Physiological and Behavioral Adaptations in Migratory Animals

Taymour Elgamal, Trina Fearon, Karim Mustafa

Abstract

Migration is a fascinating phenomenon that occurs in many disparate corners of the animal kingdom. To better understand how it works, its similarities, and its differences in relation to variation across species we have explored eight different examples. The microstructure of the Bean Goose’s feather allows durable and light flight. Canadian geese conserve 10% of their energy, optimize and maintain a better orientation by adopting flight formation. As part of understanding the factors of migratory success, we will look at different modeling of the aerodynamics of pigeons, monarch butterflies and seed dispersal. In the navigation of these migratory species, we will see much overlap with the adaptations they have developed to map their way through their journey. Salmon and sea turtles both use the same magnetoreception mechanism for orientation, and monarchs use a variation that is augmented with the sun and circadian rhythms. The benefit of this research is to shed light on the remarkable solutions that species have adopted and can be used as bioinspiration for future bioengineering projects.

Introduction

Migration is an extremely demanding performance for any species. It requires time, energy, and resources, and wouldn’t be possible without a long line of evolutionary adaptations to optimize travel to a maximal extent. For example, butterflies migrate for 4000km, and while Canadian geese might do less than half of that, they weigh up to 6.5kg. These are incredible expenditures of energy and various species have optimized their techniques to reach their yearly destinations (National Geographic, 2021).

Here, we investigate eight species with unique biomechanical advantages, specifically tailored to their situational challenges. We also investigate the aerodynamics of seed dispersal, which gives us a chance to explore forms of adaptation which have not resulted from locomotion.

We explore only three of countless ways have optimized their advantage in the air. The aerodynamic wings of the Pigeon, the incredible microstructure of the Bean Goose feather and the V-shape formation of Canadian Goose are physical and behavioral adaptations necessary for migrating such lengths. Salmon and sea turtles both use the same magnetoreception mechanism for orientation, and monarchs use a variation that is augmented with the sun and circadian rhythms. Kinetic modeling of monarch and salmon trajectories are extremely insightful to understand their extraordinary adaptations.

The microstructure of bean goose feathers

Fig. 1 “Selection of feather specimens of bean goose Anser fabalis (a) a bean goose in flight, (b) the primary feather of a bean goose, (c) a sample of a feather shaft” by Zou et al. (2020).

The composition of the microstructure of feathers

Flight, from a mechanical perspective, is an enormous challenge for a biological creature, and is “nearly paradoxical” (Lingham-Soliar, 2017). Feathers are extremely light weight but can still withstand from many directions (Lingham-Soliar, 2017). This incredible combination of properties which has allowed the existence of birds for millions of years can only be fully understood by examining the microstructure of feathers.

The bean goose is a migratory bird species, suggesting that its feather microstructure has been even further optimized (Zou et al., 2020). Further investigation of the species can also serve as a template to understand how birds achieve flight. Firstly, its feathers are tough on an elementary level due to beta-keratin, a protein which is tough in itself from forming “beta-sheets, disulfide bridge bonds, and self-assembling into insoluble structures” (Lingham-Soliar, 2014). The rachis or shaft of the feather of the bean goose is the main cylindrical structure, to which is attached to the barbs on either side (Fig. 2). Barbules are found along the barb and are found in a tight knit layout (Fig. 2). The cortex is the outer layer of the rachis, the inner space is called medullary pith and has a foamy quality (Fig. 2) (Lingham-Soliar, 2014).

Fig. 2. “A new microstructural fiber model of feather rachis and barbs and classic engineering analogues” taken by “Microstructural Tissue-Engineering in the Rachis and Barbs of Bird Feathers” by Lingham-Soliar, Theagarten (March 27, 2017).

Form and function of Bean Goose feathers

Fibers in the Bean Goose feather cortex align in a staggering formation (Zou et al.,2020). This organization of fibers wreaks the same benefits we get from staggering bricks: resistance to loads perpendicular to the direction of the fibers is vastly increased. When a force of such is applied on the feather, it is dissipated through the nodes, which is where fibers intersect (Zou et al.,2020). In other words, the weak points of the structure are dispersed to form an even stiffness without any significant vulnerabilities, a feature called a “crack-stopping mechanism” (Lingham-Soliar, 2014). Here, stiffness is distinguished from , and it means that the feather can take on loads and return to its original shape afterwards, whereas strength only refers to how much brute force the structure can handle before cracking and does not consider if a material can bend or not (Zou et al., 2020).  Moreover, the epicortex of the bean goose feather is another contributing structure which is composed of a “cross-fiber section”. As its name suggests, it’s made of overlapping fibers which grant rigidity to the feather. It also protects the rachis and barbs because it is the most outer layer surface of the system (Lingham-Soliar, 2014).

