-text available
Natural England Commissioned Report NECR432
... Color vision enables many birds to differentiate between lights of very similar wavelengths, perhaps giving some species the highest levels of spectral resolution among vertebrates (Wright, 1972(Wright, , 1979. However, even with high-spectral resolution, the ability to resolve spatial detail using colored light is below that of spatial resolution involving achromatic patterns (Potier et al., 2018). ...
... Although particular colors may have salience for particular species in the mediation of specific behaviors (Endler et al., 2005(Endler et al., , 2014, acuity for colored patterns has been shown to be significantly lower than for black and white patterns. This has been demonstrated recently in Budgerigars Melopsittacus undulatus (Lind and Kelber, 2011) and in Harris's Hawks Parabuteo unicinctus (Potier et al., 2018). Given the phylogenetic distance between these species and their marked differences in ecology, lower acuity for chromatic stimuli is likely to be a feature of the vision of all bird species, probably a feature of all visual systems. ...
The basic anatomy and physiology of bird eyes are well understood. Photoreceptor types and photopigments show little variation across species. However, the distributions of photoreceptors across the retina, and of the ganglion cells to which they connect, exhibit marked interspecific, and even interindividual, variation. There are also interspecific variations in optical systems, and in the placement of eyes in the skull. These variations give rise to significant differences in visual capacity across species. Quantified differences in visual capacity include spatial resolution, contrast sensitivity, and the topography of visual fields. These differences have been interpreted as the result of evolutionary fine-tuning of visual capacities to meet the perceptual challenges associated with gaining information for the control of visually guided tasks in different environments. The dominant tasks appear to be the control of bill or feet position, especially during foraging, and the detection of predators; tasks which make competing demands on visual capacity.
... While colour may appear attractive or salient to human observers, colour is detectable only at higher (daytime) light levels [3]. In addition, spatial resolution to chromatic patterns is always lower than to achromatic patterns [31,32]. This means that even under high light levels, a chromatic pattern will become detectable at a closer distance than the same pattern rendered achromatically. ...
Full-text available
The design of bird diverters should be based upon the perception of birds, not the perception of humans, but until now it is human vision that has guided diverter design. Aspects of bird vision pertinent to diverter design are reviewed. These are applied in an example that uses Canada Geese Branta canadensis as a putative worst-case example of a collision-prone species. The proposed design uses an achromatic checkerboard pattern of high contrast whose elements match the low spatial resolution of these birds when they are active under twilight light levels. The detectability of the device will be increased by movement, and this is best achieved with a device that rotates on its own axis driven by the wind. The recommended spacing of diverters along a power line is based upon the maximum width of the bird’s binocular field and the linear distance that it subtends at a distance sufficient to allow a bird to alter its flight path before possible impact. Given the worst-case nature of this example, other bird species should detect and avoid such a device. The basic design can be modified for use with specific target species if sufficient is known about their vision. Field trials of devices based on these design criteria are now required.
... The motion capture system was turned on at least 1 hour before the start of the experiments and was calibrated shortly before the first session (Vicon Active Calibration Wand), using Vicon Nexus 2 software for data acquisition. The motion capture cameras were set to record at 120 or 200 Hz under stroboscopic 850-nm infrared illumination, well outside the visible spectrum of these birds 46 , and a set of four high-definition video cameras (Vicon Vue) recorded synchronized reference video at 120 or 100 Hz, respectively. Each hawk was fitted with a rigid marker template comprising four 6.4-mm-diameter spherical retroreflective markers (Fig. 1) worn on a falconry backpack secured by a pair of Teflon ribbons (TrackPack Mounting System, Marshall Radio Telemetry). ...
