Frigate birds keep their eyes wide open during flight – most of the time!

Sleep patterns of flying birds

Snap-Shot of the study

Birds fly enormous distances during migratory flight. It seemed reasonable therefore to think that birds sleep while flying, especially since birds can go to sleep -one brain-half at a time.

But then, how can they function and be attentive to the demands of flying, foraging, avoiding predators, finding their route, often over water, over such long periods of time? Imagine the frigate birds with the wind on their wings as they begin their flight across the ocean, flying continuously and majestically for upto 2 months! In an elegant and well written piece of research, the authors find that frigate birds sleep very little during their long flight (1). By recording brain activity in flying birds, the authors show for the first time that these birds take short and light naps but mostly forgo sleep during migratory flight.

Background to this study

A single late night is enough to send most adult humans into a downward spiral the next day, fruit-flies that don’t sleep have their lives cut short (2-4). Birds however have been shown i) to go on long flights without resting (5) ii) to sleep uni-hemispherically – single eye open – keeping one part of the brain alert to the requirements of the environment while the other part rests (6). iii) are able to function more or less normally even when deprived of sleep (7)

So what happens during flight? Given the high energy/metabolic demands of flying the need for rest and sleep must be high, on the other hand the need for attention is also high during flight, can birds afford to sleep on the wing? One way to find out is to record the patterns of brain activity in migratory birds during flight and look for patterns of sleep and wakefulness.

What did they do?

In this study (1), sleep patterns of 15 female great frigate birds flying over the Pacific Ocean and after returning to their nest on Genovesa Island (Galápagos) were recorded using implanted devices that measured brain activity (EEG – electroencephalogram), movement of the head as well as acceleration. No behavioural differences were observed in the birds with implants during and after removal of the devices. Using these devices, the researchers measured movement of the bird, acceleration, deceleration, flapping of the wings and brain activity near the primary visual area and also collected data on weather conditions. Measuring movement of the head allowed them to separate patterns formed by head movement from actual changes in brain activity.

What did they find?

The overall EEG patterns were similar in the birds on land and during flight, allowing the researchers to look at duration and intensity of sleep. They describe three sleep-awake states roughly – wakefulness, rare episodes of REM sleep (like in humans, this is deep sleep characterized by rapid eye movement) and slow wave sleep – this is the most frequent type of sleep described in birds which can be bi-hemispherical or uni-hemispherical or assymetric (6).

During the day, the birds showed patterns of wakefulness (fast head movements together with high amplitude signals in the EEG), even at night during flapping of wings wakefulness patterns were observed. These were interspersed with slow waves which the authors identify as slow wave sleep. Rarely, between bouts of slow wave sleep, short bursts of deep sleep or REM sleep patterns characterized by dropping of the head, and twitching were also observed. Interestingly, birds ascended in altitude during slow wave sleep and descended during wakefulness. All types of slow wave sleep, including unihemsipherical, asymmetrical (when one hemisphere was more active than the other)  and bihemispherical slow wave sleep were observed during flight. There was an increase in asymmetric sleep in flight than on land but this was not correlated with any one type of movement.

Overall, frigate birds seemed to sleep very little during flight – in shorter bursts and less soundly –  a homeostatic balance was restored when these birds landed. Further, preliminary evidence from this study suggests that these bursts of sleep are enough to sustain the birds during flight.

Why is this interesting?

The very fact that these birds are able to accomplish Himalayan tasks such as follow migration routes, feed themselves, with such low levels of sleep suggests that, at least for frigate birds, sleep may be dispensable during flight. Are they postponing this need? What sort of adaptations allow them to postpone sleep or perform sleeplessly? This study is a step towards understanding adaptations to lack of sleep and perhaps a way to understand the very nature of sleep itself.

1. Evidence that birds sleep in mid-flight. Rattenborg NC, Voirin B, Cruz SM, Tisdale R, Dell’Omo G, Lipp HP, Wikelski M, Vyssotski AL. Nat Commun. 2016 Aug 3;7:12468. doi: 10.1038/ncomms12468. PMID: 27485308

2.Reduced sleep in Drosophila Shaker mutants. Nature. 2005 Apr 28;434(7037):1087-92  Cirelli C, Bushey D, Hill S, Huber R, Kreber R, Ganetzky B, Tononi G.

3. Genetics of sleep and sleep disorders. Cell. 2011 Jul 22;146(2):194-207. doi: 10.1016/j.cell.2011.07.004. Sehgal A, Mignot E.

4. http://www.curiouscascade.com/blogpost/clocking/

5. Frigate birds track atmospheric conditions over months-long transoceanic flights. Science. 2016 Jul 1;353(6294):74-8. doi: 10.1126/science.aaf4374. Weimerskirch H, Bishop C, Jeanniard-du-Dot T, Prudor A, Sachs G.

