BIRD SENSES
Tim Birkhead
INSTANT
EXPERT
34
Left or right eyed?
Bird vision varies depending
on the position of their eyes
Binocular
vision
Forward-facing Monocular
vision
eyes, eg owl
Blind
area
An eye on
either side of
the head, eg
blackbird, robin
Les Stocker/SuperStock
ui De Roy/naturepl.com
than about 20 centimetres across. This is
sufficient to allow them to find their
nesting and roosting ledges in the totally
dark caves they inhabit.
Nagel was wrong to think that
humans cannot imagine what it feels like
to echolocate. Blind people use both
passive and active echolocation to find
their way about, evinced most
spectacularly by blind kids who go
mountain biking. Interestingly, the clicks
they use to navigate safely on two wheels
are low-pitched, at about 2 kilohertz –
not dissimilar from those of the oilbird.
I am not blind, but over an eight-month
period, while writing Bird Sense, I
trained myself to echolocate and was
impressed by my own abilities.
Oilbirds can see in pitch
darkness by using clicks
to echolocate
ii | NewScientist | 3 August 2013
Different ways of seeing
Eyes on either
side and high up,
eg woodcock, duck
Seeing with sound
Although oilbirds and swiftlets are not related, they
have something extraordinary in common – both can
echolocate. Unlike bats, they utter audible clicks, but
the principle is the same: they use sound waves that
bounce back off objects to “see” in the dark. Lowfrequency sounds are less effective for echolocation
than the high-pitched calls of bats, but tests with
oilbirds show that they are able to avoid objects larger
What does it feel like to be another species? In 1974, philosopher
Thomas Nagel argued in his paper “What is it like to be a bat?” that we
can never truly know. He chose the bat because it is a mammal, like
us, yet has the ability to echolocate – a sense he believed we would
find impossible to imagine. Nagel was unduly pessimistic. Four
decades on, we can now build remarkably comprehensive pictures of
how other animals perceive the world. Birds are further removed
from us than bats, and although we cannot know exactly what it is
like to be one, we have learned enough about their senses to get a
fair idea. Their vision is particularly well understood. So, how does a
bird see the world?
below: Frans Lanting/Corbis left: Susie Cushner/The Image Bank/Getty
A chick’s eyes
become specialised
for different tasks
before it hatches
The brains of vertebrates have two
hemispheres, along with an
arrangement of nerves that means
information from the right side of the
body is processed in the left hemisphere,
and vice versa. In addition, certain
cognitive functions are located in one or
other hemisphere. Our ability to speak,
for example, is controlled by Broca’s
region in the left side of the brain. Body
and brain sidedness, or lateralisation,
was once thought unique to humans, but
in the 1970s it was discovered that
canaries use only the left side of their
brain to control song production.
We now know that birds’ brains are
more lateralised than our own.
Intriguingly, in birds with eyes located on
the sides of their head, this extends to
using the left and right eyes for different
tasks (Brain Research Bulletin, vol 76,
p 235). In day-old chickens, for example,
the right eye tends to be used for finding
food while the left scans for predators.
You might imagine this difference to be
hard-wired – genetic – but it isn’t. Just
before a chick hatches, it has its right eye
facing outwards, which means it
receives some light through the shell.
The left, inward-facing eye gets no light.
However, if you gently turn the chick’s
head in the shell so that the left eye gets
most light, lateralisation is reversed.
Fernando Trabanco Fotografía/Flickr/Getty
”In day-old chicks, the
right eye is used for
finding food while the
left scans for predators”
A BIRD’S EYE VIEW
A raptor's acute vision is
partly down to having
two focal points within
each eye. These allow it
to both enlarge distant
objects and focus on
close-up ones
Eyes high up on the head
let a woodcock see
nearly all around itself
It is often said that the reason we identify with birds
is because, like them, we are bipedal, basically
monogamous and have a sensory system heavily
dependent on vision. Birds have big eyes, and vision
dominates our perception of what it is like to be a
bird. Despite a superficial similarity, however, most
birds see the world in different ways to humans.
For a start, different bird species have three
types of visual field, depending on the position of
their eyes (see diagram, left). Those with eyes on
the side of the head – blackbirds, robins and the
like – have good lateral vision and some forward
vision, but cannot see behind them. Birds with their
eyes located high on the sides of the head, such as
ducks and woodcock, also have good lateral vision –
they may actually see two separate lateral images –
and can see behind them, but not the tip of their
own bill. Owls, with forward-facing eyes, have
binocular vision as we do, not because
this is especially important to them
but because there is nowhere else to
place their huge night-vision eyes.
