Taking to the skies

31 October 2016 - By: Caroline Wood

Taking to the skies

Ruddy Shelduck
Ruddy Shelduck - Ku Hai Lake, Qinghai, China Photo: Coke Smith


By Caroline Wood

‘On a wing and a prayer’ is certainly not how birds control their flight patterns, in fact quite the opposite. Research from the recent SEB Meeting in Brighton shows that, whether it’s during foraging, migration or everyday ‘gadding about’, bird physiology is highly tuned to help them to navigate all sorts of environments. Some of these mechanisms are even inspiring new aviation innovations which could be used in drones or other, as yet, unidentified flying objects.

Processing Power

“Bird Brain” might be a derogatory term, but it is now clear that our feathered friends quickly process a great deal of information on the wing. Visual cues in particular are very important to help birds navigate around objects and fly precisely through narrow gaps. However most birds lack the 3D stereoscopic vision that we have- so how do they manage?

Both birds and bees apparently use a system called “optic flow” where they balance the speed that visual cues move across each eye. As Mandyam Srinivasan (University of Queensland, Australia) explains “If you fly a bee or a budgie through a tunnel where the walls are moving forwards, they will speed up so that the flow of visual information continues across their retina at the same speed”. In a tapered tunnel, the image velocity increases as the walls come closer together, hence the birds slow down as the tunnel narrows. 

The eyes have it

Besides regulating speed, birds use optic flow to navigate obstacles in ‘cluttered environments’, showing “exceptional aerodynamic manoeuvring coordinated by rapid processing of visual cues” says Andrew Biewener (Harvard University, United States). He has investigated this using high-speed cameras to film pigeons trained to fly through an indoor environment between two perches. The results demonstrated that pigeons have acute spatial judgement and body awareness when steering around objects. First, they constantly selected the widest gap when confronted with a fast steering decision. Furthermore, they accurately measured the size of the gap in relation to their body and modified their wing behaviour accordingly. When the gap was fairly wide (but not enough to fly straight through), the birds adopted a ‘wing-pause’ strategy, holding their wings in position at the top of the upstroke as they passed through. For narrower gaps however, they folded their wings and tucked them in laterally against their body. Whilst this position gives less aerodynamic control, it reduces the risk of damage if the wing should touch the obstacle. “These results show that pigeons exhibit a remarkable kinaesthetic sense of body and wing position when flying past dense arrays of obstacles” says Andrew.

Mandyam has observed similar wing-behaviour in his budgies. What’s more, he found that these birds increase the trajectory of their flight just before flying through a narrow gap to compensate for the slight loss in altitude as they closed their wings. “There’s a fair amount of elaborate pre-planning going on before they go through these gaps” he says. So robust are these optic flow systems, that Mandyam has since demonstrated that they can be successfully used to automatically pilot small aircraft.  

Stable diet

But visual cues may compete with other senses that are used to maintain position. Hummingbirds hover at flowers to drink nectar and this “sustained hovering is a balancing act that presents both a motor and a sensory challenge,” says PhD student Benjamin Goller (University of British Columbia, Canada). Benjamin and his colleagues have demonstrated that a priority for hummingbirds is to keep their vision stable whilst they hover. As such, they respond to moving background images by moving their body to compensate, even when most of their visual field is stationary1. So how do they process the multitude of visual cues in natural environments while they are feeding? “We hypothesized that feeding hummingbirds would use bill contact with their food source to override their hovering response to moving visual patterns” says Benjamin. To test this, he constructed a specialized feeder; a sugar-filled syringe equipped with four strain gauges to measure how much a feeding hummingbird pushed it in the vertical or horizontal axes. Whilst the birds docked their bill into the syringe to feed, patterns of dots or lines were moved across their background vision. Surprisingly, despite having their bill inserted in the feeder, the hummingbirds still responded to the visual cues, pushing against the feeder depending on the direction the patterns moved. “This shows that hummingbirds attempt to stabilise visual motions even when docked at a rigid nectar source” says Benjamin.

However, this raises further questions including how do hummingbirds control their flight when feeding from flowers whose flexible stems also move? “We are interested in investigating the parts of the brain responsible for processing motion and how these brain regions may limit or explain the behaviours we measure” says Benjamin.

Making the most of it

Given that flight is so strenuous, it can be a fine balance for foraging birds to meet their energy needs. So it is not surprising that many species alter their flight behaviour to make the most of prevailing conditions. “GPS trackers have successfully determined where seabirds forage, yet the finer details regarding flight behaviour have been less well studied” says seabird biologist Philip Collins (University of Roehampton, United Kingdom). “Now, however, by coupling GPS devices with accelerometers we can study in-situ flight behaviour at a sub-second level of detail”. His research has focused on a population of Kittiwakes nesting on Middleton Island, off the Gulf of Alaska. The birds were fitted with accelerometers that recorded acceleration in three axes: heave (up and down), surge (forward and back) and sway (side to side). “The up and down movement allows us to identify individual wingbeats and to work out how often and how hard they are flapping” says Philip. 