6. Half-awake to the risk of predation Nature 397, 397-398 (4 February 1999) | doi:10.1038/17037 Niels C. Rattenborg, Steven L. Lima & Charles J. Amlaner

7. Adaptive sleep loss in polygynous pectoral sandpipers. Science. 2012 Sep 28;337(6102):1654-8. Epub 2012 Aug 9 Lesku JA, Rattenborg NC, Valcu M, Vyssotski AL, Kuhn S, Kuemmeth F, Heidrich W, Kempenaers B.

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An interview with Alexei Vyssotski

Q. Can you tell us a little more on how you determined that the birds were sleeping? How did you identify the pattern corresponding to sleep when you got all your recordings?

Sleep was identified by visual inspection of 4-sec episodes of raw EEG records. Slow-wave sleep is characterized by large amplitude low-frequency oscillations in EEG. These episodes are easily-detectable. Visual scoring was used because automated methods of sleep staging can’t separate properly large-amplitude EEG events from movement artifacts in all cases. Locomotor artifacts can have similar amplitude to slow-waves during in sleep.

Q. Do you think these birds sleep a lot during an annual cycle? Do migratory birds tend to sleep longer than non-migratory birds on average – there must surely be some compensatory mechanisms?

We have found that frigatebirds sleep on average 9.3 hours per day when on land and only 0.69 hours per day when flying. We did measurements only during breeding period. While the frigatebirds live in equatorial area with relatively small weather seasonal changes, one can suppose that the duration of sleep is linked stronger with the pattern of animal activity than with the time of the year per se. It is known that migratory species can stay on the wing for a long time. Extrapolating our findings to these species one can suppose that they should sleep in the flight smaller amount of time than on land, and might compensate migratory sleep loss on land later like our frigatebirds did. However, the compensatory increase in sleep duration and intensity upon landing after the trip is relatively small comparatively to missed amount of sleep on the wing. One can speak only about partial compensation of sleep loss. The birds have, probably evolutionary formed, an ability to stay without sleep significant amount of time without physiological dysfunctions. Unlike most mammals, the birds do not have so called sleep-deprivation syndrome. If a rat will be forced to stay without a sleep for significant time, it will die, but a homing pigeon can stay month-long awake and still behave properly. Migratory birds definitely reduce amount of sleep during migration, but whether they sleep longer than non-migratory birds in other situations is difficult to say.

Q. Do you think that migratory birds produce neurochemicals that resist the urge to sleep or have special brain structures?

The neurochemistry of avian sleep is investigated in much less extent than mammalian sleep. To the best of my knowledge, no special anatomical structures that are responsible for sleepless in birds have been discovered. It is assumed that the avian sleep control brain system is similar to mammalian. However, additional studies are needed to check how strong this similarity is indeed and what are the differences.

Q. Does the slow sleep wave recordings refer to the activity of only certain regions of the brain?

No. It is assumed that like in mammals, the vigilance states in birds are controlled by deep brain structures that modulate activity of superficial brain regions in a synchronous manner. However, contrary to most of mammals that have only bi-hemispheric sleep, the birds have so- called unilateral sleep, when one hemisphere is sleeping and another is awake. Thus, the avian brain hemispheres are more independent from each other than mammalian. One should note that the phenomenon of “local sleep” has been also discovered in birds. This means that if a particular region of the brain has been used intensively in a wake state, the slow waves of increased amplitude will be observed during the following sleep in this brain area.

Q. Did you have independent recordings of some of the parameters using a high speed camera to set the baseline for each bird?

Do you mean Ca2+ brain cells imaging? No, we did not do this, but of course, if would be nice to monitor how activity of different cells ensembles changes in sleep in birds. The recently developed head-attached microscopes can help to film brain in freely behaving animals.

Q. It is astonishing that you got so much information that you could put together, did you expect that when you captured the 15 birds? What were the unexpected challenges in the study?

That is true, this time we collected more information than in our previous studies. We alreadyhad experience with EEG and GPS logging. This time we compensated luck of GPS precision by the acceleration data to reveal the flight mode of the animal. 3-D acceleration data practically doubled the dataflow, but this was not a problem to log in 1 GB onboard flash memory. We did not predict the particular way of the data analysis in advance, but observing three-modal distribution of sway acceleration leaded us to separate analysis of EEG in three different flight modes (straight flight, circling to the left and to the right). The real challenge was to master the surgery and handling in an animal-friendly way to have the birds back with the equipment. Indeed, the rate of return 14 from 15 birds exceeded our expectations. To be honest, I expected larger losses and was very happy when returns exceeded 50%.

Q. Have you been to the Galapagos? What is it like to do research in that setting? Do you think that nearly 180 years after Darwin’s voyage, the biodiversity of Galapagos still holds new discoveries?