Avian and human vision differs in
other ways, too. Some birds, including
European blue tits, budgerigars and
zebra finches, can see ultraviolet,
which we cannot. Others, especially
raptors – hawks, falcons and eagles –
can see to distances far greater than
we can. One reason for this is that the
light-sensitive layer at the back of our
eyes, the retina, has one fovea, a
sensitive spot where the image is
sharpest. Raptors, in contrast, have
two foveae in each eye, which is
equivalent to a camera having both
a telephoto and a macro lens (see
diagram, left). Other birds, including
seabirds such as shearwaters, have
a fovea running in a strip across the
retina, possibly allowing them to keep
the horizon horizontal.
“A wing guided by an eye” is how
the ophthalmologist André RochonDuvigneaud characterised birds in his
handbook on vertebrate vision in
1943. Vision is certainly important for
most birds – the nocturnal kiwi is the
exception – but their other senses are
also important, as we will see.
3 August 2013 | NewScientist | iii
THE MECHANICAL SENSES
On the face of it, studying the hearing or tactile sensitivity of
birds looks unlikely to yield benefits for humans. Yet discoveries
about bird hearing could hold clues to treating deafness and
neurodegenerative diseases. And as we learn more about a
bird’s sense of touch, who knows what practical applications it
may inspire.
Sounds familiar
Extraordinary ears
background: Tom Samuelson/Caters News above: J. M. Labat/ardea.com
Dabbling with touch
There are few bird behaviours that seem more
banal than a duck dabbling in muddy water.
Familiarity breeds contempt. In fact, the sensory
processes going on inside a duck’s bill almost
defy belief.
At the tip of the beak is a semicircular
arrangement of tiny pits, visible to the eye, each
housing a receptor whose end protrudes just
above the surface. Within each one, and stretching
back inside the bill, lies a tubular structure a few
millimetres long containing a blood vessel and two
types of nerve endings called Grandry and Herbst
corpuscles. These are touch receptors. A nerve
fibre from each corpuscle joins the major nerves
running along the upper and lower jaw, eventually
connecting to the brain.
It is these two types of corpuscle – in
combination with taste receptors inside the mouth
(see page vii) – that allow ducks to distinguish
between what is edible and what is not. This is
a sophisticated process, and the sensitivity of
a duck’s bill tip may rival that of our fingertips.
iv | NewScientist | 3 August 2013
Besides ducks, many birds have touch
receptors in their bill tips. They are
especially abundant and well developed
in birds such as kiwis and waders, which
probe for hidden food. Birds probing
in wet sand, for example, can set up a
pressure wave whose shape enables
them to detect edible bivalves
(Proceedings of the Royal Society B,
vol 265, p 1377).
As well as being crucial in foraging,
touch plays an important role in birds’
social relationships. Many spend hours
preening each other – equivalent to the
social grooming of primates. Such
contact between individuals must be
felt via touch receptors in the skin, or
possibly through the modified sensory
feathers called filoplumes. Presumably,
as with primate grooming, preening
triggers the release of feel-good
chemicals that promote bonding.
Acute hearing allows
a great grey owl to
pinpoint a mouse, even
beneath the snow
The ability of owls to function in the dark is
legendary, but exaggerated. Although they have
good vision in low light, in total darkness they
cannot see at all. What owls do excel at is hearing,
which is of course useful at any time.
The ears of several owl species – not to be
confused with their feathery “ear” tufts – are
positioned asymmetrically on and in the skull
(see diagram, right). In the great grey owl, for
example, the left ear is located at 7 o’clock, the
right at 2 o’clock. This asymmetry results either
in a sound reaching the two ears at slightly
different times, or in minute differences in
volume, allowing the owl to pinpoint its source.
Great greys – among the largest of all owls – are
daytime hunters. Using their acute hearing, they
can locate rodents beneath the snow, then power
through the surface with pinpoint precision to
grasp their prey.
Some owls have asymmetric
ears, allowing them to
pinpoint a sound source with
great precision
Given the extent to which birds rely on
vocalisation and how much effort has
gone into the study of their calls and
songs, it is remarkable how little we
still know about their hearing. I wonder
whether this lack of interest is partly a
consequence of birds having no external
ear or pinna, which is part of their
reptilian heritage.
We know that birds can hear an
almost identical range of sounds to us.
They achieve this with a single middle
ear bone, rather than the three we
have – again a product of their reptilian
ancestry. Intriguingly, the hearing
ability of birds living in temperate
climes fluctuates through the year.
The auditory regions of their brains grow
during the breeding season, then shrink
when song becomes less important.
Understanding this process could
provide clues to treating Alzheimer’s
and other neurodegenerative diseases.
Another important difference
between bird and human hearing occurs
in the inner ear, and especially in the
cochlea – the structure containing the
vibration-sensitive “hearing” hairs. It is
snail-shaped in humans, hence its name,
whereas in birds it is banana-shaped.
