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.

[/vc_column_text]

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.

A whole new whale

A whole new whale- genetic analysis supports the existence of a new whale species

Snap-shot

In the mysterious dark waters of the deep seas, imaginative explorers have chased mythical creatures – from mermaids to kraken, creating an endless list of adventures. Even in the 21st century, we know very little about the creatures that inhabit these worlds. Now, a shy whale species comes into molecular spotlight as scientists use genetic tools to reveal its existence and decipher its relationship with better known cousins (1).

Background

Public Domain, https://commons.wikimedia.org

The beaked whales are a mysterious and diverse family – characterized by teeth and a prominent beak. Very little is known about this family of whales because they live in remote oceanic habitats, dive deep and seem to be sparse (1, 2). The existence of a black beaked whale is long rumored among Japanese fishermen and was first described as a possible new species by Japanese researchers in 2013 (3). A type of beaked whale known as ‘Baird’s beaked whale’ are seen the north pacific (ranging from Japan to Mexico), these whales are slate-gray in colour. Rare sightings of smaller black whales have also been reported around these regions (only around Japan). Although the black whales are distinguished by their skin tone and smaller size, these criteria alone were not sufficient to to classify them as a new species. One explanation for example could be that the black whales were just the young juveniles of the slate-gray Baird’s beaked whale. A recently published study (1) uses mitochondrial DNA sequencing to show that the black beaked whales are genetically distinct from other beaked whales and are only distantly related to the slate-gray whales with overlapping geographical niches.

What did they do?

The team has analyzed the DNA sequence of a total 178 samples of Baird’s beaked whales. These samples were painstakingly collected  from the rare live animals captured across the entire north pacific range including  two  museum samples. Unsurprisingly, majority of these samples (170) belonged to the slate-gray forms and only 8 belonged to the suspected black whales. They compared the genetic sequence (haplotype https://en.wikipedia.org/wiki/Haplotype) of particular stretches about 450 base pairs (nucleotide lengths) of mitochondrial DNA of these whales. If indeed the 8 black samples belonged to a new species, then their DNA sequence is expected to be quite similar to each other and differ considerably from the slate-gray ones.

What did they find?

Genetic analysis showed that a particular stretch of  mitochondrial DNA from the black and slate-gray whale samples had only 6-7 differences within their own group but differed from each other in 16 positions. This compares with the difference of 12 nucleotides positions that the slate-gray whales have  with a different beaked whale species Arnoux’s beaked whale, a completely  different species found in southern hemisphere (a benchmark for genetic disparity the authors have used to validate the genetic differences-). This analysis in combination with the known physical characteristics of size and colour, positions the rare black whale as a new species. The presence of 6 nucleotide differences in the mitochondrial DNA of the 8 black whales suggests that there may be high diversity within the species as well.

Why is this important?

This work highlights how little we still know about the fascinating world around us. It uses relatively inexpensive, and widely available molecular methods (sequencing short stretches of mitochondrial DNA) to support the claim of a new species of whale in the North Pacific Ocean. This raises new questions about how this species lives and thrives in the remote oceans and how it is affected by human activity.

References

References

1.Morin, Phillip A., C. Scott Baker, Reid S. Brewer, Alexander M. Burdin, Merel L. Dalebout, James P. Dines, Ivan Fedutin, et al. 2016. “Genetic Structure of the Beaked Whale Genus Berardius in the North Pacific, with Genetic Evidence for a New Species.” Marine Mammal Science, July. doi:10.1111/mms.12345.

2. (http://www.beakedwhaleresource.com/aboutbeakedwhales.htm)

3. Kitamura, Shino, Takashi Matsuishi, Tadasu K. Yamada, Yuko Tajima, Hajime Ishikawa, Shinsuke Tanabe, Hajime Nakagawa, Yoshikazu Uni, and Syuiti Abe. 2012. “Two Genetically Distinct Stocks in Baird’s Beaked Whale (Cetacea: Ziphiidae).” Marine Mammal Science, September, doi:10.1111/j.1748-7692.2012.00607.x.

An interview with Dr. Phillip Morin

Q. You have performed analysis on 5 blacks and 8 gray beaked whales, how would you increase sampling? Would you deploy a dedicated team/ facility or co-ordinate more with the fishermen in the area to collect more samples? Does the constraints of sampling limit the interpretation of your finding?