Yes, I have a real luck to spend a week at the Darvin station in Santa Cruz and then a week on Genovesa island working in the bird colony. My colleagues Bryson Voirin and Ryan Tisdale spent two weeks more waiting for birds return. This is the best place for animal study that I have ever seen. Wild birds behave almost like tame animals there and do not run away from humans. Thus, it is easy to handle them. This is, of course, one of the features that attracts biologists. The biodiversity of these islands is definitely not studied completely and will attract scientists for a long time.

Two wings that beat like one

Wing-wing and wing-haltere coordination in insect flight

 

Snap-shot

Even at incredibly high wing beat frequencies, small insects maintain precise control of relative wing movement. A recent study explores how this control is achieved (1).

Background for this work

Flight and mechanism of flight have captured human imagination since time immemorial. Ancient insects had four wings, two of these wings morphed into accessory flight organs, responsible for stability during flight, called halteres (2,3). In dipterans, a class of insects (4), it was the second pair or the hind wings that got modified into halteres.

People have noted for a long time that the two wings (on either side) move precisely in phase, while halteres and wings move anti-phase during flight, (i.e. pair of wings moves antiphase with the pair of halteres). How do insects manage this precise control?

There are at least two ways in which this can be achieved, neuronal connections which would instruct the flight muscles or a mechanical coupling of the wings/halteres themselves. The really fast movement of the wings and halteres in small insects ( about 100Hz or higher, which can be visualized using high speed videography) precludes neurons. If it were neuronal, it would be pretty close to the fastest connectivity known to us.

What did they do and find?

In this work, Deora et al., have examined these phenomena in soldier flies,  dipteran insects with easily tractable (relatively large and white -aiding contrast) halteres. They asked, how are the wings able to beat in unison and how are the halteres maintained so precisely in the opposite phase to wings? The first clues came from serendipitous observations. Dead flies were able to maintain the in-phase and anti-phase relationship of their wing -wing and wing- haltere movements. Suggesting that this connectivity was not a result of neuronal instructions and possibly resulted from mechanical linkages.

The researchers then examined which part of the exoskeleton was maintaining this connectivity by surgically removing different parts of the thoracic exoskeleton. They were able to identify a region on the thorax necessary for the near perfect co-ordination of the wings, when they removed this region, the flies were unable to maintain coordinated wing movements. Interestingly they were able to stick the piece of exoskeleton back again and restore coordinated wing beating. They also identified the region responsible for maintaining mechanical coupling between each wing and it’s haltere (on the same side).

The researchers then tested the nature and limits of this coupling. The decrease in length of wings results in increased frequency of wing beats, how long can the halteres keep up? It seems like the halteres keep up till about the time when the wing is 60% of its original length and then quite suddenly, the coupling between the haltere and wings break down.

Another unknown, which Deora et al., are trying to work out is how this mechanical coupling is switched on during flight and otherwise switched off. This question is posed by behaviours in flies for which only one wing is used. The authors suggest a gearbox and clutch mechanism and attempt to find this clutch that allows the connection of the wings during flight. As yet, the nature, position and exact mechanism of the clutch is not known.

Conclusions from this study

This work shows for the first time that the wing-wing in-phase motion is due to mechanical connections across the sides- left-right axis. The wing-haltere anti-phase relationship is maintained by mechanical connections along the body axis. But how does this mechanical connection maintain a precise phase-angle? This is still not known and remains an active area of investigation.

An interview with Dr. Sanjay Sane

Q. In your work you address the biomechanics of wing-wing coordination and wing-haltere coordination, during flight. What about insects lacking halteres altogether (like dragonflies and damselflies) and insects in which the forewings are modified into halteres?

Excellent question. Insects outside of the Order Diptera lack halteres. The only exception to this is the Order Strepsiptera, in which the forewings have been modified into halteres. In both these cases, halteres are thought to serve the function of gyroscopic sensors which are essential in informing the nervous system about the changes in body orientation during flight. They may also be sensors that provide feedback about timing which is very important for wing motion control. In larger and slower insects such as Dragonflies and damselflies, aerial control is thought to be exquisitely visually driven. Not surprisingly, almost all dragonflies and damselflies operate only under conditions of bright lights. One may ask then: what about insects that are nocturnal but lack halteres (such as moths and antlions), or else insects such as bees which typically operate under bright lights but with very high wing beat frequencies? We have experiments to show that for such insects the antennae serve a role that is similar to halteres. It is not clear presently whether the precise mechanism underlying their sensory function is the same as halteres (i.e. gyroscopic, or timing-related), and that is a major subject of investigation in my lab.

Q. Your work shows a precise control of relative wing angle and haltere angle? Why does this angle matter? Is it just to keep the halteres out of the wing’s path?

