BIO 554/754
Ornithology

Nervous System: Brain and Special Senses II

 

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 represents the principal mechanism of ocular cleansing. In birds, the external eyelids possess smooth muscle, and may close only during sleep. The nictitans, on the other hand, is operated by two striated muscles and is capable of extremely rapid sweeps across the 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).



Check out this White-eyed Buzzard's nictitating membrane


 

The nictitating membrane of many such birds has a cartilaginous-like connective tissue fold along the leading edge of 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 (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 layer of "feather epithelium." This remarkable adaptation of a surface epithelium is believed to be unique to the epithelium lining the nictitans of many birds and reptiles. Long microvilli with club-like termini and numerous secondary projections from their long axis extend from the apical membrane of epithelial cells lining the bulbar surface of the third eyelid. Those of Peregrine Falcons (above) are extremely robust and likely form a "histological feather duster" that sweeps the cornea 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.

Link:

How birds avoid crashes


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:


Source: http://www.lsi.usp.br/~bioinfo/chickeneye.html
 


Source: Rowe (2000)

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

Links:

How owls swivel their heads

Solving the mystery of owls' head-turning abilities

Study uncovers secret of the owl's amazing rotating head


 



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).


Common Pauraque (Nyctidromus albicollis)
Photo by Monte M. Taylor

Source: http://www.fieldandstream.com


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'


Source: http://www.lam.mus.ca.us/birds/guide/pg006.html

 
American Woodcock


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).

                                                From:
Fernandez-Juricic et al. (2004)


From: Avian vision, navigation, and orientation by R. Beason


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.
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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. 



Source of photo on the right: http://www.pigeon.psy.tufts.edu/avc/pblough/introduction.htm

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.

Link:

Protein unique to avian retina contributes to visual acuity by helping eyes 'breathe'

Breathing through the eyes


The avian retina has three types of photoreceptors that 'translate' light into nervous impulses:


 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

These oil droplets:


The transparent or colorless oil droplets found in many birds permit perception of very short spectral wavelengths (ultraviolet or near ultraviolet).  Such perception:



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/
Source: www.bbc.co.uk/nature/wildfacts/factfiles/243.shtml

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.


Foveae of an Arctic Tern (top) and a human (bottom)
(Source: Husband and Shimizu 2001; http://www.pigeon.psy.tufts.edu/avc/husband/avc4eye.htm)


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:

 
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.

Source: http://www.ks.uiuc.edu/Research/magsense/ms.html


Winged Migration  


Hearing and Balance - The avian ear, like that of mammals, has three sections: outer ear, middle ear, & inner ear:


Columellae of several species of birds (From: Thomassen et al. 2007).


Source:
www.bio.purdue.edu/Bioweb/People/Faculty/iten.html

Source: http://www.palaeos.com/Vertebrates/Bones/Ear/Overview.html


Cross-section through a semicircular canal


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.


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:


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.

Source: http://www.bsos.umd.edu/psyc/dooling/HC1.htm

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:


Source: http://elephant.elehost.com/About_Elephants/Senses/Hearing/hearing.html


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:

Owls note the differences in intensity and timing of sounds between the two ears.

Source: kybele.psych.cornell.edu/~edelman/Psych-214-Fall-2002/pp-week1-2.html

 


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. 

Source: www.hhmi.org/senses/c210.html

 

 

 



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.

(Figure source: web.psych.ualberta.ca/~msnyder/Academic/psych403/week8/w8oh.html)


Front view of the skull of a Tengmalm's Owl (Aegolius funereus) illustrating the asymmetrical ear openings (Norberg 2002).

Echolocation:


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.
Source: www.asawright.org/nature/oilbirds.html

Magnetoreception:

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:


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."


Homing pigeons get their bearings from their beaks -- Althought it has long been recognized that birds possess the ability to use the Earth’s magnetic field for navigation, just how this is done has not yet been clarified.  However, Fleissner et al. (2007) discovered iron-containing structures in the beaks of homing pigeons. Specifically, iron-containing subcellular particles of maghemite and magnetite were found in sensory dendrites of the skin lining the upper beak of homing pigeons. Different from earlier hypotheses concerning magnetoreception that assumed magnetite as the crucial mineral, it now appears that both iron minerals are essential for a sensitive sensory system that functions as a magnetometer. The dendrites in the pigeon bill are arranged in a complex three-dimensional pattern with different spatial orientation designed to analyze the three components of the magnetic field vector separately.  They react to the Earth’s external magnetic field in a very sensitive and specific manner, thus acting as a three-axis magnetometer. Thus, the birds may sense the magnetic field independent of their motion and posture and can identify their geographical position. Fleissner et al. (2007) believe that this ability is not unique to homing pigeons and expect that the ‘pigeon-type receptor system' might turn out to be a universal feature of all birds. 

Localization of putative magnetoreceptors in the beak of homing pigeons. A: Schematic drawing of the pigeon skull with the peripheral course of the ophthalmic branch of the trigeminal nerve that gives rise, by its median branch (R. o. medialis, ramus ophthalmicus medialis) to the entire somatosensory innervation of the tip of the upper beak. B: Macroscopic view of the inside of the upper beak. White dots indicate the sites of the candidate magnetoreceptor nerve endings as derived from serial histologic sections (t, tongue). C: Sagittal section through the inner skin of the upper beak. The areas with meghemite and magnetite (arrows) are above the solid layers, epidermis (ep), and dermis (d), within the stratum laxum of the subcutis (sc) that got its name from the spongy texture with numerous fat cells (fc). Scale bars = 2 mm in B, 100 micrometers in C (From: Fleissner et al. 2003).

 

Graphic source: thisislondon

 
Homing Pigeons


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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Useful links:

Bird vision

Hearing and the Bird Ear

Taking a Bird's-Eye View…in the UV: Recent studies reveal a surprising new picture of how birds see the world

The Life of Birds: Bird Brains


Back to BIO 554/754 Syllabus

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