Vision - Birds, with the possible exception of diurnal
primates
(e.g., humans), are the vertebrates which may rely most heavily on
vision
to function in their environment. The most obvious visually-dependent
behavior
of birds is flight, but birds also exhibit an impressive range of
visually-guided behaviors other than flight, e.g., foraging, predator detection,
& mate choice.
Swamp Harrier (Circus approximans)
The avian eye is large relative to the size of the head &
brain. For example, human eyes make up about 1% of the total mass of
the
head; European Starlings eyes make up about 15% of the mass of their
head.
The advantage: large eyes provide larger & sharper images. Birds
also
have 3 eyelids; one upper and one lower eyelid plus a nictitating
membrane.
This nictitating membrane is between the other two eyelids and the
cornea
and has its own lubricating duct equivalent to our tear duct.
Bird vision
The nictitating membrane, or third eyelid, is unique to vertebrates,although not found in all groups. In many species, it representsthe principal mechanism of ocular cleansing. In birds, the
externaleyelids possess smooth muscle, and may close only
during sleep.The nictitans, on the other hand, is operated
by two striatedmuscles and is capable of extremely rapid
sweeps across theocular surface to clear the cornea of debris. Ocular surfacelubrication originates from two secretory glands. The lacrimalgland is situated in the inferior temporal quadrant associatedwith the more active lower eyelid, although in many speciesthis
gland is absent or rudimentary. Additionally, most birds,especially
cormorants and falcons, have a second secretory glandcalled
a Harderian gland located in the posterior and nasalaspect
of the orbit associated with base of the nictitatingmembrane.
In falcons, this secretory gland produces a viscoussolution
to moisten the cornea during the breathtaking stoopsthat
are the falcon’s trademark. Although the compositionof
these secretions is not known, a compound such as hyaluronicacid
would moisten the surface without the rapid evaporationseen
with a more dilute tear film. Such a coating would maintaina
smooth surface, but might pose other difficulties by collectingdebris
(Schwab and Maggs 2004).
Check out this White-eyed Buzzard's nictitating membrane
The nictitating membrane of many such birds has a cartilaginous-likeconnective tissue fold along the leading edge of the membranecalled
the marginal plait (photomicrograph to the right). With each blink this
flange-likeflap collects the tear film and any associated
debristo drain through the enlarged puncta (openings that act like little valves to take tears out
of the eye) into the nasolacrimal system.It is
probably aided in this corneal cleansing role by a layerof
"feather epithelium." This remarkable adaptation of a surfaceepithelium
is believed to be unique to the epithelium liningthe
nictitans of many birds and reptiles. Long microvilli withclub-like
termini and numerous secondary projections from theirlong
axis extend from the apical membrane of epithelial cellslining
the bulbar surface of the third eyelid. Those of Peregrine Falcons
(above) are extremely robust andlikely form a
"histological feather duster" that sweeps thecornea clean
with each darting excursion of the clear nictitans (Schwab and Maggs
2004).
Some authors have suggested that in certain aquatic birds a transparent nictitating membrane of high refractive index could compensate for the refractive loss of the cornea in water. However, measurements of refractive indices, refractive state and curvature for several aquatic birds have revealede that the nictitating membrane does not have a refractive function; the refractive indices of the cornea and nictitating membrane are very similar, the nictitating membrane does not alter the refractive state of the eye, and its curvature, when it is in place in front of the globe, is virtually the same as that of the cornea (Sivak et al. 1978).
Birds can safely and accurately fly through narrow passages between objects, e.g., in dense forests or other cluttered habitats, by balancing optic flow. In other words, as they (or, for example, humans in a vehicle!) move forward, objects that are closer seem to travel faster than objects that are further away. By insuring that nearby objects on either side are moving at similar speeds, birds can fly mid-way between, and avoid, those objects. On the left side of this figure, both walls had vertical stripes that provided 'strong' motion cues (or strong optic flow); on the right, the wall on the bird's right had horizontal stripes, providing weak motion cues (or weak optic flow), whereas the wall on the bird's left had vertical stripes and provided strong motion cues (or strong optic flow). When birds have strong motion cues on each side, they can balance optic flow and fly mid-way between objects (or walls). When birds lack strong motion cues, they are unable to balance optic flow and may inadvertently fly too close to the object (or wall) providing weak motion cues (as on the right side of this figure) (Figure source: Bhagavatula et al. 2011).
Safely negotiating narrow passages -- Although considerable effort has been devoted to investigating how birds migrate over large distances, surprisingly little is known about how they tackle so successfully the moment-to-moment challenges of rapid flight through cluttered environments. It has been suggested that birds detect and avoid obstacles and control landing maneuvers by using cues derived from the image motion that is generated in the eyes during flight. Bhagavatula et al. (2011) investigated the ability of Budgerigars to fly through narrow passages in a collision-free manner by filming their trajectories during flight in a corridor where the walls were decorated with various visual patterns. Their results demonstrate that birds negotiate narrow gaps safely by balancing the speeds of image motion that are experienced by the two eyes and that the speed of flight is regulated by monitoring the speed of image motion that is experienced by the two eyes. These findings have close parallels with those previously reported for flying insects, suggesting that some principles of visual guidance may be shared by all diurnal, flying animals.
Eye size, brain size, prey capture and
nocturnality
-- Behavioral adaptation to ecological conditions can lead to brain
size
evolution. Structures involved in behavioural visual information
processing
are expected to coevolve with enlargement of the brain. Because birds
are
mainly vision-oriented animals, Garamszegi et al. (2002) tested the
predictions
that adaptation to different foraging constraints can result in eye
size
evolution, and that species with large eyes have evolved large brains
to
cope with the increased amount of visual input. Using a comparative
approach,
Garamszegi et al. (2002) investigated the relationship between eye size
and brain size, and the effect of prey capture technique and
nocturnality
on these traits. After controlling for allometric effects, they found a
significant, positive correlation between relative brain size and
relative
eye size. Variation in relative eye and brain size were significantly
and
positively related to prey capture technique and nocturnality. These
findings
suggest that relative eye size and brain size have coevolved in birds
in
response to nocturnal activity and, at least partly, to capture of
mobile
prey.
Structure of the avian eye:
characteristic shape, with front & back sections being
spheres of
unequal
radii. Eye shapes varies among birds, ranging from globose or flattened
(most diurnal birds; below) to tubular (owls; also shown below)
light entering the eye is refracted by the cornea & lens and
strikes
the retina where the sensory cells (the cells that convert light into
nervous
impulses) are located
(A) Cross section
through the eye of an owl showing the cornea and lens
that projects images onto the retina. (B) Variation in the placement of eyes in the skull
of birds shown by cross sections through the head of an owl and of a
small songbird (Figure from Martin 2017).
Owls have tubular eyes with little extraocular musculature, to maximize the size of the eyes.
