Birds

 

Three types of blinking were recorded in birds: reflex, associated with pecking and spontaneous.

Reflex blinking and blinks on pecking are discussed elsewhere.

 

 

 

There are three types of spontaneous blink in birds:

 

1. Nictitating membrane blink

This is the commonest type of blink and it is present in all birds. It is usually rapid in onset, brief and accompanies head turns, but becomes prolonged when combined with saccadic oscillation of the eyes, or elevation of the lower eyelid. It can occur:

        1a. With the head still 

Nictitating membrane blinks occurring when the head is still are are the easiest to see. They are often associated with saccadic oscillation (see below).

Figure 35.png

Nictitating membrane blink with the head still in a bush stone-curlew (Burhinus grallarius). At 40ms, the membrane has reached the pupil and at 80ms the cornea is covered. The membrane is almost transparent, so it is likely that vision is retained during the blink.

Nictitating membrane blink with the head still in a grey heron (Ardea cinerea). Note that the anterior part of the upper eyelid appears to be pulled down slightly during the blink. Again the nictitating membrane is transparent. Played at one eighth speed.

There may be an advantage in retaining vision during a blink, both as prey and as predator. In the case of water birds like penguins and ducks, transparent nictitating membranes might allow the bird to use these for protection while diving.

Nictitating membrane blink with the head still in a little penguin (Eudyptula minor), played at 20% speed.

Nictitating membrane blink with the head still in an Australian wood duck (Chenonetta jubata), played at 10% speed.

Nictitating membrane blink with the head still also showing rhythmical rocking of the eyeball (saccadic oscillation - see link) in an Australian wood duck, played at 20% speed.

Nictitating membrane blink with the head still in a Muscovy duck (Cairina moschata). During the blink the eyeball moves in a rhythmic rotatory fashion (saccadic oscillation). Played at one eighth speed

Figure 36.png

At 45ms, the membrane has reached the pupil and at 95ms the cornea is covered.

Nictitating membrane blinks in birds can be unilateral, asynchronous or synchronous. Seeing both eyes during a blink is easy with raptors which have forward facing eyes and more difficult, but still possible, in birds with eyes on the sides of the head.

Almost synchronous nictitating membrane blinks seen in both eyes of a Muscovy duck. Played at one eighth speed.

Synchronous nictitating membrane blinks and saccadic oscillation in an apostle bird (Struthidea cinerea). Played at 20% speed.

Nictitating membrane blink with the head still in a palm-nut vulture (Gypohierax angolensis), played at 20% speed.

In many birds, the nictitating membrane is opaque, temporarily blinding the eye during a blink.

Nictitating membrane blinks with the head still in a Asian woolly-necked stork (Ciconia episcopus). The membrane is opaque. Played at 20% speed.

The degree of opacity of the nictitating membrane varies widely from species to species. It is not easy to determine the ecological factors which are responsible for this.

Nictitating membrane blink with the head still in a southern cassawarry (Casuarius casuarius), played at 10% speed. The membrane here is opaque but not as much as the Asian woolly-necked stork. NB It is the camera moving, not the head.

Nictitating membrane wink in the left eye of a white-crowned hornbill (Berenicornis comatus), played back at 30% speed.

In humans, blinking is synchronous in the two eyes. Winking can only be done by voluntarily closing one eye. In birds, winking is common. An advantage may arise from the fact that vision, albeit with a reduced field, is retained during a wink, even with an opaque nictitating membrane. 

       1b. On head turn 

This is by far the commonest type of blink seen in birds. With almost every, but not all, turns, there is a blink. So frequently does it occur that the question arises, what is it achieving.

Nictitating membrane blink on head turn in bush stone curlew, played at 5% speed.

Figure 40.png

At 40ms, the membrane is halfway across the cornea and at 120ms it has covered it. The blink lasts 280ms.

Nictitating membrane blink on head turn in an Andean condor (Vultur gryphus), played at 20% speed

Nictitating membrane blink on head turn in an emu (Dromaius novaehollandiae), played at 20%. Frame by frame analysis shows that in most cases, the blink begins before the onset of the head movement.

For obvious reasons, it is much easier to study blinking in large birds with large eyes.

Nictitating membrane blink in  both eyes on head turn in an ostrich (Struthio camelus). Played at 5% of recording speed. The blinks in the two eyes appear to be fairly synchronous in onset. The membrane is opaque.

Figure 37.png

The blink lasts 280ms.

Nictitating membrane wink in the right eye on head turn and later in the left eye with the head still in a black-breasted buzzard (Hamirostra melanosternon), played at 30% speed. Note the skin of the anterior part of the upper and lower eyelids is pulled out in the first wink.

In the same individual, a synchronous nictitating membrane blink was seen.

Synchronous nictitating membrane blink with the head still in the same individual.

It s not clear what determines whether the bird winks or blinks.