These materials grant stiffness and rigidity but the feather is also flexible. This is due to the medulla pith. It allows gas to flow through the rachis, which in turn allows the rachis to absorb much more energy and release this gas upon impact (Zou et al., 2020). This foamy network completes the cortex and epicortex because it gives the feather some resilience by allowing it to compress and stretch (Lingham-Soliar, 2014). The medulla’s function is just as primordial as those of the cortex and epicortex because the bird can experience many unexpected loads in flight.

Lastly, the lightness of the feather from bean goose comes from the ingenious combination of structures explored above. The medulla pith is least dense yet occupies the most volume in the rachis which is beneficial to the feather (Zou et al., 2020). The cortex and epicortex which are denser are less voluminous. Their main constituent, beta-keratin, is also a light polymer (Zou et al, 2020).

V-Shape formation in Canadian geese

Fig. 3. “Canada Geese V formation”. [Retrieved from Ted. 2010. https://www.flickr.com/photos/frted/5142119589. (Accessed 07/10/2021)]

Flight formation is a phenomenon observed amongst many bird species during migration. It is known that it brings two major benefits to the bird species who use this method: it reduces energetical costs and provides an optical way for birds to communicate (Hummel, 1995). The local Canada Geese depend on this strategy more than many birds, and for various reasons. First, they are one of the heaviest birds to migrate, which means that they require more energy to migrate but will also benefit most from this formation (Badgerow, 1988). They also don’t perform other energy saving tricks observed in other bird species, like gliding and soaring, since they are too large (Badgerow, 1988).

Aerodynamic advantage of flight formation

Although many flight formations are observed, the V-shape is most popular amongst Canadian Geese (Badgerow, 2014). The aerodynamic advantage observed is due to upwash. Wings in flight create an air vortex is created where air flows downwards at the back of the wing and flows upward near the side and back of the wing (Portugal et al., 2014). These are respectively named downwash and upwash. Upwash can be leveraged if another wing is in its field of direction. This is exactly what birds do. Upwash generates more lift and slightly tilts the wing (Hummel, 1995). Generally, in horizontal flight, lift is purely vertical and cancels out the weight of the bird. However, a tilted wing gives a horizontal component to the lift which aids the bird in flying forward. The bird therefore experiences a drag reduction (Hummel, 1995). Drag reduction results in a total reduction in flight power and can be shown by the following equation:

∆N=∆D∙V     (1)

Where  is the power reduction in newtons,  is the drag reduction in newtons and V is the speed in meters per second (Hummel, 1995). Relative power can also be given by the following equation:

E={∆N\over N}  (2)

                                                                                                             

Where E is the percentage of energy reduction, and N is the total energy required in Newtons (Hummel, 1995). Everything is function of “number of wings present in formation” (Hummel, 1995). Therefore, the more wings, the more overall power reduction.

It is also true that energy reduction is most observed when wings of adjacent birds as close to each to each other as possible (Hummel, 1995). It becomes mathematically evident how Canadian geese benefit most from this formation because they migrate in larger flocks (Badgerow, 1988).

For small birds, notable oscillating disturbances are created when they flap their wings because they flap at a much larger angle than large birds. This deters the effect of flight formation for small birds, and conversely, gives a large bird like the Canadian goose an ever-bigger advantage.

Flight formation mastery

Canadian geese save about 10% of their energy by travelling together and use other techniques while in flight formation to ensure that they preserve the most energy possible (Badgerow, 1988). Firstly, it was recorded that despite strong winds they maintain a close distance between one another to maximize flight formation gains. Their large wingspan also allows them to remain close to each other while maintaining a free visual field that isn’t obstructed by the wings of other members. This gives them a communication advantage which saves them time and energy in the long run because they have a better orientation as a group and travel more directly to their destination rather than they would otherwise (Badgerow, 1988).

Pigeons

Birds are one of the most thought of animals when it comes to , since they can travel great distances and their flight as well as the physics behind it has been long studied by scientists.

One of the more interesting examples of birds, is the commonly known rock pigeon or homing pigeons, and how they can return to their loft after having travelled a great distance away. Research suggests that there are two well regarded hypotheses for the navigation of pigeon: olfactory reception and magnetoreception (Mora et al., 2004). Amazingly, magnetoreception was furthered studied by Mora et al. in pigeons and confirms that they can detect magnetic field intensities and navigating accordingly.