To compensate, most owls can turn their heads with great speed, nearly 270° atop a thin,
lightweight spinal column; so quickly that myths of complete 360° cranial revolution have
sprung up adding to the mythology of owls. As can be seen in the cranial slice taken at the
midline of the cornea above the upper mandible, the eyes of Eastern Screech-Owls are large, both
on an absolute and relative basis. They are frontally placed, providing as much binocular stereopsis
as possible, as is typical for avian predators. The stereoscopic binocular visual field is approximately 60-70°,
although the visual field is larger. The eyes together outweigh the brain as often occurs in
raptorial species, especially the nocturnal owls (British Journal of Opthamology, Sept. 2000 issue).
Tubular eye of an owl ( Bayon et al. 2007)
How owls rotate their heads 270 degrees without damaging arteries
Rings of bony plates surrounding the iris of the eye
are present in most birds. On the left is a drawing of the
arrangement of the plates in an albatross eye showing
how the ossicles shape the junction between the cornea and the sclera.
To the right is the skull of an eagle showing the
positioning
of the ossicles within the orbit. The primary purpose of the
ossicles appears to be to reinforce the corneal scleral
junction. In birds, the ossicles allow the animals to adjust the shape
of the
cornea during accommodation (Rowe 2000).
some nocturnal
birds (goatsuckers; Caprimulgiformes) have a layer at the back of the
eye called the tapetum lucidum (literally 'bright carpet') that acts as
a mirror & reflects light back through the retina and, thereby,
makes
it more likely that light will strike sensory cells in the retina. As a
result, birds with a tapetum lucidum can see much better under low
light
conditions. The presence of a tapetum lucidum produces the 'eyeshine'
of
goatsuckers and some mammals.
Retina of a Common Pauraque showing rods (r), cones (c), and tapetum (t) (From: Rojas et al. 2004).
Barred Owl
Visual resolution of Great Cormorants compared with fishes, aquatic mammals and other birds. Each symbol represents the maximal resolution reported for a given species in a given reference. Amphibious diving mammals (solid squares) suffer little or no loss of resolution upon submergence. Cormorant's (solid triangles) visual resolution in air is in the lower range reported for birds, whereas underwater it is within the higher range reported for fishes (circles) and higher than that of diving mammals (From: Strod et al. 2004).
Cormorants stay in focus -- Eyes better adapted for terrestrial vision and emmetropic (in focus) in air tend to be hyperopic (far sighted) underwater, whereas eyes better adapted for aquatic vision are emmetropic in water and tend to be myopic (near sighted) in air. For example, the corneas of some penguins (Sphenisciformes) and albatrosses (Procelariiformes) are relatively flat, with refractive powers lower than those of avian species of comparable eye size. Such corneas suffer relatively little loss of refractive power when submerged. However, several other bird species that are pursuit-divers have strongly curved corneas. These corneas have a high refractive power in air, and, as a result, the lens must compensate for the absence of corneal refraction during dives (Katzir and Howland 2003).
Compared with other bird species, the visual resolution (acuity) of Great Cormorants in air was found to be a bit lower than average, but resolution underwater was comparable to that reported for fishes, pinnipeds (e.g., seals and sea lions) and cetaceans (e.g., killer whales and dolphins). The requirements to perform precise visuo-motor tasks in two optically different media, and the ability to accommodate using their cornea and lens in air and just the lens underwater make the vision of pursuit-diving birds a model of vertebrate capacities at the extreme (Strod et al. 2004).
Accommodation in the eye of a Hooded Merganser (Mergus cucullatus). (Left) Sagittal section of the eye of a Hooded Merganser
without accommodation. (Right) Sagittal section of the eye of a Hooded Merganser stimulated with nicotine sulphate to
approximate accommodation. When accommodating, muscle contraction (Brucke's muscle) forces the ductile lens though the rigid pupil
creating a 'bulge' (called the anterior lenticonus) (From: Schwab 2002).
Schematic drawing of a brain showing the relative
locations of the day-
and night-vision (cluster N) brain regions in night-migrant
songbirds. The thamalofugal and tectofugal visual pathways have been
determined in other bird species. Upper right, the extent of cluster N
seen from the dorsal surface of the brain.
[A, arcopallium; P, pallidum; E, entopallium; St, striatum; N,
nidopallium; M, mesopallium; H, hyperpallium; ICo, intercollicular
complex; v, ventricle; OT, optic tectum; HF, hippocampal formation;
IHA, interstitial region of the hyperpallium apicale (HA); DNH, dorsal
nucleus of the hyperpallium; W, visual Wulst; GLd,
lateral
geniculate nucleus, dorsal part; Rt, nucleus rotundus]
Night-vision brain area in migratory birds -- Twice each year, millions of night-migratory songbirds migrate thousands
of kilometers. To find their way, they must process and
integrate spatiotemporal information from a variety of cues including
the Earth's magnetic field and the night-time starry sky.
Mouritsen et al. (2005) discovered that
night-migratory songbirds possess a tight cluster of
brain regions highly active only during night vision. This
cluster, named "cluster N," is located at the dorsal
surface of the brain and is adjacent to a known visual
pathway. In contrast, neuronal activation of cluster N was
not increased in nonmigratory birds during the night,
and it disappeared in migrants when both eyes were covered.
In night-migratory songbirds cluster N is
apparently involved in enhanced night vision, and could be
integrating vision-mediated magnetic and/or star compass information
for night-time navigation. Why would night-migrants need to evolve a
distinct night-vision system, when all songbirds
can see at night? Night-migrants may require specialized
development of a cerebral system such as cluster N for
seeing better at night and/or for visual night-time
navigation. The navigation signals sensed and the
information processed could be star-light constellations
and/or the Earth's magnetic field. The latter possibility
would be in line with theoretical, molecular , and
behavioral evidence suggesting that the Earth's magnetic
field modulates the light sensitivity of specialized
receptor molecules differently in various parts of the
retina, leading to perception of the magnetic field as visual
patterns. As a consequence, the brain regions ultimately
extracting the reference direction provided by the geomagnetic
field should process and compare purely visual input from
the retina.
Monocular vs. Binocular Vision
The eyes of most birds are on the side of their heads, allowing them
to see objects on each side at the same time (monocular vision). This
provides
birds with a wide field of view, e.g., Rock Doves (pigeons) can see 300
degrees without turning their head and American
Woodcocks can see 360 degrees! With monocular vision, birds may
have
a harder time judging distances and have poorer depth perception. Of
course,
these birds do have a limited field of binocular vision directly in
front
of them (and woodcocks also have a field of binocular vision behind
them).
Other birds, like owls, have their eyes located to the front giving
them
a much wider field of binocular vision. These birds may have a 180
degree
field of overall vision with most of that binocular. See
'The Bird Site - Senses'
The eyes
of most birds are aligned laterally, and each visual axis gives a
lateral, or monocular, view. This lateral visual field serves to
monitor predators and conspecifics, as well as to detect food at some
distance. Most birds also have, in addition to a central fovea, a
second retinal fovea, located in the temporal retina (see Figure below). The cyclopean
area is the combination of the frontal and lateral visual fields.