Nictitating membrane blinks on head turn and at rest in a grey-crowned crane (Balearica regulorum) played at 30% speed.

Nictitating membrane blink on head turn in a Northern bald ibis (Geronticus eremita) at 10% speed. The membrane is opaque.

Figure 38.png

Nictitating membrane blink on head turn in a bearded barbet (Lybius dubius). At 80ms after the onset of the blink, the nictitating membrane has covered the cornea and the medial part of the upper lid has lowered slightly. The membrane is transparent.

Capturing a nictitating membrane blink on head movement is difficult in smaller birds as the head movements are often very rapid causing 'movement blur'. Also the eyes are small and the blink brief.

Rapid head rotation preventing visualisation of blinking in a Pekin robin (Leiothrix  lutea) played at 10% speed.

Nevertheless, it is possible to capture a blink when the head movements are a little slower.

Nictitating membrane blink on head turn in an Oriental dollarbird (Eurystomus orientalis), played at 10% speed.

Nictitating membrane blink in a male regent bowerbird (Sericulus chrysocephalus), played at 10% speed.

Nictitating membrane blinks in a Bali myna (Leucopsar rothschildi), played at 20% speed.

Nictitating membrane blinks at rest and on head movement in an Andean cock of the rock (Rupicola peruvianus), played at 20% speed.

In hornbills, nictitating membrane blinks may occur in association with eye as well as head movements.

Nictitating membrane blink on eye movement in a wreathed hornbill (Rhyticeros undulatus), played at 30% speed.

Nictitating membrane blink and a wide range of eye movements in a female great hornbill (Buceros bicornis), played at one eighth speed.

In humans, voluntary gaze shifts are achieved by rapid (saccadic) eye movement. In most birds, lacking eye movements, gaze shifts are achieved by rapid head movements.

Nictitating membrane blinks during rapid (saccadic) head turns with minimal lowering of the medial part of the upper eyelid in a vulturine guinea fowl (Acryllium vulturinum).

Above played at 5% of the recording speed.

Figure 39.png

At 40ms, the nictitating membrane has almost covered the cornea and there is minimal lowering of the medial part of the upper eyelid. At 80ms,  the membrane is withdrawing. The blink lasts 120ms.

Not all head movements in birds are associated with blinks. To gauge distance, some birds 'peer'.

Side to side head movement (peering) in a fledgling barn owl (played back at 20% speed). Blinking is not usually seen during peering.

One of the ways in which birds and insects gauge the distance of a static object is by moving their head from side to side while fixating on the object. Closer objects will appear to be larger and to move more rapidly than distant objects (van der Willigen et al 2002).

       1c. With movement of the upper and/or lower eyelids (see below)

2. Lower eyelid blink 

 

This is usually slow in onset, prolonged and mainly occurs in drowsiness and during preening. 

Slow, sustained elevation of the lower lid in a drowsy red crested turaco (Tauraco erythrolophus).

Slow, rising and falling of the lower lid in a drowsy fairy penguin (Eudyptula minor), played at 10% speed

Slow, rising and falling of the lower lids in a black-footed penguin (Spheniscus demersus), played at 20% speed

Nictitating membrane blink with slight elevation of the lower lid followed by a slow sustained elevation of the lower lid in a great cormorant  (Phalacrocorax carbo), played at 10%.

Slow rising and falling of the lower lid in a little black cormorant (Phalacrocorax sulcirostris)

Figure 42.png

Asymmetrical elevation of the lower eyelids in a Barking owl (Ninox connivens).

Figure 43.jpg

Elevation of the lower eyelid in drowsiness in a black-necked stork (Ephippiorhynchus asiaticus). The skin of the lower eyelid lacks pigmentation and is paper thin, perhaps allowing light to enter the eye during a lower lid blink.

Lower eyelid blinks are often associated with movement of the nictitating membrane. How often this happens is hard to say as the eyelid obscures the membrane – you can only see it when the lower eyelid fails to cover the eye completely.

Nictitating membrane blink followed by elevation of the lower lid in a male blacked-necked stork.

Lower lid elevation with crossing of the nictitating membrane and saccadic oscillation in a bush stone curlew, played at 1/8th the speed.

Figure 45.png

Lower lid elevation with the nictitating membrane across the pupil at 480ms in a bush stone-curlew

Nictitating membrane blink merging into prolonged elevation of the lower eyelid in a drowsy green peafowl (Pavo muticus), played at one eighth speed.

Sometimes, prior to sleep, the lower lid rises and falls repeatedly.

Repeated lower lid blinks in a drowsy female mallard (Anas platyrhynchos).

Figure 41 a.png

Stills from video.

Nictitating membrane blink and repeated rising and falling of the lower lid in a banded lapwing (Vanellus tricolor).

The lower lids are elevated during self preening and when being preened.