In the experience showed on the left, the pigeon had to choose one of the two feeding platforms, located on either side of him, hidden behind a curtain. One of the feeding platforms had an induced magnetic anomaly and the other didn’t. If they chose the right one, they would get fed, if not they would get a time penalty.

After repetitive training, the pigeons where capable of identifying the right feeding platform (the one with the magnetic anomaly) approximately 60 % of the time, witch strongly suggest that they are indeed capable of identifying . And orient themselves accordingly.

Fig. 4. Experimental tunnel used in conditioned choice discrimination of magnetic stimuli. [Retrieved from Mora, C., Davison. et all “Magnetoreception and its trigeminal mediation in the homing pigeon” (Accessed 013/10/2021)]

But magnetoreception is not the only way pigeons can navigate, in fact it has been shown through experimentation that depriving pigeons of olfactory perception by occlusion of the nostril, causes a disturbance of orientation once they are released. And homing pigeon are unable to find their way back to their nest. The result of these experiments suggest that pigeons can associate odorous stimuli carried by the wind to the direction it came from. In other words, if they recognize a familiar sent at the moment of their release, they can orient themselves in the opposite direction from which the odor came from and therefore find their way back to its origin.

Physiological adaptation

Other than the fact that they have hollow bones which allows for flight, pigeon wings are complex biomechanical system that have been optimized for flight. If we look at something as trivial their shape, we can see that the wings are constructed in a way that permits them to utilize fluid mechanics to their advantage to lift off.

Fig. 5. Simplified model of a pigeon air foiled wing structure

If we look at this diagram that depicts a pigeon wing viewed in cross-section, we can see that the shape of the wing permits the air to flow faster on the top of the wing and slower at the bottom of the wing. We know that air is a fluid thereby if we apply Bernoulli principle that states that as the speed of a moving fluid increases its pressure decreases, we can conclude that the pressure applied on the lower end of the wing is much greater than the one applied on the top. This results in an upward force that permits the bird to take off, we call this phenomenon the lift.

But wing shape is not the only parameter in bird’s aerodynamics, feather also play a big role in bird flight. Most birds, including pigeon have some degree of flexibility in the tips of the wings, which allow the feathers to function as an individual aerodynamic surface. A study conducted by: (B Klaassen van Oorschot et al) indicates that that the passive deflection of primary feathers might be an optimizing factor of bird flight. The researcher tested the correlation between feather flexibility and aerodynamic forces in a wind tunnel. They considered and measured: sweep, bend, and twist of the primary feathers. The results showcased that passive deflection of these feathers depend mainly on the attack angle as well as the velocity of the air. It also showcased that different feather deflected air in a different manner. The takeaways from this experience are as follow: first and foremost, bird feathers interact with air in a much more complicated three-dimensional manner than a simple air foil, which could lead to interesting bio inspired wings for example that utilizes passive deflection to its advantage instead of rigid air foil (like planes). And second, this showcases how feather shapes and structures can be adapted to different and therefore be considered a driver of selection when it comes to birds.

Seed dispersal

We have been focused on describing the trend and phenomenon of different animals, but what about ? How can they overcome their fixed life? One of the ways to do is by morphologically adapting to be able to optimize their seed dispersal mechanism depending on the environment they are located in.

Apart from gravity the three most vastly used methods of seed dispersal by plants are anemochory (by wind), hydrochory (by water) and zoochory (by animals). We will look at such a mechanism through the example of a common flower, the dandelion.

Dandelions are the prime example of anemochory due to their very particular structure. The top of the dandelion fruit develops into this parachute like structure called “pappus” that helps disperse the seed using an exterior vector, the wind. Although the pappus acts like a parachute, keeping the seed afloat in the air for longer, there mechanics are quite different. The pappus of the Dandelion does not “capture” air like a parachute, but rather lets the air flow through and around its structure in a way that creates a low-pressure vortex on top of the pappus allowing to hold the seed up and decelerate its descent.

