Sleepy birds have ascending lower eyelids

I was looking at the photo of a sleeping female paradise shelduck and then suddenly I noticed that the eye globe was mostly covered by the lower eyelid not by the upper, which is totally opposite to the condition in humans! Then I checked photos of many other birds with closed eyes that I took over the years and most of them had closed eyes covered with lower eyelids. What a finding! Well, it could be well known fact to some, but to me, it was a fresh finding. Then I checked several textbooks and references to confirm my finding. And yes, in most birds, except a few birds such as owls, lower eyelid is bigger and more mobile than the upper counterpart. When they close eyes, depressor palpebrae inferioris muscle, which controls the lower eyelid movement, is relaxed. Whereas in humans and in other mammals, the general rule is that the upper eyelid is more developed than the lower eyelid. When we want to close eyes, we relax upper eyelids, anatomically speaking, levator palpebrae superioris muscle and other associated muscles that elevate upper eyelid are relaxed. Then a more complete closure of eye opening is helped by the contraction of orbicularis oculi muscle. When we are sleepy, we have drooping (upper) eyelids, whereas sleepy birds have ascending (lower) eyelids. It was quite an interesting finding to me.

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Birds have vigilant eyes

While I was searching through the references, it was clear to me that birds have limited number of muscles that control the eyelid movement whereas mammals have more muscles involved not only in palpebral opening or closure but also in facial expression, which is an important tool for communication in social animals. Many birds are gregarious as well, but their communication relies more on verbal signals and whole body cues rather than delicate facial expressions. I reason that the evolutionary path to the body structure designed for efficient flight eliminated or minimized many muscles that are not directly functioning for flying.

And I noticed that many birds mostly maintain their eyes open. Once I videographed a seagull standing on a pedestrian passage. I was holding my iPhone with video-on and approaching to the seagull but at certain distance where the seagull did not feel comfortable, he suddenly flapped its wings and stepped back a little. I was surprised as he was. Both of us moved back. Later I was watching the video and I noticed the seagull was staring at me the wholetime without a blink! Meanwhile I immediately closed my eyes when I was stepping back.

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Contemporary human life does not require constant alertness for a sudden attack from a certain predator. Hence, we rather droop the eyelids to protect eyes when an unexpected thing surprises us whereas a bird fixates its eyes on every potential hazard. Most of the time they maintain their eyes wide open, even when they hit the water for fishing or when they fly through the night. During these activities, their eyes would get harmed by abrasions or desiccation if they don’t have the third eyelid, otherwise known as membrana nictitans or nictitating membrane, which can be transparent or translucent. Fishes, amphibians, reptiles, and avian species have functional nictitating membrane to protect eyes while eyes still receive visual signals from outside. When the nictitating membrane covers the entire eye, a bird looks like a wearing a pair of goggles or contact lenses. In mammals, nictitating membrane is mostly a vestigial organ or merely functions as a gland secreting lubricant.

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Birds can sleep even during flying

Although all sensory information is essential for a bird’s survival, visual information has the utmost importance. The optic nerve (II) is larger than any other cranial nerves. Even during sleeping, they frequently open eyes to check potential nearby threat. They do not sleep for an extended period of time like a dog or a human, their active sleep periods are short and interrupted many times. More interestingly, birds can sleep with one hemisphere while the other is awake, which is called unihemispheric sleep. This physiological phenomenon was described in several bird species and aquatic mammals as well, such as dolphins, porpoises, sea lions, walruses, and one manatee.

In avian species, after optic nerves enter through foramen opticum, they completely cross at the optic chiasm, which means a hemisphere receives the visual signal from the contralateral retina (Whereas in humans, the decussation occurs partially; hence, a hemisphere receives parts of visual signals from both the ipsilateral and contralateral retinas.) So, if a bird engages in unihemispheric sleep with the open right eye, the bird’s left hemisphere is awake while the right side is asleep. This unihemispheric sleep is useful for predator detection. An analysis of electroencephalographic (EEG) recordings from 16 mallards hatched at the lab showed that mallards sleeping at the ends of the row, compared with the ducks in the center, had a 150% increase in unihemispheric sleeping and a preference for keeping the open eye looking in the direction of potential threat, i.e., the direction away from the group (N.C. Rattenborg et al. Behavioural Brain Research. 1999;105:163–172). As the birds at exposed ends perceive greater risk of predation, they had more unihemispheric sleep with one open eye. Meanwhile the ducks in the center flanked by other ducks had biihemispheric sleep with both eyes closed.