Visual fields of birds have been categorized
as:
Type 1 (a). Large cyclopean area; largely
monocular vision (e.g. Rock Pigeon Columba livia, Starling Sturnus
vulgaris and Cattle Egret Bubulcus ibis)
Type 2 (b). Very large cyclopean area;
small binocular fields in front and back (e.g. Eurasian Woodcock Scolopax
rusticola)
Type 3 (c). Larger frontal area with large
binocular field (e.g. Tawny Owl Strix aluco).
A
view to a kill: why airborne hunters don't dive straight in
(New
Scientist; 11/25/00) - The mystery of why birds of prey spiral in
towards
their victims may have been solved. They do it to make the most of
their
pin-sharp sideways vision. Vance Tucker of Duke University has long been puzzled by the way birds of
prey
approach their dinner. In studies of Peregrine Falcons, he & his
colleagues
found that the birds almost always follow a curved path once they get
within
1.5 km of their prey (Tucker 2000a). "We had observed these curved paths
for years, and I was racking my brains to explain that," says Tucker.
He
suspected the explanation lay in the birds' vision. Tests have shown
they
see objects in front of them most clearly when they turn their heads
about
40 degrees to one side (i.e, the image falls on the deep fovea; see Figures below). But turning their heads in mid-flight might
increase
the birds' aerodynamic drag, slowing them down. To test this, Tucker
placed
models of Peregrine Falcons and Red-tailed Hawks in a wind tunnel.
Force
sensors showed that, at a wind speed of 42 km per hour, the drag on
birds
whose heads were turned 40 degrees was more than 50% greater than on
those
looking straight ahead. To avoid this, Tucker concludes, the birds keep
their heads straight and follow a path called a logarithmic spiral.
That
way, they can keep one eye fixed on their prey. And while a spiral path
is longer, the speed advantage more than compensates.
Section through a falcon's head at the foveal plane. Both foveae (shallow and deep) & the center of the pupils are on the plane. LOS, line of sight.
|
Relative receptor densities along the foveal plane of a falcon. A relative density of 1 represents 62,000 receptors/square mm [Both figures from Tucker (2000b)].
Two views of the visual fields of Red-tailed Hawks (a, d), Cooper's Hawks (b, e), and American Kestrels (c, f). (a–c) Orthographic projection of the boundaries of the retinal fields of the two eyes, along with projection of the pectens and bill tips. A latitude and longitude coordinate system was used with the equator aligned vertically in the median sagittal plane. The bird's head is imagined to be at the center of the globe (grid is at 20° intervals). (d–f) Horizontal sections through the horizontal plane (90°–270°) showing the visual field configuration of each species. Each chart represents the average retinal visual field when the eyes were at rest.
Raptor visual fields and hunting strategies -- Different strategies to search for and detect prey may place specific demands on sensory modalities. O'Rourke et al. (2010) studied visual field configuration, degree of eye movement, and orbit orientation in three diurnal raptors. Red-tailed Hawks have relatively small binocular areas (~33°) and wide blind areas (~82°), but intermediate degree of eye movement (~5°), which underscores the importance of lateral vision rather than binocular vision to scan for distant prey in open areas. Cooper's Hawks' have relatively wide binocular fields (~36°), small blind areas (~60°), and high degree of eye movement (~8°), which may increase visual coverage and enhance prey detection in closed habitats. Additionally, Cooper's Hawks can visually inspect the items held in the tip of the bill, which may facilitate food handling. American Kestrels have intermediate-sized binocular and lateral areas that may be used in prey detection at different distances through stereopsis and motion parallax; whereas the low degree eye movement (~1°) may help stabilize the image when hovering above prey before an attack. These results indicate that: (a) there are between-species differences in visual field configuration in these diurnal raptors, (b) these differences are consistent with prey searching strategies and degree of visual obstruction in the environment (e.g., open and closed habitats), (c) variations in the degree of eye movement between species appear associated with foraging strategies, and (d) the size of the binocular and blind areas in hawks can vary substantially due to eye movements. Interspecific variation in visual fields and eye movements can influence behavioral strategies when visually searching for and tracking prey.
The avian retina, in contrast to that of mammals, is
avascular
(contains no blood vessels), which prevents shadows & light
scattering.
This 'improvement' is possible because of a uniquely avian structure -
the pecten. This highly vascular structure projects from the
retina
(see diagrams above; for photo on the right: P = pecten, R & Y =
areas
of the retina, & F = fovea) and nutrients & oxygen diffuse from
it, through the vitreous body (see diagram above), to the retinal cells
- the rods and/or cones.
On the left, a goat fundus (or back of the eye) with
retinal blood supply from central
or cilioretinal arteries (same as humans). On the
right,
a screech-owl fundus with no
vessels in the retina.
(Source: www.vetmed.ucdavis.edu/courses/vet_eyes/conotes/con_chapter_12.html)
Localization of globin E (GbE) in the chicken retina. PE, pigment epithelium (above this layer would be the choroid); OS, outer segment of photoreceptors (cones);
IS, inner segment of photoreceptors. On the right, the fluorescing, or 'glowing', area along the OS indicates the presence of GbE (From: Blank et al. 2011).
Oxygen and the avian retina -- Vertebrate eyes require large amounts of energy and, therefore, oxygen. Supplying adequate oxygen to the avian retina is potentially challenging because birds have large eyes and thick retinas with high concentrations of sensory cells (rods and cones), but bird retinas contain no blood vessels. Globin E (GbE) , or eye globin, was recently identified as an eye-specific globin in domestic chickens (Gallus gallus). In addition, globin E genes have been found in Zebra Finches and Wild Turkeys, but appear to be absent in non-avian vertebrates. Blank et al. (2011) found that the photoreceptor cells of the chicken retina have high levels of GbE protein. Because other types of globins, such as hemoglobin, myoglobin, and neuroglobin, help transport and store oxygen in the blood (hemoglobin), muscles (myoglobin), and nervous system (neuroglobin) of vertebrates, it is possible that GbE helps supply photoreceptor cells in the avian eye with oxygen.
The avian retina has three types of photoreceptors that 'translate'
light into nervous impulses:
rods - black & white vision
cones - color vision
double cones - color vision
Five major classes of retinal neurons are also
recognized: photoreceptors,
bipolar cells, horizontal cells, amacrine cells, and
ganglion cells. The photoreceptors
(rods and cones), bipolar cells, and horizontal cells
make synaptic contacts with each other in the outer
retinal layers. The bipolar, amacrine, and ganglion
cells
make contact in the inner retinal layers.
(Source: Husband and Shimizu 2001;
http://www.pigeon.psy.tufts.edu/avc/husband/avc4eye.htm)
Nocturnal birds, like owls, have retinas consisting entirely of
rods,
while the retinas of diurnal birds contain both rods & cones. The
single
cones, as well as one or both segments of double cones, contain oil
droplets (see photo to the lower right of oil droplets in the
retina
of a European Starling)which
consist of lipids in which carotenoid pigments are dissolved
can appear transparent, pale yellow, green, orange, or red
are positioned at the distal end of the inner cone segments,
covering
the
entire width of the receptor. Light passes through the droplet before
entering
the photosensitive outer segment.