Again, an excellent question! It is not clear at all whether the precise control of wing/haltere relative angle matters or is just a results of the physics of coupled oscillators (which wings and halteres seem to be). In some flies, the phase difference is not 180 degrees, so there appears to be nothing sacrosanct about that value. Yet, in a majority of the flies, the phase difference is 180 degrees despite great variation in thoracic morphology – so that cannot be coincidental. What dies matter, as we have shown in the paper, is that whatever the characteristic phase difference is for the given insect, it stay true because the timing information is a crucial feature of the feedback that the haltere provides. Our current hypothesis is that the actual phase difference is just a consequence of the physics of the coupled oscillators that causes their motion to fall into fixed in-phase or out-of-phase modes.

Q. What inspired you to think about mechanical connectivity?

When we observed the maintenance of wing/wing and wing / haltere phase difference in dead flies, it was immediately evident that the nervous system was not involved. The only other possibility was mechanical connectivity – which was fantastic because it answered many other questions that we had about speed and precision.

Q. Tell us more about the clutch? If it is internal , how would you probe it?

Two ways to probe it. One is careful experiments in which we can manipulate individual components of the wing hinge. Not easy, but if we find the right kind of flies in plentiful supply, it may be possible. The second and more direct way is to use X-ray micro-tomography – except this is very difficult and you need to know where to look. Our old-fashioned experiments may help there.

Q. Did you think of using other insects with different wing sizes, instead of manipulating the same insect and making its wings shorter?

Whatever insects we use, we will need internal controls because various aspects of the thorax do not scale isometrically. Manipulating the same insect is a far better option under the circumstances because internal control is then guaranteed.

Q. How does your work impact the way we think about insect flight?

In a major way, I think. For one, it clearly demarcates which aspects of wing and haltere coordination are active vs. passive. This has not been clear at all in previous studies on this topic. The second is that it generates clear and predictive and minimal hypotheses to explain a diverse set of observations (such as bee wing warm-up etc.) in a vast number of insects. It also throws light on how insect flight coped with miniaturization of the body form, which is an important evolutionary question because it appears to underlie the spectacular evolutionary success of insects as a group.

Q. Can you reduce insects to mechanical machines? If yes, does this affect the way you view the world as well as investigate a question?

This is a philosophical question and my answer is going to be speculative. Also, it is a question that applies not only to insects, but to animals in general. I do not think animals can be reduced to mechanical machines, although the way we conduct our science is such that we cannot help but assume some reductionist scenario like that. Our approach is at least as old as and derived from Rene Descartes, who in his brilliant treatise “A discourse on method” argued that all animals are machines (except for humans, of course, because they “possess a soul” unlike the brutes). His ideas were influenced by Newton’s recent discovery of laws of mechanics, and William Harvey’s discovery of heart being merely a mechanical pump, etc. It must have been tempting to think that everything can be explained by laws of mechanics. In later years, this approach has included the function of nervous system which is also essentially driven by the physics of cable theory and electrical conduction and gained currency through Sherrington’s discovery of reflexes and the idea of “a chain of reflexes”. So, add electrical circuits to the mix – but keep the basic idea of a mechanical machine. Where this approach fails however, is that it is unable to explain how animals, including insects, generate new and “spontaneous” activity. If they did not generate spontaneous activity, one imagines a universe in which all animals were essentially fancier versions of wind-up toys – but we know from experience that they are not. How can humans or circus elephants learn to ride bicycles or mice their pin-wheels? How do insects learn to deal with scenarios such as electric shocks which they may have never encountered in their evolutionary history? Surely, the brain is capable of generating novelty activity that ensures that it does not produce simple, copy-book, discrete set of responses to challenges posed by a continuum world.

Q. Humans have historically been interested in all things that fly, with the vested interest of putting ourselves in the sky. Do you have a similar motivation for studying insect flight?

Not particularly. One has to choose one’s battles, and mine has been to understand the nature which is far more sophisticated and fascinating than anything I will be able to build, or have the expertise for. That said, I am in full admiration of anyone who tries to use these concepts for building things that fly. We collaborate with such engineers, and help them as much as we can, and sit back and watch with admiration when they achieve incredible feats of engineering. It makes us appreciate the intricacies of nature even more!

References

1.“Biomechanical basis of wing and haltere coordination in flies.” Tanvi Deora et al., Proc Natl Acad Sci U S A. 2015

2. “The Gyroscopic Mechanism of the Halteres of Diptera”, J. W. S. Pringle, Philosophical Transactions B., 1948

3. “The evolution of insect wings and their sensory apparatus.” Dickinson MH et al., Brain Behav Evol. 1997

4. Classification of Insects from the Royal Entomological Society

5. “The aerodynamics of insect flight.” Sanjay Sane, J Exp Biol. 2003