Elevation of the lower lid during preening in a brown pelican (Pelecanus occidentalis), played at 30%.

Nictitating membrane blink followed by elevation of the lower lid during preening in a buff-banded rail (Gallirallus philippensis), played at 20%.

Elevation of the lower lid during preening in a bush stone-curlew.

Figure 44.jpg

Still from video.

Nictitating membrane blink and elevation of the lower lid during preening in a bush stone-curlew.

Elevation of lower lid during preening in a white-headed pigeon (Columba leucomela). Note the elevated lower lid is paper thin.

Nictitating membrane blink merging with elevation of the lower lid in a male blue peacock (Pavo cristatus), as its mate approaches to preen it.

3. Upper eyelid blinks

 

Upper eyelid blinks are mainly confined to three Orders of birds – owls , parrots and pigeons.

Upper lid and nictitating membrane blink on head turn in a masked owl (Tyto novaehollandiae). The upper lid and nictitating membrane of the left eye descend (incompletely) first and then rise as the right eye becomes involved, played at 5% speed.

Figure 46.png

Stills from video. Blinking in the two eyes is not synchronous. Both upper lid and nictitating membrane movements extend over the pupils but only partially cover the corneas.

Synchronous upper lid blink in a barn owl (20% speed)

Synchronous upper lid blink in a spotted eagle owl (20% speed)

Bilateral upper lid blink in a Verreaux eagle owl (20% speed)

Bilateral upper lid and nictitating membrane blink on head turn in a wood owl (20% speed)

Rarely, a nictitating membrane blink without involvement of the upper lids may be seen in owls.

Nictitating membrane blinks and a wink in a southern white faced scops owl (20% speed)

Figure 47.jpg

Figure from Cassells’ Book of Birds (1872). Eye of an owl, showing the arrangement of the nictitating membrane. Both eyelids are divided through their middle and everted, so as to display the nictitating membrane, a, and the passage for the tears (puncta lachrimalia), b.

Upper eyelid winks and synchronous blinks (played at 50% speed) and a nictitating membrane and upper lid blink (played at 10% speed) in a green-winged macaw (Ara chloropterus).

Partial upper lid, full nictitating membrane blink and saccadic oscillation in a yellow-tailed black cockatoo (Calyptorhynchus funereus), played at 30% speed.

Figure 48.png

Stills from video showing that at maximum blink, the upper lid only partially covers the eye.

Upper lid and nictitating membrane blink with the head still in an African grey parrot(Psittacus erithacus), played at 20% speed

Upper lid blink on head turn in a Barbary dove (Streptopelia risoria), played at 20% speed

Figure 49.png

Nearly full upper lid blink in a zebra dove (Geopelia striata). 

In some species, the upper lid movement is slight.

Minimal upper lid movement during nictitating membrane blinks in a flock bronzewing (Phaps histrionica)

In Orders other than owls, parrots and pigeons, the occasional individual species within an Order may be found which also blinks with its upper eyelid.

Upper lid blink in a Gouldian finch (Erythrura gouldiae), played at 20%.

Upper lid blink in a Zebra finch (Taeniopygia guttata), played at 10%.

Upper lid blinks in a green woodpecker (Picus viridis), played at 10%.

Upper lid and nictitating membrane blinks in a blue-crowned motmot (Momotus coeruliceps), played at 10%. The eyelids are white.

Upper lid blinks on head turns and pecking in a Baird's sandpiper (Calidris bairdii) in Hawaii, played at 30%. 

When birds which blink with their upper eyelids become drowsy, an upper lid blink often merges with elevation of the lower lid. Blinks involving the lower lid take longer than simple upper lid blinks.

50a.png

An upper lid blink in a superb fruit dove (Ptilinopus superbus) lasts 80ms compared with 1160ms when the lower lid becomes involved (see below).

Prolonged blink involving first the upper lid then the lower in a drowsy superb fruit dove. 

Figure 50b.png

At 120ms, only the upper lid is involved. At 520ms, the lower lid has partially elevated, as has the upper lid. The blink lasts 1160ms.

Upper and lower lid blink in a wonga pigeon (Leucosarcia melanoleuca). The upper lid descends, then the lower lid rises to meet it. Upper and lower lids then rise in unison. Played at 20% speed.

Upper and lower lid blink in a Nicobar pigeon (Caloenas nicobarica). The lower lid is elevated then the upper lid descends and the two lids move in unison. Played at 20% speed.

Upper and lower lid blink in a common emerald dove (Chalcophaps indica). The upper lid descends, then the lower lid rises to meet it. The nictitating membrane also crosses. 

Figure 51.png

At 80ms, the upper lid has covered the eye. At 320ms, the lower lid has risen while the upper lid is still partially down. The blink lasts 840ms.

Comment. What is striking in these examples of upper and lower eyelid blinks is the way the lids initially move in opposite direction towards each other, then change and move in the same direction in a coordinated manner.