Fig. 6. Dandelion fruit. https://commons.wikimedia.org/wiki/File:Taraxacum_officinale_fruit3_(16375088191).jpg (Accessed 013/10/2021)]
Fig. 7. “How a Vortex Helps a Dandelion Fly.” [Retrieved from J. Gorman and C. Whitworth. 2018. https://www.nytimes.com/video/science/100000006166266/how-a-vortex-helps-dandelions-fly.html. (Accessed 10/10/2021)]
Fig. 8. “Pappus morphing alters seed flight and fluid dynamics.” [Retrieved from 20. Seale, M.; Zhdanov et al., “Informed dispersal of the dandelion” (Accessed 10/10/2021)]

Furthermore, researchers have also discovered that depending on the humidity of the environment the angle of the pappus gets restricted (Figure 8). This restriction results in a smaller vortex which in turn, results in an increase of the falling velocity of the pappus. This mechanism is an interesting example of a physiological adaptation in the dandelion since, humidity is an indication of the presence of water, which is one of the important factors that results in the seed germination.

Other studies were made by students from the university Edinburgh to test the hypothesis that empty space is key to the creation of this low-pressure vortex. To test their hypothesis, they created artificial dandelion seeds constructed from silicon disks containing a lot of empty space. They found out that interaction with the air where very similar and a vortex was indeed created. Understanding the biomechanics behind these dandelion seed could offer new technological advancement, especially in the nano industry.

Monarch Butterflies (Danaus plexippus)

Each year the sky is blanketed by monarch butterflies, (Danaus plexippus), which weigh about one gram, as they fly approximately 4000 km to a small region in central Mexico. This trip not only takes them across the continent of North America, but it also takes them as high as 3000m above sea level (Sridhar et al. 2021).

Flight

To first understand how the monarch completes a flight 80 million times its body length (Sridhar et al. 2021), it is important to know how it flies. The monarch generates propulsion from intermittent flapping at a low frequency of 10 Hz and using its 5cm wings for gliding (Sridhar et al. 2021). Further study into the flight mechanism of butterflies by Johansson et al. has shown that butterflies sustain flight by a clap-like motion during the upstroke, thereby generating a thrust, and support their weight using a lift force that is created during the downstroke. This clap-motion is facilitated by the flexibility of the wings.

At an elevation of 3000m above sea level, lift force plays a key role in monarch migratory success. At such a height, there is a 76% reduction in air density, and by proportionality, a 76% reduction in aerodynamic drag (Sridhar et al. 2021). By studying the kinematics of monarchs in a chamber, Sridhar et al was able to collect information about the butterfly’s fight in different atmospheric conditions. They found that a change in altitude had an insignificant effect on flapping frequency, even when accounting for wing-deformation due to the flexibility of the wings. This is in accordance with the above statement that, while it is the flapping frequency that creates thrust, the lift is associated with the downstroke. Compensation for the low air density would therefore not come from an increased flying speed, but rather a greater force generated.

Navigation

For guidance on this long flight, monarchs use a unique combination of light-sensing and magnetoreception to map their route. The position of the sun works in combination with the insect’s circadian clock to create a time-compensated sun compass (Reppert et al.).  Sunlight scatters, creating a polarization pattern and spectral gradient of skylight, from which monarchs draw directional instructions. Monarchs integrate a form of magnetoreception into their navigation, however, they augment the magnetic information with sun-positioning. (Wan et al. 2021). The time component is relied on as the sun’s position changes throughout the day.

The polarized light is detected in the eye through photoreceptors that express UV-opsin, but it is the antennae that connects the time to the sun’s position. (Sridhar et al. 2021). It is likely also where the magnetic sensing abilities lie, via type 2 cryptochromes. (Wan et al. 2021).

The circadian clock, adjusting position of the sun with time of day, follows the sunrise and sunset. Removing the clock shows disorientation in monarchs. It works by negative-feedback loop during transcription, creating different rhythms in the mRNA and protein levels of clock-related aspects of the bug (Reppert et al.). Photoreceptors that read UV-A/blue light, type 1 cryptochromes (CRY1), synchronize the circadian clock (Wan et al. 2021)

Fig. 9. The annual migratory paths of the Monarch butterfly (Danus plesippus). Image A shows a monarch butterfly in flight, image B shows the South-ward migration to the overwintering destination, and image C shows the Northern return trip of the butterflies. [Adapted from Reppert et al., “Navigational mechanisms of migrating monarch butterflies.”]
Fig. 10. The sequence of motions as the butterfly propels itself up and forwards [Adapted from Johansson et al., “Butterflies fly using efficient propulsive clap mechanism owing to flexible wings.”]

Loggerhead Sea Turtles (Caretta caretta)

Loggerhead sea turtles begin their migration upon hatching on sandy beaches, entering the ocean, where they go on to span entire ocean systems. Throughout their lives they follow internal navigating abilities to coast through gyres, returning to pre-marked feeding, mating, and nesting areas.