These oil droplets:
absorb light below their characteristic wavelength of
transmission
&,
therefore, provide a protective shield against UV light
probably act as lenses that focus light onto the photoreceptor
&
improve
the reception of visual pigments
The transparent or colorless oil droplets found in many birds permit
perception of very short spectral wavelengths (ultraviolet or near
ultraviolet).
Such perception:
serves a signaling function in some species (bird plumage tends
to have
shorter wavelength reflectance than many other natural objects).
is likely used as a cue in discriminating foods (e.g., plants,
seeds,
berries)
or other natural objects.
Evolution of vertebrate UV vision. Circles indicate
extant
organisms, and squares indicate ancestral species.
Black filled symbols indicate UV vision, purple filled
symbols indicate violet vision, and open symbols
indicate absence of UV or violet vision. UV vision is
mediated by visual pigments that absorb light maximally at 360 nm.
Violet (or blue) pigments absorb light maximally from
390–440 nm. The arrow shows the root of the tree and the
common ancestor of vertebrates (Zhang 2003).
Examination of the
phylogenetic distribution of UV and
violet vision across vertebrates suggests that violet vision originated
at least four times, in frogs, birds, primates, and cetartiodactyls (Zhang 2003). In most extant vertebrates, UV vision was directly
inherited
from the vertebrate ancestor, but in birds, it was apparently restored
from violet vision secondarily. Analysis by Odeen and Hastad (2003)
indicates
that UV vision was regained at least four times in birds. Shi and
Yokoyama
(2003) argue that that the presence of UV vision is associated strongly
with the availability of UV light in the environment and with
UV-dependent
behaviors. For example, coelacanths (the so-called "living fossil" that
lives at depths 200 m in the ocean) and dolphins(see Figure above) live
in marine environments where UV light cannot reach.
Given an abundance of UV light in their
environment, why
have so many organisms switched from UV vision to violet vision? Shi
and
Yokoyama (2003) suggest two major reasons. First, UV light, even at 360
nm, can damage retinal tissues. Second, by achieving violet vision,
organisms
can improve visual resolution and subtle contrast detection. On the
other
hand, in the avian lineage, their ancestor lost UV vision, but some of
its descendants regained it (See Figure to the right).
Birds use UV vision in many ways: Kestrels (Falco
tinnunculus) use UV reflection of vole urine, left as scentmarks,
to
locate prey (more details on this below). Blue Tits (Parus caeruleus) use their UV vision to detect camouflaged caterpillars. Female
Bluethroats
(Luscinia svecica) choose mates based on UV coloration of males.
Nestlings in some species advertise their quality to parents via UV
reflectance
of their ‘flanges’ (the rim around the edge of their mouth).
Type of vision system mapped onto phylogenetic
relationship
among avian taxa (phylogeny based on DNA–DNA hybridization analysis;
Sibley
and
Ahlquist 1990).The passeriform families are combined (in bold). White denotes violet sensitive (VS), black indicates ultraviolet
sensitive (UVS), and gray indicates taxa with both systems
(Ödeen and Håstad 2003).
Recent work has revealed that some birds of
prey see
a wider color spectrum than we do, including ultraviolet light. How
might
this be useful? Kestrels (Falco tinnunculus) are a familiar
sight
in Europe hovering along motorways and grasslands. They are watching
for
small rodents. Their quarry is fast and nimble and ranges over habitat
that is often uniform and extensive. At times, the kestrel's task must
seem like a search for the proverbial needle in a haystack. However,
rodents
mark their runs with urine and feces, which are visible
in ultraviolet light. In tests, wild kestrels brought into
captivity
were able to detect vole and mouse latrine scents in ultraviolet
settings
(Koivula et al. 1999). This ability enables them to screen large areas
of vegetation in a relatively short time and to concentrate hunting at
'busy intersections'. Source: www.bbc.co.uk/nature/birds/
may play a role in navigation as an adaptation to the coloration
of an
unclouded sky. Short-wavelength gradients would vary depending on the
sun's
angle in the sky. These gradients would increase in saturation as the
sun
moves from directly overhead to an angle of 90 degrees. Color
gradients
in the sky due to UV or polarized light may also assist navigation when
the sun is hidden by clouds (Husband and Shimizu 1999). See
'Bird
colour vision: exploring the fourth dimension.'
Photopigment absorption spectra for a pigeon and a
human.
(Husband
and Shimizu 2001, adapted from Bowmaker 1991)
Animals extract information about the spectrum of light
striking different regions of their retinas by contrasting the
responses
of photoreceptors containing different
photopigments. This figure shows
the absorption spectra of the three types of photopigment that
mediate human color vision and the four types of
photopigment
that
mediate color vision in European Starlings. Because Starlings
have four cone photopigments, there are four different
outputs, and none are identical to any of the three outputs
of the
human
cones.
Because these photoreceptor outputs are all that
nervous
systems retain for the analysis of color, the colors we see are
different
from the colors seen by a Starling (or any other
animal).
Objects having one hue to a human may have drastically different hues
to
a
bird (Rowe 2000).
UV Got Great Feathers, Baby - Female
birds see
something in their mates that evades the human eye: the ultraviolet
gleam
of their plumage. Birds, like many other animals, can perceive
ultraviolet
light as well as the wavelengths visible to the human eye;
insects,
for example, use UV reflectance to home in on flowers. Bennett et
al. (1997) wondered what else birds might do with their UV vision. So
they
captured 16 female starlings and 32 males & designed an experiment
to see if females used UV reflectance to pick their beaus. For each
test
the researchers let a female check out 4 different males, lined up
behind
transparent filters that blocked UV light. To gauge her interest, the
team
measured how long the female stood & how many times she hopped in
front
of each male. Then they let another female size up the same four males.
For the next round of tests, they removed the filters and revealed the
same males in their full-color glory. They found that under any
lighting
condition female starlings had very similar tastes. About 90% of the
time,
the two females preferred the same male of any given four. But the type
of light determined which male was deemed top bird. Without the filter,
females preferred males whose feathers reflected lower amounts of UV.
But
without UV light, "females switched their preference away from plumage
color," says Innes Cuthill, a behavioral ecologist at the University of
Bristol. He's not sure exactly what guided their choice instead, but
suspects
body language such as rates of feather fluffing. The moral, the
researchers
say, is not to ignore UV wavelength when studying bird mate choices.
"We
can't always rely on the colors we see to predict birds' mate choice," Cuthill says.
Areas & foveae - many birds have a horizontal streak or
"central
area" across the retina with higher concentrations of sensory cells,
usually
with a fovea (area of highest concentration of sensory cells) at each
end.