In both, the hair cells detect changes
in pressure and transform these into
electrical signals, which are interpreted
as sound in the brain. Crucially, we
cannot replace damaged hair cells,
making deafness a scourge in older
people. Birds, have no such problem:
they can grow new hair cells. If we can
discover the genetic basis underpinning
this difference, it could give us the
potential to solve a common cause
of age-related hearing loss.
3 August 2013 | NewScientist | v
Elusive smell
The navigation abilities of many birds seem almost
miraculous. Release a Manx shearwater, a seabird
that rarely crosses land, from a church tower in Venice,
and it will unerringly find its way back to its breeding
burrow on the island of Skokholm off the west coast
of Britain. How? And what about barn swallows and
the many other species that commute, summer
and winter, between the northern and southern
hemisphere – how do they navigate? Such questions
have preoccupied researchers for well over a century.
Today we know that birds have a variety of
navigational mechanisms, including sun and star
compasses and olfactory cues. The most recently
discovered, and most mysterious, is the ability to
sense the Earth’s magnetic field. It was once
considered impossible, but in the 1980s suspicion
began to grow that birds do indeed possess this sixth
sense. We still do not know exactly how it works,
but what we do know is mind-bogglingly bizarre.
First, birds seem to detect the direction of the
magnetic field using microscopic crystals of
magnetite – a magnetic form of iron oxide – located
around their eyes and in the nasal cavity of the upper
beak. More recently, it has emerged that they may
also detect the strength of the field via a chemical
reaction – physicists have known since the 1970s
that certain chemical reactions can be modified by
magnetic fields. Stranger yet, studies of the European
robin indicate that the reaction involved is induced
by light entering the bird’s right eye only (Journal
of Comparative Physiology A, vol 191, p 675).
Researchers are currently striving to find out where
in the body the reaction takes place. Meanwhile,
some speculate that it might allow birds to “see” the
contours of the Earth’s magnetic field – something
that is difficult to envisage as a mere human.
Ornithologists long believed that birds lack a sense of
smell. This prejudice seemed to be confirmed in the
early 1900s by poor research designed to “prove” its
absence. One such study, published in Nature no less,
involved offering a single turkey two plates of food,
one placed on top of some smelly substance such as
lavender oil, the other free from additional smells.
The turkey promptly ate the lot, then downed a third
helping contaminated with malodorous prussic acid,
and died. Conclusion: birds have no sense of smell.
So the myth persisted, despite contradictory
evidence from earlier anatomical studies. In 1837, for
example, British biologist Richard Owen’s dissection of
a turkey vulture had led him to conclude that it had a
“well-developed organ of smell”. Similarly, he found
evidence for large olfactory bulbs in the brain of the
recently discovered kiwi. Later observations of wild
kiwis snuffling around in the undergrowth at night in
search of earthworms left little doubt they use their
sense of smell to forage. But kiwis are so unlike other
birds that it was easy to dismiss them as an exception.
Then, in the 1960s, work by Betsy Bang at Johns
”Birds have
a variety of
navigational
mechanisms,
including star
compasses and
olfactory cues”
Hopkins University in Baltimore,
Maryland, transformed ideas about
avian olfaction. She found the nasal
conchae – structures within the nose,
which in humans warm incoming air
and detect odours – to be large and
elaborate in some birds. Convinced
that birds must be able to smell, she
turned her attention to the olfactory
bulb. She found it differed in relative
size between species by a factor of 12,
reflecting the extent to which their
lifestyle depended on olfaction (see
table, below right).
Today, attitudes have changed so
dramatically that one recent study
described albatrosses and petrels as
living in an “olfactory seascape”, using
their refined sense of smell to find
food, breeding colonies and even
their nesting burrow and partner
(PNAS, vol 105, p 4576).
MYSTERIOUS AND MORE MYSTERIOUS
With their hard beaks and expressionless faces, birds do not appear
to respond to a delicious flavour or a bad odour as we do. This may
partly explain why ornithologists have been slow to attribute taste
and smell to them. We still know so little that there is huge potential
for discovery here. But for now, it is another little-known sense – the
mysterious ability to detect the Earth’s magnetic field – that excites
most interest among researchers.
A matter of taste
Dogs often swallow their food so rapidly it seems they
barely have time to taste anything, but as every dog
owner knows, they are certainly not indifferent to
taste. The same is true of birds.
Early evidence of a sophisticated gustatory sense in
birds was found by John Weir, a bird-keeping colleague
of Charles Darwin and Alfred Wallace. He noticed that,
when given caterpillars of the ermine moth, his cage
birds spat them out and shook their heads in disgust.