Navigation

 A map would be insufficient for the turtle, it needs to know where it is relative to its destination even when swept off course by currents. To help provide the turtle with its position relative to other landmarks on its migratory path, four known elements of the magnetic field are used. After displacing hatchlings to unfamiliar inclination angles, such as ones found on the extremes of gyres, researchers Lohmann and Lohmann noticed visible states of disorientation. The ones placed at the extreme magnetic inclinations corrected their position to the inclinations associated with the safe, central part of the gyres. In addition, the researchers placed the turtles in a water-arena surrounded by a computerized coil system. From their work, four elements of the magnetic field have been identified as positioning information used by the loggerhead. The first element is the angle of inclination, the steepening of field lines as they move to one of the Earth’s poles. It can use the field intensity in two ways, horizontally and vertically. In addition, it can read the intensity of the total field (Lohmann et al. 2008).

Swimming

The rocking of the waves plays a key role in assisting the turtle with its migration. Experiments by Manning et al. with sea turtle hatchlings in wave stimulators has shown that the hatchlings can distinguish between waves with different amplitudes and periods, responding most to the movements mirroring the motion of the waves at their natal beach. The hatchlings follow the circular movement of the wave passing over it, using its inner ear to trace the direction it gets accelerated due to the wave and using this to derive its position with respect to wave propagation direction (Lohmann et al. 1995). Manning et al. subjected hatchlings to combinations of amplitude and period, that when used as parameters equated to the same acceleration. Turtle response to this stimulation showed that they can use kinematic information as insight into the happenings of their surroundings.

Fig. 11. Loggerhead sea turtle movement due to wave propagation [Adapted from Manning et al. “Discrimination of Ocean Wave Features by Hatchling Loggerhead Sea Turtles, Caretta Caretta”]
Fig. 12. Elements of the Earth’s magnetic field read by sea turtles [Adapted from Lohmann et al., “Geomagnetic Navigation and Magnetic Maps in Sea Turtles.”]

Pacific salmon (genus Oncorhynchus)

A salmon’s life is bookended by its migratory activities. The salmonid will follow its magnetoreception instincts, like the loggerhead sea turtle, from its natal ground in freshwater streams to the open seas, where it will spend much of its life (Putnam et al, 2014). To complete its life cycle, it will travel upstream against the current and up waterfalls, to return to its birthplace, spawn, and then die.

Fig. 13. Life and migratory cycle interdependence in Pacific salmon.  [Adapted from Hiroshi Ueda., “Physiological mechanism of homing migration in Pacific salmon from behavioral to molecular biological approaches.”]

Swim speeds

To return to its natal grounds, the mature salmon must travel hundreds of kilometers upstream. During this period of high, continuous activity, the salmon is in a state of fasting and therefore is fully reliant on reserves of fat and other sources of energy. This necessitates finding a balance between energy-efficient (slow, coasting speeds) or hydraulically optimum speeds (fast bursts).

     By focusing on a segment of one migratory path known to be energetically taxing, researchers Hinch and Bratty were able to extract data to model the swim speeds of successful and unsuccessful fish, measured in body lengths/second (BL/s). They found that the successful fish went into periods of bursts less frequently and maintained lower minimum speeds (successful: 5.81 BL/s and unsuccessful: 11.49 BL/s), maximum speeds (successful: 0.07 BL/s and unsuccessful: 1.22 BL/s), and average speeds (successful: 1.85 BL/s and unsuccessful: 4.23 BL/s), thereby saving energy. Those who made it through the pass made use of the reverse-flow paths created by the riverbanks, allowing them to maintain slower speeds while keeping a forward motion.

Another important aspect of salmon locomotion is the jump to overcome waterfalls. Lauritzen et al used a combination of video and modeling the trajectories, via a ballistic model of jumping, to understand the requirements for a successful jump and the implications of brown bear’s presence. The model found that, for a fall of 110-170 cm , a minimum x-distance of 98 cm, jump angle of 66°, and velocity of 507 cms-1. This helps provide insight into success factors. Salmonid jumping from shallow eddies will not have long enough underwater acceleration distances to get to the minimum takeoff velocity, this short acceleration distance explaining its failure to overcome the falls. Most notably, unsuccessful fish often jumped from too far and too slowly, meaning they were never able to meet the parameters necessary to obtain the lowest needed jump height. Interestingly, jumping too high also posed a disadvantage. Beyond wasted energy, it put the fish at more risk of being caught by a bear (average height of caught fish was 52% greater than the mean height for a successful jump). Extrapolating the potential vertical maxima of jumps that ended up with the fish getting caught, as it is more difficult for bears to catch them at a lower heigh. To account for this, salmon studied were found to jump around 17 more often if there were no brown bears. Fish that jumped successfully had little variability in the angle of takeoff, but the fish that failed had a high degree of variability, suggesting that they were confused by the signals in the pool they jumped from.