Full-text available
Perching at speed is among the most demanding flight behaviours that birds perform1,2 and is beyond the capability of most autonomous vehicles. Smaller birds may touch down by hovering3–8, but larger birds typically swoop up to perch1,2—presumably because the adverse scaling of their power margin prohibits hovering⁹ and because swooping upwards transfers kinetic to potential energy before collision1,2,10. Perching demands precise control of velocity and pose11–14, particularly in larger birds for which scale effects make collisions especially hazardous6,15. However, whereas cruising behaviours such as migration and commuting typically minimize the cost of transport or time of flight¹⁶, the optimization of such unsteady flight manoeuvres remains largely unexplored7,17. Here we show that the swooping trajectories of perching Harris’ hawks (Parabuteo unicinctus) minimize neither time nor energy alone, but rather minimize the distance flown after stalling. By combining motion capture data from 1,576 flights with flight dynamics modelling, we find that the birds’ choice of where to transition from powered dive to unpowered climb minimizes the distance over which high lift coefficients are required. Time and energy are therefore invested to provide the control authority needed to glide safely to the perch, rather than being minimized directly as in technical implementations of autonomous perching under nonlinear feedback control¹² and deep reinforcement learning18,19. Naive birds learn this behaviour on the fly, so our findings suggest a heuristic principle that could guide reinforcement learning of autonomous perching.
... Aside from predicting colour appearance the SBL model highlights comparatively unexplored trade-offs in visual systems, with contrast sensitivity potentially linked to dynamic range and to other factors such as low-light vision and temporal acuity. For example, birds have poor luminance contrast sensitivity, but high temporal acuity consistent with a low neural bandwidth in the SBL model (Potier, Mitkus, and Kelber 2018;Ghim and Hodos 2006;Boström et al. 2016). CC-BY 4.0 International license perpetuity. ...
Full-text available
An object's colour, brightness and pattern are all influenced by its surroundings, and a number of visual phenomena and "illusions" have been discovered that highlight these often dramatic effects. Explanations for these phenomena range from low-level neural mechanisms to high-level processes that incorporate contextual information or prior knowledge. Importantly, few of these phenomena can currently be accounted for when measuring an object's perceived colour. Here we ask to what extent colour appearance is predicted by a model based on the principle of coding efficiency. The model assumes that the image is encoded by noisy spatio-chromatic filters at one octave separations, which are either circularly symmetrical or oriented. Each spatial band's lower threshold is set by the contrast sensitivity function, and the dynamic range of the band is a fixed multiple of this threshold, above which the response saturates. Filter outputs are then reweighted to give equal power in each channel for natural images. We demonstrate that the model fits human behavioural performance in psychophysics experiments, and also primate retinal ganglion responses. Next we systematically test the model's ability to qualitatively predict over 35 brightness and colour phenomena, with almost complete success. This implies that contrary to high-level processing explanations, much of colour appearance is potentially attributable to simple mechanisms evolved for efficient coding of natural images, and is a basis for modelling the vision of humans and other animals.
Full-text available
Throughout their evolution seabirds have not had to contend with the collision risk posed by discrete objects that extend into their flight space above the water surface. However, the recent introduction of offshore wind turbines has significantly increased the potential for collisions. Bird collision risk with Offshore Wind Farm (OWF) turbines is now a major consenting consideration for OWF projects due to potential local population impacts on birds, especially those associated with protected sites. Therefore, the possibility of reducing those risks through a simple mitigation is highly desirable. Key elements for the design of vision-based mitigation measures aimed at reducing the collision of marine birds with wind turbines should be based upon knowledge of the vision of birds, not the vision of humans. May et al. (2020) tested a vision-based wind turbine mitigation measure and reported a modelled 70% reduction in annual turbine-blade collision mortality rate at a terrestrial location in a suite of 19 bird species. The aim of the present proposals is to extend this vision-based mitigation approach and increase its applicability to a broad suite of bird species considered vulnerable to collisions with wind turbines at sea. Key aspects of the vision, behaviour and ecology of marine birds which contribute to their collision risk under a range of natural viewing conditions are reviewed. The same information is then employed to give insights into the requirements of vision-based mitigation measures. We argue that the internal visual contrast of wind turbines should be increased using achromatic patterns applied to blades and pylons. These patterns should reduce the collision vulnerability of marine birds in general and should be effective under a range of visibility conditions determined by natural light levels and weather conditions. The measures should allow birds with different flight speeds and visual acuities to detect turbines sufficiently early to allow alteration of flight direction and avoid collision. The proposed mitigation requires changes to the appearance of wind turbines that can be implemented at the time of manufacture. They do not interfere with statutory requirements already required for the marking of turbines for the benefit of shipping and aircraft.