Kittiwakes
Kittiwakes. Photo: Phillip Collins


The results showed that Kittiwakes take advantage of the wind speed to reduce the amount of work associated with flight. “When birds have a favourable tailwind they have an overall faster speed, however when we subtract the wind speed, we find that the actual speed of flight down to the bird is lower” says Philip. Curiously, the kittiwakes were found to keep the same flapping rate regardless of the conditions – instead they vary their speed by how hard they flap their wings. So in unfavourable headwinds, the birds fly faster by flapping harder, without changing the rate of flapping.

“These results show that individuals adjust their behaviours in response to different conditions” says Philip. “However, the applicability of these results will likely vary depending on the flight style of the species”. As the Kittiwakes’ flight style includes flapping and gliding, it is currently unknown whether wind conditions similarly affect soaring species, such as albatrosses, or those that flap continuously, including shags and cormorants.

Uplifting behaviour

Meanwhile, other species have learnt how to exploit urban environments during their foraging trips. “We have found that seagulls systematically alter their flight trajectories to utilise the updraught generated by a row of seafront hotels” says Cara Williamson (University of Bristol). 

Cara and her colleagues used laser range-finding binoculars to capture the trajectories and ground speeds of Lesser Black-backed and Herring gulls as they commuted along the seafront of Swansea. A wind profile was generated by releasing a helium balloon and Feeding the data into a Computational Fluid Dynamics Model demonstrated that the gulls use the updraught from the hotels to maintain altitude during gliding, tracking its position as it gained altitude. “This reduces the energy cost of flight when commuting between foraging grounds and the nests,” explains Cara. 

Furthermore, they also used the profile of the buildings to offset the effects of gusts and turbulence. Because the gulls’ speed is dependent on the updraught, on windier days the birds would fly at a greater distance from the hotel, to maintain their optimum speed. “In addition, we found that the angle the gulls’ position themselves at depends on the oncoming wind speed,” says Cara. On more turbulent days, the gulls would fly above the hotels, rather than in front of them. This takes advantage of the quasi-circular geometry of the updraught. As Cara explains “If a gull is subject to a horizontal gust whilst flying at the top of a contour it will move in position but maintain the same air speed. But if it experiences a vertical gust, it will be moved into an adjacent vertical column which will either reduce or increase the gull’s airspeed until it returns to its original position and speed”. This results in a ‘self-regulating’ phenomenon, which returns the gulls to the same position and velocity even if a gust pulls them off course. 

Potentially, these insights could help solve flight problems with unmanned aerial vehicles (UAVs). “UAVs are limited by battery technology and are susceptible to gusting” explains Cara. “Using gulls as inspiration could extend the current range that UAVs can operate within and increase their robustness to gusts”2.

Going up in the world

When it comes to long-distance migrations, birds often don’t have much control over the conditions: they simply have to keep airborne to cover the distance in time. Yet some defy the odds even further by making their journeys at high altitudes where oxygen is much scarcer. 

“At altitudes in excess of 4000m, available oxygen is greatly reduced, therefore birds have to fuel expensive flapping flight with greatly limited resources” says PhD student Nicole Parr (University of Exeter). Despite this, Bar Headed Geese (Anser indicus) make biannual migrations between their breeding grounds in Northern China, Mongolia and Tibet, and their wintering grounds in India, crossing the forbidding Himalayas in the process. They have been recorded flying at over 7,000m and according to one legend they have even been seen flying over Mount Everest. Not surprisingly, these birds have a whole host of physiological adaptations to make the most of any available oxygen. These include a greater density of capillaries in the pectoral muscles, the ability to increase cardiac output up to 5 times and haemoglobin with greater oxygen-carrying capacity. 

For a long time, these exceptional birds were thought to be just that – the exception. However, Nicole’s research has shown that such adaptations to extreme hypoxia may be more widespread. Her focus has been the Ruddy Shelduck (Tadorna ferruginea), a species which migrates between wintering grounds in Myanmar and breeding grounds in Northern China or Mongolia, a distance of over 3,500 km. It was unknown what route they used, until a tracking study investigating the spread of avian influenza H5N1 indicated that the birds crossed the Himalayas3. To investigate this, Nicole followed the progress of 15 Ruddy Shelducks fitted with GPS trackers. “The tags recorded the coordinates and altitude of each duck every 2 hours and the duration of tracking varied between a couple of months to 3 years” says Nicole. 