This wonderful asymmetric sleep works also during flying. Can you believe birds can sleep while flying without falling down? Many birds make several days, weeks, of months of non-stop flight. Maybe it’s a natural adaptation to the airborne lifestyle. The avian airborne sleeping was demonstrated for the first time in great frigatebirds [Fregata minor) by N.C. Rattenborg et al (Interface Focus 2017;7:20160082). They captured 15 female, great frigatebirds caring for chicks and surgically implanted a sensor to record EEG and attached data loggers on the head for EEG and wings for GPS. After the birds returned and completed the post-flight recovery, data loggers were retrieved from 14 birds.

The average period of the foraging trip was 5.8 days (maximum 10 days), covering 1988 km (maximum 3000 km). In-flight sleep occurred only during soaring and gliding flight. Sleeping time on the wing was quite short compared with the sleeping time on land: 0.7 hour per day during the flight vs. 12.8 hours per day on land. Of course, these numbers are the total time of sleeping. Each episode of sleep lasted at average 12 seconds during the flight, 52 seconds on land. They used more unihemispheric sleeping during the flight than on land. When the bird circled to the left, the left hemisphere slept and vice versa. Authors speculated that the unihemispheric sleeping might be to avoid collisions with their flying peers or to monitor navigational cues or oceanic conditions. More interesting facts discovered in the study were that both hemispheres were asleep time to time and the rapid eye movement (REM) sleep also occurred during flight. It is known that skeletal muscle tone is significantly decreased during REM sleep in humans; however, the accelerometer recordings in the birds showed only dropping of the head and twitching. Episodes of REM sleep lasted at average 4.9 seconds in the air and 5.9 seconds on land.

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Considering the fact that the birds spent half of the days for sleeping on land, their physiological demand for sleeping and resting is quite substantial. Nonetheless, they could forgo sleeping for almost a week or up to ten days when they have a mission for finding food for their chicks! I think this is a great finding we can learn from nature. A strong will to fight for life! Well, of course, different physiologies or ecological pressures have played in diverse living styles of individual species. Therefore, we cannot be like birds. Still and all, I’d like to be like a bird who can withhold sleeping for an extended period when necessary. Otherwise, I can think this way: if I try to complete a work during the night before deadline but I fall asleep without a finished outcome means that the work was not more important than my own physiological needs. Therefore, I should respect my sleepiness. Hehe!

But no bird would drive a car while napping with both hemispheres unless the bird wants to commit suicide or kill other birds! Humans really should learn the unihemispheric sleeping thing from birds!

References

[1] Kaminski J, Waller BM, Diogo R, Hartstone-Rose A, Burrows AM. Evolution of facial muscle anatomy in dogs. Proc Natl Acad Sci U S A. 2019;116(29):14677–14681. doi:10.1073/pnas.1820653116

[2] Jones, M.E.H., Button, D.J., Barrett, P.M. et al. Digital dissection of the head of the rock dove (Columba livia) using contrast-enhanced computed tomography. Zoological Lett 5, 17 (2019). https://doi.org/10.1186/s40851-019-0129-z

[3] Lin LK. Eyelid Anatomy and Function. In Ocular Surface Disease: Cornea, Conjunctiva and Tear Film. Elsevier Inc. 2013. p. 11-15 https://doi.org/10.1016/B978-1-4557-2876-3.00002-X

[4] Kirk N. Gelatt. Essentials of Veterinary Ophthalmology. 3rd Edition. Lippincott Williams & Wilkins; 2000

[5] Konig, Horst E., Korbel, Rudiger, Liebich, Hans-Georg. Avian Anatomy: Textbook and Colour Atlas. 2nd Edition. 5M Publishing Ltd.; 2016

[6] Lehrbuch der Anatomie der Haustiere. Band 5. Anatomie der Vögel. via Google Books

[7] W. Van den Broeck. Histology of Birds. http://www.histology-of-birds.com/galleries.php?id=81&v=2

[8] Rattenborg NC, Lima SL, Amlaner CJ. Facultative control of avian unihemispheric sleep under the risk of predation. Behavioural Brain Research 1999;105:163–72. https://doi.org/10.1016/S0166-4328(99)00070-4.

[9] Rattenborg NC. Sleeping on the wing. Interface Focus 2017;7:20160082. https://doi.org/10.1098/rsfs.2016.0082.