Full-text available
Bright iridescent colours are widespread in several aquatic and terrestrial animal taxa and are usually involved in intraspecific communication and/or predator avoidance. Camouflage by iridescence may be one strategy to avoid predators when the animal exhibits bright colours that match the brightness of its surroundings. Hence, animal structural colouration may have a “brightness matching” or “counter‐brightness” function when observed against bright or glossy backgrounds. Here, we addressed the role of such counter‐brightness effect of the iridescent wings of the Morpho dragonfly Zenithoptera lanei for avoiding detection. We hypothesized that the bright reflectance of the dragonfly wings is cryptic against the bright water surface and the glossy vegetation where they naturally occur, protecting the dragonfly from visually oriented predators, deceiving prey and signalling to conspecifics when desired. We addressed whether (1) the iridescent colours of Z. lanei wings function as a visual strategy to reduce their wing detectability by brightness matching the background and (2) the detectability of wings against vegetation and water varies according to the observer. For this, we modelled how conspecifics, dipteran prey and predatory birds see the odonate wings against the vegetation of the Neotropical Savannah and against the water surface where the dragonflies perch. Our results suggest that Z. lanei dragonflies can avoid detection by predators, prey and conspecifics when perched on their natural habitats (i.e., ponds) against the bright background of the water surface. Here, we add evidence to the multifunctionality of structural colours in animals and the function of iridescence in camouflage. The bright iridescence and ultraviolet reflective nanostructures of Z. lanei wings when coupled with striking behavioural displays may provide a dynamic and safe intraspecific communication channel. Morpho dragonflies exhibit remarkable iridescent wings. Males communicate with females and rivals using wing colour. Moreover, we show that males may use their wings to camouflage against the water surface.
Full-text available
Flight is the most energetically costly activity that animals perform, making its optimisation crucial to evolutionary fitness. Steady flight behaviours like migration and commuting are adapted to minimise cost-of-transport or time-of-flight, but the optimisation of unsteady flight behaviours is largely unexplored. Unsteady manoeuvres are important in attack, evasion, and display, and ubiquitous during take-off and landing. Whereas smaller birds may touchdown slowly by flapping, larger birds swoop upward to perch - presumably because adverse scaling of their power margin prohibits slow flapping flight, and because swooping transfers excess kinetic to potential energy. Landing is especially risky in larger birds and entails reaching the perch with appropriate velocity and pose, but it is unknown how this challenging behaviour is optimised. Here we show that Harris' hawks Parabuteo unicinctus minimise neither time nor energy when swooping between perches for food, but instead minimise the gap they must close under hazardous post-stall conditions. By combining high-speed motion capture of 1,592 flights with dynamical modelling and numerical optimization, we found that the birds' choice of where to transition from powered dive to unpowered climb minimised the distance from the perch at which they stalled. Time and energy are therefore invested to maintain the control authority necessary to execute a safe landing, rather than being minimized continuously as they have been in applications of autonomous perching under nonlinear feedback control and deep reinforcement learning. Naïve birds acquire this behaviour through end-to-end learning, so penalizing stall distance using machine learning may provide robustness in autonomous systems.
Full-text available
Research on animal colouration has grown exponentially in the last decade thanks to multidisciplinary approaches. Most studies were focused on trade-offs between communication and mimicry, which represent the two main constraints and drivers of the evolution of body colourations. Reptiles are excellent model species in order to investigate such field of study and lizards in particular show great variability of body colourations and their functions. We studied the lizard Podarcis siculus analysing the variations of dorsal colour of three populations and we obtained clear patterns of seasonal and ontogenetical variation of dorsal colour. According to baseline colour, males were greener and brighter than females, although no difference in saturation was recorded. According to seasonal variations, analyses showed that both sexes significantly vary in colour during the year: males reached higher peaks of hue and saturation later than females during spring; contrastingly, females showed higher peaks of brightness, reached earlier similarly to hue and saturation. Ontogenetic variations were recorded only in males, which become greener, less bright and saturated with growing size. Therefore, our results suggest the occurrence of two opposed strategies in colour expression between sexes: males' dorsal colouration plays a major role in communication, while females are more crypsis-oriented.