Her results confirmed that Ruddy Shelducks do indeed cross the Himalayas, and that they are even capable of flying up to 6,800 m high. But why go to such extreme heights, especially when the task is so demanding? It’s thought that the distance saved by taking the direct route, rather than skirting around the mountains, allows the birds to reach their wintering grounds before resources are depleted by other species. 

Meanwhile, this discovery opens up the possibility that other species are also making incredible journeys at high altitude. “Potentially, other species which winter and breed in similar areas of Asia make a comparable flight across the Himalayas, and possibly there are also species which migrate at high altitudes in the Andes of South America” says Nicole. Nevertheless, it remains unknown what physiological adaptations allow Ruddy Shelducks to fly above the mountains. Nicole plans to investigate this by making physiological comparisons – including metabolic rate, muscle histology and haemoglobin- between Ruddy Shelduck and lowland migrant waterfowl. “Ruddy Shelduck are helping to increase our understanding of the diversity of physiological responses to the challenge of high altitude” she concludes.

In for the kill

Yet some species take to the heights for a different reason – to hunt for their next meal. Peregrine falcons are renowned for their remarkable ‘stoops’, where they dive at great speeds from a high altitude to strike their prey. But this carries considerable risk of injury, especially as they often pull out of the stoop just meters above the ground. So how and why did they develop this strategy?

“You often hear anecdotes of peregrines diving down at lightning speeds to hit their prey with an enormous blast that leaves it dead or even beheaded,” says Robin Mills, computational modeller at Charlotte Hemelrijk’s lab (University of Groningen, Netherlands). “But literature records that these events are rare.” In fact, most stoops are only performed at moderate speeds and the prey is slowly crushed to death in the peregrine’s claws. So if the dive doesn’t kill the prey outright, why do peregrines stoop? To investigate this, Robin built a bird-flight simulator. Inputs on reaction time, visual accuracy, steering precision and biomechanical constraints were used to produce a model of falcons hunting a variety of prey species, using data gleaned from peregrines fitted with GPS trackers that were trained to hunt lures attached to model aircraft (collected by the Oxford Flight Group). “After running the simulator over thousands of generations, we can observe which hunters were successful and under what conditions” says Robin. The results have already shown that, without the right guidance and control, high-speed stoops would not be suitable for manoeuvring after sharply-turning prey. “The bones would break and the pectoral muscles would tear if a peregrine decided to spread its wings fully to turn sharply after its prey during a stoop,” says Robin.

Rather, peregrines use a technique called “proportional navigation”, a guidance law used in homing missiles. In simple terms, they adjust their trajectory to intercept the prey at a point ahead of time, avoiding the need for sharp turns. Approaching from above gives the falcon greater control over this finely tuned guidance system. In the simulation, the peregrines evolved different stoop strategies depending on the flight behaviour of the prey species.  “When using proportional navigation in the model, the optimal altitude to initiate a stoop (and so the speed at interception) is higher for more sharply turning prey” says Robin. The faster the peregrine dives, the closer the interception point is to the prey’s current position, limiting its chance to escape. However, controlling a high-speed stoop requires razor-sharp vision and finely-tuned aerodynamic control. “When we allowed for even a small amount of visual error in the model, no high-speed stoops evolved,” says Robin. This may explain why peregrines prefer hunting homing pigeons which fly in a straight line, allowing for slower, shorter stoops. 

“From my model results, I conclude that these impressive high-speed stoops only evolve for the finest of hunters,” says Robin. So don’t be fooled by the dazzling displays of falconers – the exceptions to the rule!

So the next time you watch a flock of birds pass overhead, remember it’s not quite as effortless as it may appear. But understanding how they do it is helping us take our technology to the skies. 

References

1. Goller, Benjamin and D. L. Altshuler. 2014. Hummingbirds control hovering flight by stabilizing visual motion. Proceedings of the National Academy of Sciences USA 111(51): 18375-18380

2. http://www.uva-bits.nl/project/flight-energetics-of-urban-lesser-black-backed-gulls-a-case-study-for-bio-inspired-flightuav-technology/  DOI: 10.1098/rstb.2015.0394

3. Prosser, D. J. et al. Satellite-marked waterfowl reveal migratory connection between H5N1 outbreak areas in China and Mongolia. Ibis (Lond. 1859). 151, 568–576 (2009)

 

  

 

 

 

Category: Animal Biology
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Caroline Wood

Caroline Wood was the SEB’s 2014 science communication intern. Since then, Caroline has been a regular contributor the SEB, reporting on events and writing insightful features for our members.
Caroline has an undergraduate degree from Durham University in Cell Biology and is currently a PHD student at Sheffield University studying parasitic Striga weeds that infect food crops. You can read her blog here.