Photoreceptor (cone) densities in the foveae may be as high as
65,000
per
square millimeter in some diurnal birds of prey (e.g., American
Kestrel)
(Gunturkun 2000).
In humans, by comparison, the density of cones in the fovea is
about
38,000
per square millimeter (Curcio & Allen 1990).
The eyes of Oilbirds -- An extreme
example of
a low light-level lifestyle among flying birds is provided by the Oilbird,Steatornis
caripensis. Oilbirds breed and roost in caves in northern South
America and Trinidad, often at sufficient depth that no daylight can
penetrate,
and forage for fruits at night. Using standard microscopy techniques,
Martin
et al. (2004) investigated the retinal structure of oilbird eyes and
used
an ophthalmoscopic reflex technique to determine the parameters of
these
birds visual fields. The eyes are relatively small (axial length 16.1 ±
0.2 mm) with a maximum pupil diameter of 9.0 ± 0.0 mm, achieving
a light-gathering capacity that is the highest recorded in a bird
(f-number
1.07). The relatively large pupil helps the oilbird eye collect four
times
more light than the human eye. The light-sensitive rod cells within the
eye are stacked three deep, with a density of about 1,000,000 per mm2
--
more than double the number usually found in vertebrate eyes. The
tiered
strategy, which has previously been found only in deep-sea fish,
maximizes
the chance that every photon of light entering the eye will be
intercepted.
But extreme sensitivity comes at a cost.The retina’s tiered structure
makes
it difficult for the brain to work out exactly where the light has come
from, so oilbirds have a poor eye for detail. Martin et al. (2004)
therefore
suggest that these nocturnal birds rely on a combination of information
from smell and echolocation, as well as from sight, to forage
successfully.
Visual acuity:
is defined as the ability to discriminate two points as being two
points or, in other words, the ability of an observer to resolve fine spatial details.
overall, the visual acuity of many birds is comparable to humans (see figure below)
however, some birds, e.g, passerines, large raptors, & vultures,
may
have acuity 2.5 - 3 times that of humans. For example, the acuity of
American
Kestrels is such that they can recognize insects just 2 mm long from a
distance of 18 meters (Fox et al. 1976).
A sharp-eyed kestrel catching insects in flight.
Grating acuity across bird species. Nocturnal species, like owls, are at the lower end of the acuity spectrum. In contrast, diurnal raptors have very
high visual resolution. Typical values for humans and cats are shown for comparison. Grating acuity is the smallest distance between single elements of a
periodical pattern that is just resolved (and is reported as cycles per degree [cpd]) (Figure from Harmening and Wagner 2011). Although owl spatial acuity is below that of
most other birds,
they have excellent absolute sensitivity (i.e., the smallest amount of light that just elicits visual perception) as well as excellent depth perception.
From Wikipedia: "Resolution in CPD can be measured by bar charts of different numbers of white/black stripe cycles. For example, if each pattern is 1.75 cm wide and is placed at 1 m distance from the eye, it will subtend an angle of 1 degree, so the number of white/black bar pairs on the pattern will be a measure of the cycles per degree of that pattern. The highest such number that the eye can resolve as stripes, or distinguish from a gray block, is then the measurement of visual acuity of the eye." For humans, grating acuity generally ranges from about 30 to 60 cpd (e.g., 50 CPD means detecting 0.35 mm line pairs at 1 m).
Migrating birds may 'see' magnetic field -- Migrating
birds navigate without a compass, map, or GPS unit. But they may carry
their own navigational array, which lets them "see" the Earth's
magnetic
field. Ritz et al. (2000) used chemical experiments, physics theory and
3-D computer modeling to show that part of a bird's optical system
could
be affected at a molecular level by weak magnetic fields. Migrating
birds
appear to draw from the Earth's magnetic field visual information about
whether they're properly oriented along the migration route. The birds
aren't simply pointed in a particular direction by the magnetic effect,
like flying compass needles. They actually see the field in some way.
Ritz
et al. (2000) don't know exactly what the birds see. But their research
suggests that they get some sort of visual feedback when they're on
path
and a different cue when they stray, kind of like clear reception when
a TV antenna is aligned vs. static when it's not. Migrating birds
likely
combine this information with other navigational cues. Other animals,
like
salmon, salamanders and hamsters, likely have similar abilities. Ritz
et
al. (2000) traced the system to "receptors" in the eyes and brain,
proteins
that absorb light & provide information about color, day, and
night.
The retina includes color receptors, black & white receptors, and
another
type known to regulate circadian rhythms. This receptor, which makes
you
sleepy at night, also appears to play a role in processing magnetic
signals.
Scientists have observed magnetic reception previously. For example,
the
"magnetoreception" of bacteria filled with magnetic particles that make
them natural compasses. But the way it's accomplished in higher
animals,
whose systems aren't chock-full of tiny magnets, has been a mystery.
Ritz
et al.'s (2000) research doesn't settle the question, but it does
provide
a promising avenue for further inquiry. -- Greg
Kline, Champaign News-Gazette
More information about magnetoreception is provided below.
Hearing and Balance - The avian ear, like that of mammals,
has
three sections: outer ear, middle ear, & inner ear:
outer, or external, ear - unlike mammals, birds have no pinna.
The
short
canal (external acoustic meatus) leading to the tympanic membrane
(eardrum)
is covered by special feathers that do not obstruct sound transmission.
middle ear - one middle ear bone (stapes or columnella), not 3 (malleus, incus, & stapes) like mammals
Columellae of several species of birds (From: Thomassen et al. 2007).
The semicircular canals serve as a kind of gyroscope helping the brain to detect where is up and where is down, and the body to stay balanced. Bronzati et al. (2021) investigated the structure of these canals in the earliest representatives of the reptile group called Archosauria, which include birds (and their dinosaur relatives) and crocodylians. Some of the earliest dinosaurs had canals as large as those seen in some living birds, indicating that dinosaurs evolved a bird-like sense of balance long before the origin of flight. These authors also found that there was a great variation in the size of these canals in the first stages of archosaur evolution, indicating a burst of ecological diversity during the rise of these animals in the beginning of the age of the reptiles.
Head (circles) and body (squares) vertical
oscillations,
and humeral excursion during
the wingbeat cycle of a Black-billed Magpie taken
from
x-ray film (Warrick et al. 2002).
The avian neck as a shock absorber
(Warrick et
al. 2002) -- During flapping flight when lift production ceases during
upstroke, birds experience downward accelerations due to gravity and
upward
accelerations due to lift. Many forms of locomotion produce similar
stresses,
but only flying species would experience these oscillations 10 times a
second (a typical avian wingbeat frequency). At least two sensory
functions
could be severely impacted by such rapidly alternating accelerations:
vision,
and static equilibrium. Vision might be affected by simply
introducing
extraneous visual flow. Similarly, the maculae of the inner
ear, which
in all vertebrates use the acceleration due to gravity to provide
information
regarding the position of the head, would be subjected to
accelerations
that might compromise this function. Given that birds probably do not
need
to continuously confirm the vertical oscillations of the body during
flapping
flight, there may have been selective pressure to isolate the head from
these vertical accelerations, leaving their eyes and maculae free to
gather
only useful information about their paths through and positions in
space.