Full-text available
Diurnal raptors (birds of the orders Accipitriformes and Falconiformes), renowned for their extraordinarily sharp eyesight, have fascinated humans for centuries. The high visual acuity in some raptor species is possible due to their large eyes, both in relative and absolute terms, and a high density of cone photoreceptors. Some large raptors, such as wedge-tailed eagles and the Old World vultures, have visual acuities twice as high as humans and six times as high as ostriches—the animals with the largest terrestrial eyes. The raptor retina has rods, double cones, and four spectral types of single cones. The highest density of single cones occurs in one or two specialized retinal regions: the foveae, where, at least in some species, rods and double cones are absent. The deep central fovea allows for the highest acuity in the lateral visual field that is probably used for detecting prey from a large distance. Pursuit-hunting raptors have a second, shallower, temporal fovea that allows for sharp vision in the frontal field of view. Scavenging carrion eaters do not possess a temporal fovea that may indicate different needs in foraging behavior. Moreover, pursuit-hunting and scavenging raptors also differ in configuration of visual fields, with a more extensive field of view in scavengers. The eyes of diurnal raptors, unlike those of most other birds, are not very sensitive to ultraviolet light, which is strongly absorbed by their cornea and lens. As a result of the low density of rods, and the narrow and densely packed single cones in the central fovea, the visual performance of diurnal raptors drops dramatically as light levels decrease. These and other visual properties underpin prey detection and pursuit and show how these birds’ vision is adapted to make them successful diurnal predators.
Full-text available
The retinae of many bird species contain a depression with high photoreceptor density known as the fovea. Many species of raptors have two foveae, a deep central fovea and a shallower temporal fovea. Birds have six types of photoreceptors: rods, active in dim light, double cones that are thought to mediate achromatic discrimination, and four types of single cones mediating color vision. To maximize visual acuity, the fovea should only contain photoreceptors contributing to high-resolution vision. Interestingly, it has been suggested that raptors might lack double cones in the fovea. We used transmission electron microscopy and immunohistochemistry to evaluate this claim in five raptor species: the common buzzard (Buteo buteo), the honey buzzard (Pernis apivorus), the Eurasian sparrowhawk (Accipiter nisus), the red kite (Milvus milvus) and the peregrine falcon (Falco peregrinus). We found that all species, except the Eurasian sparrowhawk, lack double cones in the center of the central fovea. The size of the double cone-free zone differed between species. Only the common buzzard had a double cone-free zone in the temporal fovea. In three species, we examined opsin expression in the central fovea and found evidence that rod opsin positive cells were absent and violet-sensitive cone and green-sensitive cone opsin positive cells were present. We conclude that not only double cones, but also single cones may contribute to high-resolution vision in birds, and that raptors may in fact possess high-resolution tetrachromatic vision in the central fovea. This article is protected by copyright. All rights reserved.
Full-text available
Differences in visual capabilities are known to reflect differences in foraging behaviour even among closely related species. Among birds, the foraging of diurnal raptors is assumed to be guided mainly by vision but their foraging tactics include both scavenging upon immobile prey and the aerial pursuit of highly mobile prey. We studied how visual capabilities differ between two diurnal raptor species of similar size; Harris's Hawks Parabuteo unicinctus, which take mobile prey, and Black Kites Milvus migrans, which are primarily carrion eaters. We measured visual acuity, foveal characteristics and visual fields in both species. Visual acuity was determined using a behavioural training technique; foveal characteristics were determined using ultra-high resolution spectral-domain optical coherence tomography (OCT) and visual field parameters were determined using an ophthalmoscopic reflex technique. We found that these two raptors differ in their visual capacities. Harris's Hawks have a visual acuity slightly higher than Black Kites. Among the 5 Harris's Hawks tested, individuals with higher estimated visual acuity made more horizontal head movements before decision. This may reflect an increase in the use of the monocular vision. Harris's Hawks have two foveas (one central and one temporal) while Black Kites have only one central fovea and a temporal area. Black Kites have a wider visual field than Harris's Hawks. This may facilitate the detection of conspecifics when they are scavenging. These differences in the visual capabilities of these two raptors may reflect differences in the perceptual demands of their foraging behaviours.