Movement of the nictitating membrane in birds is achieved by the combined action of the pyramidalis and quadratus muscles stretching the elastic nictitating membrane over the cornea as shown in the figures from Walls (1962) and Williams (1994). The quadratus muscle wraps round the tendon of pyramidalis (n). Having two muscles pulling on the same tendon allows more traction to be exerted on the tendon than if there were only one.

Figure 52.jpg

The tendon to the nictitating membrane (n) is pulled by the combined action of quadratus [B(Q)] and pyramidalis (Pyr).

Figure 53.png

Quadratus

Pyramidalis

Tendon attached

to nictitating

membrane

Tendon of the nictitating membrane (D. Williams 1994).

a) Anterior view of eyeball b) Posterior view of eyeball.

When quadratus and pyramidalis relax at the end of a blink, the nictitating membrane resumes its resting position by elastic recoil. The upper eyelid is elevated by levator palpebrae dorsalis (superioris), a striated muscle innervated by the oculomotor (IIIrd cranial) nerve.  The lower eyelid is depressed by depressor palpebrae ventralis, a striated muscle which is innervated by the mandibular branch of the trigeminal (Vth cranial) nerve. Orbicularis palpebrarum, a smooth muscle which is innervated by autonomic (probably parasympathetic) nerves, raises the lower eyelid and depresses the upper eyelid (Baumel et al 1993).

 

In species capable of upper eyelid blinks, it is likely that the upper eyelid is kept tonically elevated by the action of smooth muscle innervated by sympathetic nerves, the equivalent of Muller’s muscle in humans – weakness of which is responsible for the ptosis reported in Horner’s syndrome in birds: an eagle owl (Bubo africanus) (Williams and Cooper 1994) and in a Red-bellied parrot (Poicephalus rufiventris) (Gancz at al 2005).

 

The main source of tears is the Harderian gland at the base of the nictitating membrane. Tear fluid passes through a canal which opens inside the conjunctival sac between the eyeball and the nictitating membrane. The lacrimal gland lies in an inferotemporal position to the globe. It is absent in penguins and owls.

 

Comments on blinking in birds

Birds have nictitating membrane blinks which clean and lubricate the cornea with secretions from the Harderian and lacrimal glands, and lower lid blinks which protect the eye to some extent from injury during preening as well as in sleep. Birds abandoned the muscle required for globe retraction, as they did by and large those required for eye movements This was done in the interests of accommodating larger eyes relative to the size of the skull and lightening the load for flight. The question arises, why did three Orders of birds add upper lid movement, often only partially covering the eye, to the nictitating membrane blinks. What was the advantage?

 

As birds cannot retract their eyes, and it is retraction in other Classes of animal which provides most protection from mechanical injury, did adding the upper eyelid to nictitating membrane blinks provide more protection from injury? And did the feather equivalent of eyelashes on the upper eyelids provide rapid reflex closure of the eyes when these were touched by potentially damaging objects like twigs or leaves? Perhaps, though Walls (1962) does not believe that eyelids provide much protection from mechanical injury.

Evolutionary considerations

Birds and crocodilians, evolved from archosaurs from which dinosaurs also came. While crocodiles have hardly changed in the last 150 million years, producing only 21 species, birds have undergone an enormous transformation. There are more than 10,000 extant species of birds, all derived from the ground-dwelling survivors of the great meteor-induced extinction which occurred 65 million years ago. Taking to the air required major changes including the development of large eyes of high acuity and reduction in the weight of the skeleton. The globes came to fill the orbits and extra-ocular muscles were greatly reduced in size. Eye movements were largely replaced with head movements.

References

Baumel, J.J., King, A.S., Breazile, J.E., Evans, H.E., and Vanden Berge, J.C. (Eds). 1993. Handbook of Avian Anatomy: nomina anatomica avium. Nuttall Ornithological Club.

Gancz, A.Y., Malka, S., Sandmeyer, L., Cannon, M., Smith, D.A. and Taylor, M. 2005. "Horner's syndrome in a Red-bellied parrot (Poicephalus rufiventris)." Journal of Avian Medicine and Surgery 19:30-34.

van der Willigen, R.F., Frost, B.J and Wagner, H. 2002. "Depth generalization from stereo to motion parallax in the owl". J Comp Physiol A. 187: 997-1007.

Walls, GL. 1963. The vertebrate eye and its adaptive radiation. New York and London: Hafner.

Wight, P.A.L, Burns, R.B., Rothwell, B. and Mackenzie, G.M. 1971. "The harderian gland of the domestic fowl." J. Anat. 110(2):307-315.

Williams, D.L. and Cooper, J.E. 1994. "Horner's syndrome in an African spotted eagle owl (Bubo africanus)." Vet. Rec. 15;134(3):64-66.

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