Digitized x-ray film of a single Black-billed Magpie (Pica pica)
flying in a wind tunnel at 8 m per sec show that they have the ability
to isolate the head from the movement of the body during flapping
flight.
In level flight, the bird's body fell an average (± standard
deviation)
of 1.44 ± 0.30 cm with every upstroke, while it restricted head
vertical movement to as little as 0.14 cm during a wingbeat cycle
(average
for all wingbeats = 0.43 ± 0.21 cm). The degree to which the
bird
decoupled vertical movement of the head and body appeared to depend on
whether or not the bird was changing position in the wind tunnel. For
example,
the head exactly followed the body during a brief climb, but was
immediately
isolated from the sinusoidal body excursion (as it was at the beginning
of the series; see Figure above ) as soon as level flight was
re-established.
This suggests that the isolation of the head from the vertical
accelerations
may be important in allowing an uncluttered vestibular ‘picture' of the
bird's substantive changes in vertical position. While the anatomical
details
of this dampening mechanism are undescribed, a spinal reflex involving
the flexors and extensors of the dorsal and ventral cervical
musculature
(e.g., the semispinalis capitus, biventer cervicis; longus colli) seems
likely.
the cochlea is where 'sound' is converted into nervous impulses
that
travel
to the brain. More precisely, hair cells (basilar papilla) within the cochlea are 'deflected' by pressure waves, generating nervous impulses.
Avian cochlea. The sensory epithelium, consisting of hair cells and supporting cells, rests on the
basilar member (BM). The hair cell range in height from tall (T; near the superior margin, sup) to short
(S; near the inferior margin, inf).
The tectorial membrane (TM)
is located just above the hairs (also
called stereocilia). The 'hollow' areas above the tectorial membrane and below the basilar membrane are
filled with fluid called perilymph (Figure from Tilney and Saunders 1983).
A: Surface view of the basilar papilla of a Kiwi obtained from scanning electron
microscopy.
B: Cross section of a Kiwi cochlea (Figure from Corfield et al. 2011).
Birds 'hear' like mammals do:
1) Sound waves (pressure waves in the air) cause the tympanic
membrane
(eardrum) to vibrate.
2) Vibration of the eardrum causes vibration of the stapes.
3) Vibration of the stapes causes vibration of the oval window (a
membrane
at the entrance to the cochlea).
4) Vibration of the oval window causes pressure waves in the
fluid in
the
cochlea.
5) These pressure waves cause movement of the basilar membrane
(on
which
hair cells, or papilla, are located).
6) As the basilar membrane 'vibrates', the hair cells are
'deflected'
or
bent by contact with the tectorial membrane & this generates
nervous
impulses.
7) Impulses travel to the avian brain, stimulate nerve cells in
the
brain, & the bird 'hears.'
Bird cochleas are between 2 and 11 mm in length and
contain
between 3,000 and 17,000 hair cells.
Hair cells form a continuum, ranging from 'tall' to
'short.' Short hair cells are located on the basilar membrane (blue), a
membrane that moves or vibrates in response to pressure
waves in the cochlea. When the hairs move against
the tectorial membrane (yellow), nerve fibers at the
base of the hairs are activated and nervous impulses are generated.
The perceived frequency of a sound depends on which
hair
cells are stimulated (with those further from the oval
window responsible for higher frequencies; in birds,
the average space constant, i.e., distance along the cochlea relative
to frequency detected, is < 1 mm/octave (Manley
2000,
and figure also from Manley 2000).
Loss or damage of
sensory, or hair, cells in the inner
ear, results in hearing impairment. These cells can be damaged by
overexposure
to intense sounds. In mammals, once these hair cells are lost, they are
not replaced, so hearing loss is permanent. Birds, however, have the
remarkable
ability to regenerate and replace the hair cells of the inner ear
following
damage or loss (Dooling and Dent 2001). Here are scanning electron
microscopic
pictures of bird inner ears at three different time periods after
exposure
to a chemical (kanamycin) that destroys hair cells. After 28 days, the
number of hair cells in the regenerated bird ear has nearly returned to
normal levels.
Hearing of Archaeopteryx vs. living birds -- The earliest known bird, Archaeopteryx, had a similar hearing range to that of Emus, suggesting that the 145 million-year-old creature — despite its reptilian teeth and long tail — was more birdlike than reptilian. Using computed tomography, or CT imaging, Walsh et al. (2009) found that the length of the inner ear of birds and reptiles could be used to accurately predict their hearing ability and even aspects of their behavior. “In modern living reptiles and birds we found that the length of the bony canal containing the sensory tissue of the inner ear is strongly related to their hearing ability,” said study co-author Paul Barrett. “We were then able to use these results to predict how extinct birds and reptiles may have heard and found that Archaeopteryx had an average hearing range of approximately 2000 Hz. This means it had similar hearing to modern Emus, which have some of the most limited hearing ranges of modern birds.” Walsh et al. (2009) studied in the inner ear anatomy of 59 species of living and extinct birds and reptiles. “By examining the three dimensional CT scans we were able to see for the first time the real relationship between hearing ability and behavior in extinct reptiles and birds,” said Stig Walsh, Natural History Museum palaeontologist and lead author on the study. “The size of the cochlea duct (the bony part of the inner ear housing the hearing organ) in living birds and reptiles accurately predicts the hearing ranges of these animals. This simple measurement can therefore provide a direct means for determining hearing capabilities, and possibly behavior, in their extinct relatives, including Archaeopteryx.” This study also adds more information about how bird-like Archaeopteryx was (Source: Ohio University).
Hearing ranges of birds:
For most birds, hearing is best at frequencies of 1 - 4 kHz, but
some
birds
are able to detect much higher frequencies (up to 10 - 12 kHz).
The ability of birds to discriminate differences in the frequency
of
sounds & to detect gaps between sounds is generally similar to humans.
Median audiograms for 48 species of birds. Birds hear best at frequencies between 1 - 5 kHz,
with hearing most sensitive at about 2 - 3 kHz. In general, owls (Strigiformes) can detect softer sounds
than other birds over the entire range of frequencies. dBSPL is a measurement of sound pressure level in decibels,
where 0 dBSPL is the reference to the threshold of hearing for a typical person (Figure from: Dooling 2002).
Sound localization:
considerable evidence that birds can & do localize the
vocalizations
(or other sounds) of their own & other species
many owls are specialized for localizing the source of sounds
(and,
therefore,
prey). Some owls have facial discs that assist in sound localization. For example, Barn owls are well known for their conspicuous ruff. The ruff serves as a sound collector and is very important for sound localization.
Owls note the differences in intensity and timing of sounds between
the two ears.
Feather types on the Barn Owl’s head. Three types of feathers are shown (Koch and Wagner 2002).