At the time, though, Weir’s discovery of a sense of
taste in birds was rather eclipsed by Wallace’s
realisation that distasteful caterpillars often sport
warning colours, and that the two traits evolved
together as a signal to would-be predators.
Later investigators assumed that, like us, birds
must have taste buds on the tongue. When they
looked for these they found a puzzle, because they
seemed to have too few to discriminate between
palatable and distasteful foods. Then, in 1974,
Herman Berkhoudt at the University of Leiden in
the Netherlands discovered what looked like a taste
bud in the tip of a duck’s beak. His painstaking
microscopic examinations eventually revealed that
a mallard’s taste buds are located in five clusters,
four in the upper jaw and one in the lower, with
none on the tongue. Although birds have far fewer
taste buds than mammals – humans have some
10,000 while mallards have about 400 – they can
nevertheless taste salt, sour, bitter and sweet,
as we do. Whether they also respond to umami
has not been tested.
The length of a bird's olfactory bulb relative
to the whole brain was first
measured in the late 1960s
and found to correlate
with reliance on their
sense of smell
Migratory birds such as
barn swallows may be
able to “see” the Earth’s
magnetic field
Robert Norbury/Millennium above: Biosphoto/SuperStock
Bob Croslin
A sixth sense
37% Snow petrel
34% Kiwi
29% Turkey vulture
20% Feral pigeon
16% Shorebirds
15% Domestic fowl
10% Songbirds
3 August 2013 | NewScientist | vii
Tim Birkhead
Tim Birkhead is a professor at
the University of Sheffield, UK,
where he teaches animal
behaviour and the history of
science. He is a Fellow of the
Royal Society of London and his
research has taken him all over
the world in the quest to
understand the lives of birds.
Next
INSTANT
EXPERT
Jon Butterworth
The Higgs
Boson
7 September
So much to discover
Of all the senses, the area I consider
most fascinating is that of emotions.
Do birds have emotions? Do they
sense pain and pleasure? Some have
argued that non-humans cannot
experience such emotions as we
do because they do not possess
consciousness. This is a thorny issue,
not least because consciousness is
ill defined and extremely difficult to
measure in any objective, scientific
way. Nevertheless, there is now some
evidence that birds do have emotions.
Many, for example, maintain
long-term pair bonds, and there
are several anecdotal accounts of
separated partners being reunited
after a long period of absence,
accompanied by behaviours – such
as protracted greeting displays – that
certainly imply they have an
emotional bond.
Studying the emotional lives of
birds may seem like an academic
indulgence, but the point about
pure research is that one can never
anticipate how it might eventually be
useful. We have already seen how the
ability of birds to regenerate hair cells
in the inner ear provides the potential
to conquer certain forms of human
deafness. In general, the lack of
information on bird senses means
viii | NewScientist | 3 August 2013
that this is an area of huge
opportunities, ripe for exploration.
Our understanding of the sense of
smell in small birds is almost
negligible, for example, yet by using
fMRI to observe brain activity, we
could potentially screen dozens of
species in a relatively short time to
see whether and how much they
respond to different odours. fMRI and
other new technologies look set to
change the way we think about the
senses – and not just those of birds.
We are obsessed by our own
senses, but understanding them
is a challenge. Looking at those of
other animals may provide insights.
Increasingly, biologists interested in
the behaviour of animals in the wild
look to the anatomy and physiology
behind behaviours and how these are
connected. It is the combination of
whole animal biology, evolutionary
thinking and sensory biology that will
open up new areas of knowledge.
That makes birds the perfect research
subjects, since we already know so
much about their natural behaviour.
In September 2014, the Royal
Society will host a meeting on the
sensory biology of birds, an indication
that this is at last becoming a hot
topic for research.
recommended READING
Bird Sense by Tim Birkhead
(Bloomsbury, 2012)
“What Is It Like to Be a Bat?” by T. Nagel,
The Philosophical Review, vol 83, p 435
“Through animal eyes: what behaviour
tells us” by M. S. Dawkins, Applied
Animal Behaviour Science, vol 100, p 4
“Structure and function of avian taste
receptors” by H. Berkhoudt, in Form
and Function in Birds, vol 3 (Academic
Press, 1985)
“Avian olfactory receptor gene
repertoires: evidence for a welldeveloped sense of smell in birds?”
by S. Steiger et al., Proceedings of the
Royal Society B, vol 275, p 2309
“The magnetic retina: light-dependent
and trigeminal magnetoreception in
migratory birds” by H. Mouritsen and P. J.
Horer, Current Opinion in Neurobiology,
vol 22, p 343
“An integrative and functional
framework for the study of animal
emotion and mood” by M. Mendl et al.,
Proceedings of the Royal Society B,
vol 277, p 2895
Cover image
Les Stocker/Oxford Scientific/Getty