Full-text available
Vision is essential for birds, but the metabolic demands of retinal processing, and also the costs of carrying large eyes, are likely to impose strong selective pressures to optimize performance. This chapter describes how birds acquire visual information, and in particular general principles in physiological optics, and image coding by the photoreceptors. Birds are compared to other animal groups such as insects and primates, while the ways in which eyes differ between birds are related to their visual ecology. Of particular relevance are the light level at which a species is active, how the bird forages and captures its food, and whether it is aquatic. The main topics discussed are as follows: physiological optics, accommodation, visual fields, photoreceptor spectral sensitivities and the function of colored oil droplets, and the way in which signals from the different types of photoreceptor are used in visual behavior.
Many animals use vision to detect, discriminate, or recognize important objects such as prey, predators, homes, or mates. These objects may differ in color and brightness—having chromatic and achromatic contrast to the background or to other objects. Visual models are powerful tools to investigate contrast detection, but need to be calibrated by experimental data to provide robust predictions. The most critical parameter of current models—receptor noise—is usually estimated from a small number of behavioral tests on chromatic contrast thresholds, while equivalent tests of achromatic thresholds in a wide range of animals have often been ignored. We suggest that both chromatic and achromatic contrasts in studies of visual ecology should be examined using calibrated model parameters, and we provide a compilation of what is currently known on visual thresholds and corresponding noise estimates. Besides the need for careful parameter estimation, we discuss how the robustness of model predictions depends on assumptions about overall light intensity, background color and brightness, object size, and behavioral context.
Birds with larger eyes are predicted to have higher spatial resolution because of their larger retinal image. Raptors are well known for their acute vision, mediated by their deep central fovea. Because foraging strategies may demand specific visual adaptations, eye size and fovea may differ between species with different foraging ecology. We tested whether predators (actively hunting mobile prey) and carrion eaters (eating dead prey) from the order Accipitriformes differ in eye size, foveal depth, and retinal thickness using spectral domain optical coherence tomography and comparative phylogenetic methods. We found that (1) all studied predators (except one) had a central and a temporal fovea, but all carrion eaters had only the central fovea; (2) eye size scaled with body mass both in predators and carrion eaters; (3) predators had larger eyes relative to body mass and a thicker retina at the edge of the fovea than carrion eaters, but there was no difference in the depth of the central fovea between the groups. Finally, we found that (4) larger eyes generally had a deeper central fovea. These results suggest that the visual system of raptors within the order Accipitriformes may be highly adapted to the foraging strategy, except for the foveal depth, which seems mostly dependent upon the eye size.
Inferences about mechanisms at one particular stage of a visual pathway may be made from psychophysical thresholds only if the noise at the stage in question dominates that in the others. Spectral sensitivities, measured under bright conditions, for di-, tri-, and tetrachromatic eyes from a range of animals can be modelled by assuming that thresholds are set by colour opponency mechanisms whose performance is limited by photoreceptor noise, the achromatic signal being disregarded, Noise in the opponency channels themselves is therefore not statistically independent, and it is not possible to infer anything more about the channels from psychophysical thresholds. As well as giving insight into mechanisms of vision, the model predicts the performance of colour vision in animals where physiological and anatomical data on the eye are available, but there are no direct measurements of perceptual thresholds. The model, therefore, is widely applicable to comparative studies of eye design and visual ecology.
AlSTCT.--Based upon previous reports of high visual acuity in falcons, we hypothesized that prey activity influenced prey selection by American kestrels (Falco sparverius) more than prey size. Wild, free- ranging kestrels were simultaneously offered one adult (22-30 g, 3.5-4.0 cm in length) and one juvenile (6-12 g, 2.0-2.5 cm in length) brown laboratory mouse (Mus musculus). Mice were presented to kestrels on a 1 x 1 m board with a light-green background marked into 10 x 10 cm squares. To prevent escape, each mouse was tethered to a clear strand of monofilament fishing line. Mouse activity was documented by observing the mice through 8 x binoculars and recording the behavior of each mouse into a portable cassette recorder. In trials pairing active mice (large or small) with inactive (dead) mice (large or small), kestrels selected active mice 90% of the time. Kestrels also selected the more active of two mice significantly (regardless of size) in trials which we reduced the activity of one mouse, or in trials which one mouse was naturally less active than the other. These results suggest that within the range of prey sizes used in this study, kestrels select prey on the basis of activity, and exhibit little size discrimination in prey choice decisions.