The contour feather (top) is the typical contour feather found everywhere on the head and body except in the ruff;
it shows no specialization. Auricular feathers (left) fill the ruff. This feather type has a reduced ramification so that it becomes acoustically
transparent but still is effective in preventing the ruff from becoming dirty. Reflector feathers (right) form the border of the ruff. This feather type
is very densely ramified and, thus, is able to influence the path of the sound. Scale bars 1 cm (From: von Campenhausen and Wagner 2006).
Locating
a Mouse by Its Sound - At Caltech in the mid-1970s, Masakazu
(Mark)
Konishi began studying the auditory system of barn owls to resolve the
question: Why do we have two ears? While most sounds can be
distinguished
quite well with one ear alone, pinpointing where sounds are coming from
requires a complex process called binaural fusion, where the brain
compares
information received from each ear & translates subtle differences
into a perception of a single sound coming from a particular location.
The ability to identify where sounds are coming from based on auditory
cues is common to all hearing creatures, but owls - especially barn
owls
- excel at the task. These birds exhibit such extraordinary sound
localization
abilities that they are able to hunt in total darkness.
Together with Eric Knudsen, now at Stanford
University,
Konishi undertook experiments in 1977 to identify networks of neurons
in
the brains of owls that could distinguish sounds coming from different
locations. He did so by probing the brains of anesthetized owls with
fine
electrodes. With electrodes in place, a remote-controlled sound speaker
was moved to different locations around the owl's head. As the speaker
moved, imitating sounds the owl would hear in the wild, the
investigators
recorded the firing of neurons near the electrodes. Over several
months,
Konishi and Knudsen identified an area in the midbrain containing cells
called space-specific neurons that fired only when sounds were
presented
in a particular location. Astonishingly, the cells were organized in a
precise topographic array, similar to maps of cells in the visual
cortex
of the brain. Aggregates of space-specific neurons, corresponding to
the
precise vertical and horizontal coordinates of the speaker, fired when
a tone was played at that location.
"Regardless of the level of the sound, these
cells always
responded to the sources at the same place in space. Each group of
cells
across the circuit was sensitive to sound coming from a different place
in space, so when the sound moved, the pattern of firing shifted across
the map of cells," Knudsen recalls.
Some owls have asymmetrical
ear openings, allowing them to accurately note differences in
the intensity and timing of sounds in both the
horizontal
(azimuth) and vertical (elevation) planes.
occurs in 2 families of birds: Steatornidae (oilbirds) & Apodidae
used for orientation in dark caves
birds (& other animals) echolocate by producing clicking
sounds and
then receiving and interpreting the resulting echo
The Oilbird
(Steatornis caripensis), a nocturnal bird of South America
that
lives in caves and feeds on fruit, mainly the nuts of oil palms.
Oilbirds are about 30 cm (12 inches) long, with a fanlike tail and long
broad wings. They have a strong hook-tipped bill, long bristles around
the wide gape, and large dark eyes. Oilbirds use echolocation to find
their
way within the caves where they roost and nest from Trinidad and Guyana
to Bolivia. The sounds
emitted are within the range of human hearing: bursts of
astonishingly
rapid clicks (as many as 250 per second). Oilbirds also utter squawks
and
shrieks that suggest their Spanish name, guácharo ("wailer"). At
night, oilbirds fly out to feed, hovering while they pluck fruit from
trees.
Two to four white eggs are laid on a pad of organic matter on a ledge
high
up in a cave. The young, which may remain in the nest for 120 days, are
fed by regurgitation until they are 70 - 100% heavier than adults.
Indians
render the squabs for an odorless oil for cooking and light; hence the
bird's popular and scientific names.
Birds use multiple sources of directional information for navigation, e.g., the time-compensated sun-compass of homing pigeons and diurnally-migrating songbirds. Nocturnally-migrating birds cannot use the sun, but use the stars for orientation. Other information, like the glow in the western sky after sunset caused by the setting sun can be used shortly after sunset along with the stars. However, use of the sun, stars, and the glowing sky requires that at least part of the sky is visible to the birds. Many birds are also able to accurately orient when the sky is not visible (e.g., cloud cover). This requires non-visual sources of information. Many studies have established that birds are sensitive to the Earth's magnetic field. Pigeons and other birds use the geomagnetic field as a compass, and are also sensitive to slight temporal and spatial variation in the magnetic field that are potentially useful for determining location. The avian magnetic compass may be:
a light-dependent,
wavelength-sensitive system that functions as a polarity compass (distinguishing poleward from equatorward rather than north from south). The receptor is within the retina and is based on one or more photopigments, perhaps cryptochromes (Beason 2005).
based on magnetite and might serve to transduce location information independent of the compass system. This receptor appears to be associated with the ophthalmic branch of the trigeminal nerve and is sensitive to very small changes in the intensity of the magnetic field (Beason 2005).
The inclination compass -- Rather than using the polarity of the earth's magnetic field (i.e., the compass points north), birds use the inclination of magnetic field lines relative to gravity. An inclination compass provides information about the axis of the field lines as well as the direction towards the magnetic pole or equator. The intersection of the magnetic field lines with the horizon points polewards (in both the northern and southern hemispheres) and the direction where the inclination angle diverges points toward the equator (Muheim 2004).
The avian inclination compass provides information about the alignment of the magnetic field not the polarity of the field (like a compass does).
From: Muheim (2004).
Light-dependent magnetic compass -- External magnetic fields can influence photon-induced processes that involve biomolecular reactions and recent work suggests that molecules called cryptochromes are involved. Magneto-sensitive photoreceptors distributed throughout the retina of the eye may show increased or decreased responses to light, depending on their alignment relative to the magnetic field and allow birds to actually see the magnetic field lines. Current evidence suggests that the right eye of birds is more important than the left in 'seeing' magnetic field lines. The figure to the left illustrates how magnetoreception information might be perceived by birds. Using an inclination compass can create problems close to the magnetic poles (90 degrees) and at the magnetic equator (0 degrees). The alignment of the field lines (vertical at the poles and horizontal at the equator) makes it impossible to choose the correct direction. Fortunately, birds have alternative means of obtaining directional information (e.g., sun and stars). From: Muheim (2004).
When excited with light, CPF forms a short-lived charge-separated state with a negative charge on the ball-like fullerene unit and a positive charge on the rod-like carotenoid unit. The lifetime of the charge-separated state before it returns to its lowest energy or ground state is sensitive to the magnitude and direction of a weak magnetic field similar to Earth's.
Using the earth’s magnetic field to navigate -- Current evidence suggests that birds use magnetically-sensitive chemical reactions initiated by light (called chemical magnetoreception) to orient themselves, but no chemical reaction has been shown to respond to magnetic fields as weak as the earth’s. However, Maeda et al. (2008) have now synthesized a molecule (carotenoid-porphyrin-fullerene, or CPF) that is sensitive to both the magnitude and the direction of magnetic fields as tiny as the Earth’s (which is, on average, one-twenty thousandth as strong as a refrigerator magnet). The synthesized molecule consists of three units (a carotene-porphyrin-fullerene triad). When excited by light, the triad molecule forms a charge-separated state with the negative charge on the soccer-ball-like fullerene (or buckyball) portion and the positive charge on the rod-like carotene portion. The triad molecule, in its charge separated state, could be thought of as having little bar magnets at either end – so far apart that they interact with each other only weakly.