Actually, we have sampled 5 of the new black form, included DNA sequences from the 3 that were previously analyzed in Japan, for a total of 8 of the black form. We included 170 of the gray form in our study, ranging from Japan to Mexico across the North Pacific. We would certainly like to have more samples of the black form, and hope that researchers who have data on additional beached whales that they think may be the black form will contact us, and that researchers, fishermen and others who see live beaked whales can help us to find where they spend their time when they are alive. At the moment we do not have funding to commit to this type of study, but if we are able to get a better idea of where to look for them, that could help us develop a more specific (and less expensive) study. Although the sample size is fairly small, the fact that samples are from both Japan and the Bering Sea strengthens the result, and the fact that we have sampled across the known range of Baird’s beaked whales (the gray ones) also strengthens our interpretation of 2 separate species in the North Pacific.

Q. What do we know about the behaviour of the black whale – are they solitary or social? Are they hunter carnivores or live on krill? Usually food is abundant in the shallow sea near the coast and in deeper sea basins the food becomes scarce, do we know something about their dietary habit that allows them to survive? Is the restriction of their abundance in particular geographical locations is because of a known nutrient gradient around your sampling sites?

There are 22 known species of beaked whales, and to my knowledge all of them live primarily in deep waters and feed on squid and/or fish at depth, and are naturally not abundant, probably due to this dietary specialization, high energy needed to obtain sufficient food, and patchiness of food sources. All are also typically found in smaller groups, though Baird’s beaked whale is known to travel in larger groups of 30 or 40 at times. Although we don’t know anything about the behavior or habits of the new species, we can infer that, like other beaked whales, it feeds at depth on squid or deep/bottom fish, and probably travels in small groups (a few individuals).

Q. Mitochondrial DNA versus genomic DNA for phenotyping – what are the challenges of using complete genomic sequences – What would the advantages of doing complete genome sequencing be?

Genome sequencing remains relatively expensive and requires quite a lot of high-quality DNA. For the purposes of determining whether there are 2 species, short sequences of mitochondrial DNA are actually very diagnostic (and therefore adequate), very inexpensive, and can be generated even from bone specimens in museums. We will very likely do some additional sequencing from the nuclear genome to get a more precise estimate of the amount and timing of divergence among the 3 species in the genus Berardius, but full genome sequencing is unlikely to contribute much in the absence of more information on the biology, life history, behavior, etc. of the species, so that is were we are better off putting our research time and effort.

Q. When do you call something a new species ?Can you tell us a little bit more about how haplotypes are used to infer distance and diversity? What other lines of evidence would further strengthen the black beaked whale as new species?

That’s a difficult question, as evolution is a continuous process, and taxonomy (the process of describing species and higher taxa) is an artificial hierarchy imposed on evolution to help us understand and describe biodiversity. We are using a species concept that infers species when genetic evidence indicates that they are evolving along independent evolutionary trajectories, e.g., they do not significantly interbreed and have not for long enough that they have evolved different ecosystem niches and functions (e.g., different food sources or feeding behaviors, habitat use, mating systems, acoustics, etc.). The mtDNA data strongly suggests that this is the case, as there are only very small differences between haplotypes of individuals within each form (≤5), and much larger differences between haplotypes of the two forms (16-26). The fact that the 2 adult specimens of the black form from which we have measurements are only about 2/3 the size of adult Baird’s beaked whales (far outside the normal size range for adult Baird’s whales), and that they have darker skin and several other recognizable (to experts) physical differences also indicates that they are different species, not just variation within a species.

Q. Do you see yourself as a sort of molecular explorer? How would you go about naming the new black whale?

This study has very much been like molecular exploration! We’ve used genetics to help us identify specimens that were previously identified as Baird’s beaked whales, and then been able to follow up with additional studies on those specimens. We use genetics that way frequently for marine mammals because it is so difficult to study them in their natural habitats. Official naming of the new species is done by publishing a complete description of the species (as complete as the specimens will allow), including some skull morphology if possible, and identification of a type specimen (the “holotype”) that will mostly likely be a skull in the Smithsonian Museum that was collected in 1948, but previously thought to be from a small Baird’s beaked whale. There is a team of researchers from Japan that are currently working on that publication and will most likely propose a scientific name. They were the first to indicate that this might be a new species in 2013 based on the 3 specimens from Japan, so that is why they have taken the lead in describing and naming it.

Q. What are the implications of your findings for whaling and conservation?

Baird’s beaked whales and several other toothed whales and dolphins are still commercially hunted in Japan, so it will be important for the whaling industry and scientists there to monitor the hunts to make sure that the new species, which appears to be much more rare than Baird’s beaked whales, is not taken. There are also other potential human impacts that could endanger this species, including seismic exploration, navy sonar, increasing ocean noise from other sources, pollution, entanglement in fishing gear, competition with humans for food, and climate change. Now that we know it’s there, we can work to learn more about it and, hopefully, how to protect it from these potential impacts