How could this influence the direction taken by a migrating bird? Birds appear to orientate at dusk, and cryptochromes (light-sensitive proteins known to be present in the retinal neurons of some birds) form their pair of free radicals when "activated" by the blue light typical of dusk. Thus, dusk might activate the birds' magnetic sense, producing the radical pair. The concentrations of each free radical would be controlled by the Earth's magnetic field that varies with latitude. As a result, the radicals would bind in varying degrees with other signalling molecules, depending on how far north or south the animal is. How would birds decode this"magnetic sense?" Some investigators believe that birds have an additional layer to their vision that, when switched on, allows them to visually "see" the Earth's magnetic field in a manner similar to "head-up displays" in fighter jets and some cars, where transparent screens displaying information are built into windscreens.
Head-up display of a fighter jet.
Study could help identify mechanism of magnetoreception in birds — Migrating birds stay on track because of chemical reactions influenced by the Earth’s magnetic field. The birds are sensitive even to rapidly fluctuating artificial magnetic fields. These fields had no effect on magnetic materials such as magnetite, indicating that the birds do not rely on simple chunks of magnetic material in their beaks or brains to determine direction, as experts had previously suggested. Ritz et al. (2004) exposed 12 European robins to artificial, oscillating magnetic fields and monitored the orientation chosen by these birds. The stimuli were specially designed to allow for responses that could differ depending on whether birds used small magnetic particles on their bodies or a magnetically sensitive photochemical reaction to detect the magnetic field. “We found that the birds faced in the usual direction for their migration when the artificial field was parallel to the Earth’s natural magnetic field, but were confused when the artificial field was applied in a different direction,” said Ritz. “Since the artificial field’s oscillations were too rapid to influence magnetic materials like magnetite, it suggests that the most likely mechanism for magnetic orientation in these birds involves tiny changes to magnetically sensitive chemical reactions, possibly occurring in the eyes of the birds — we are not sure.”
“Unlike our senses involving vision, hearing, smell and touch, we do not know what receptors underlie magnetoreception,” Ritz said. “Migratory birds have long been known to possess a magnetic compass that helps them find the correct direction during their migratory flights. It has remained unknown, however, how birds can detect the direction of the Earth’s magnetic field. “Now, our study points to what we need to look for a molecular substrate for certain chemical reactions."
How a night-migrating songbird might detect and use its magnetic compass. (a) During the day, the bird forages to fuel up for its journey.
(b) During twilight and at night, dim light (mainly in the blue-green range) excites photoreceptor molecules (probably cryptochromes) in the retina (the image
shown is a transverse cut through the eye; photoreceptors at top & ganglion cells at bottom). The light excitation initiates an unknown signalling pathway
(involving radical-pair formation & electron-transfer) modulated by the earth's magnetic field. (c) The magnetic field direction is translated by the sensory cells of
the retina into a visual pattern that is sent to the brain.
(d) Head-scanning. Head movements may make it easier to detect the visual pattern generated by
the magnetic field. (e) Visual input is relayed to the brain where
the compass direction is determined. It is possible that input from magnetoreceptors in the bill
(see above) is also important in the process of determining direction.
(f) If the bird's internal clock and internal physiology (e.g., hormones) are in migratory
mode, a comparison between the reference direction and the bird's
genetically-coded migratory direction fixes its magnetic compass orientation. (g) Magnetic
compass information is integrated with input from other orientation cues
(e.g., sun-related twilight information) that helps insure that a bird is orienting correctly
(see 'Sense of direction' on the Bird Biogeography II page for details
about the study of migrating Swainson's Thrushes). (h) The bird's spatiotemporal orientation program
ensures that it arrives at the appropriate breeding or wintering
site (picture shows the distribution of recoveries of banded European Robins relative to where they
were banded; arrow indicates the main migratory direction).
From: Mouritsen and Ritz (2005).
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3744.
ocular surface to clear the cornea of debris. Ocular surface
lubrication originates from two secretory glands. The lacrimal
gland is situated in the inferior temporal quadrant associated
with the more active lower eyelid, although in many species this
gland is absent or rudimentary. Additionally, most birds, especially
cormorants and falcons, have a second secretory gland called
a Harderian gland located in the posterior and nasal aspect
of the orbit associated with base of the nictitating membrane.
In falcons, this secretory gland produces a viscous solution
to moisten the cornea during the breathtaking stoops that
are the falcon’s trademark. Although the composition of
these secretions is not known, a compound such as hyaluronic acid
would moisten the surface without the rapid evaporation seen
with a more dilute tear film. Such a coating would maintain a
smooth surface, but might pose other difficulties by collecting debris
(Schwab and Maggs 2004).
the membrane called
the marginal plait (photomicrograph to the right). With each blink this
flange-like flap collects the tear film and any associated
debris to drain through the enlarged puncta (
Tubular eye of an owl ( Bayon et al. 2007) 
Tucker of Duke University has long been puzzled by the way birds of
prey
approach their dinner. In studies of Peregrine Falcons, he & his
colleagues
found that the birds almost always follow a curved path once they get
within
1.5 km of their prey (Tucker 2000a). "We had observed these curved paths
for years, and I was racking my brains to explain that," says Tucker.
He
suspected the explanation lay in the birds' vision. Tests have shown
they
see objects in front of them most clearly when they turn their heads
about
40 degrees to one side (i.e, the image falls on the deep fovea; see Figures below). But turning their heads in mid-flight might
increase
the birds' aerodynamic drag, slowing them down. To test this, Tucker
placed
models of Peregrine Falcons and Red-tailed Hawks in a wind tunnel.
Force
sensors showed that, at a wind speed of 42 km per hour, the drag on
birds
whose heads were turned 40 degrees was more than 50% greater than on
those
looking straight ahead. To avoid this, Tucker concludes, the birds keep
their heads straight and follow a path called a logarithmic spiral.
That
way, they can keep one eye fixed on their prey. And while a spiral path
is longer, the speed advantage more than compensates. 
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monitored the orientation chosen by these birds. The stimuli were specially designed to allow for responses that could differ depending on whether birds used small magnetic particles on their bodies or a magnetically sensitive photochemical reaction to detect the magnetic field. “We found that the birds faced in the usual direction for their migration when the artificial field was parallel to the Earth’s natural magnetic field, but were confused when the artificial field was applied in a different direction,” said Ritz. “Since the artificial field’s oscillations were too rapid to influence magnetic materials like magnetite, it suggests that the most likely mechanism for magnetic orientation in these birds involves tiny changes to magnetically sensitive chemical reactions, possibly occurring in the eyes of the birds — we are not sure.” 