 Fig. 14. The three trajectories involved in salmon jumps: the shorter dotted line represents predicted jumps, the longer dotted line represents unsuccessful jumps, and solid represents successful jumps [Adapted from Lauritzen et al., “A kinematic examination of wild sockeye salmon jumping up natural waterfall.”]

Clearly from the intensity of swimming and jumping, there is a high energy demand on the salmon. To account for that, metabolic activity is increased to oxidate elevated levels of lipids. The fish respond to constant exercise and fasting by increasing the amount of muscle to oxidize fatty acids. Genetic and metabolic data collected by Morash et al found that dorsal muscle significantly decreased as the salmon went through their migration, while the percentage of protein stayed the same. To complete the spawning migration the oxidation of substrate must meet the energy demands of the swimming salmon. This is supported by the increase of transcript levels for lipid oxidizing proteins increasing by ten times. The success of the salmon heavily hinges upon its ability to oxidize substrates at a rate which meets its energetic demands, as set by muscle tissue. By the time the salmon reaches the spawning stages, these same enzymes are at their lowest levels, which may be due to lower muscle metabolic capacity and protein depletion. 

Conclusion

Navigation and migration are two particularly important aspects of certain animal’s life cycle, and animals have all developed their own unique way of tackling such challenges. From magnetoreception in sea turtles to optimized aerodynamic formation in birds, the goal has been the same, to minimize energy consumption to optimize efficiency. These are merely a few examples of the numerous migratory phenomena in the animal kingdom, phenomenon that offers very promising future bio-inspired engineering product.

References:

  1. Badgerow, John P. “An Analysis of Function in the Formation Flight of Canada Geese.” The Auk 105, no. 4 (October 1988): 749–55. https://doi.org/10.1093/auk/105.4.749.
  2. Cummins, C., Seale, M., Macente, A. et al. A separated vortex ring underlies the flight of the dandelion. Nature 562, 414–418 (2018). https://doi.org/10.1038/s41586-018-0604-
  3. Groth, J. “Monarch Migration Study.” Swallowtail Farms. November 10, 2000. http://www.swallowtailfarms.com/pages/educationalproducts_mms.html. (Accessed 11-10-2021)
  4. Hinch, Scott G, and Jessica Bratty. “Effects of Swim Speed and Activity Pattern on Success of Adult Sockeye Salmon Migration through an Area of Difficult Passage.” Transactions of the American Fisheries Society, vol. 129, no. 2, 2000, pp. 598–606., doi:10.1577/1548-8659(2000)129<0598:EOSSAA>2.0.CO;2.
  5. Hummel, D. “Formation Flight as an Energy -Saving Mechanism.” Israel Journal of Zoology 41, no. 3 (1995): 261–78. https://doi.org/10.1080/00212210.1970.10688779.
  6. Johansson, L. C.; Henningsson, P. Butterflies fly using efficient propulsive clap mechanism owing to flexible wings. Published:20 January 2021. https://doi.org/10.1098/rsif.2020.0854
  7. Klaassen van Oorschot, B.; Choroszucha, R.; Tobalske, B. W. Bioinspiration & Biomimetics. Passive aeroelastic deflection of avian primary feathers. Published 20 July 2020 • © 2020 IOP Publishing Ltd https://iopscience.iop.org/article/10.1088/1748-3190/ab97fd
  8. Lauritzen, D. V, et al. “A Kinematic Examination of Wild Sockeye Salmon Jumping Up Natural Waterfalls.” Journal of Fish Biology, vol. 67, no. 4, 2005, pp. 1010–1020., doi:10.1111/j.0022-1112.2005.00799.x.
  9. Lingham-Soliar, Theagarten. “Microstructural Tissue-Engineering in the Rachis and Barbs of Bird Feathers.” Scientific Reports 7, no. 1 (March 27, 2017): 45162. https://doi.org/10.1038/srep45162.
  10. Lingham-Soliar, Theagarten. “Feather Structure, Biomechanics and Biomimetics: The Incredible Lightness of Being.” Journal of Ornithology 155, no. 2 (April 1, 2014): 323–36. https://doi.org/10.1007/s10336-013-1038-0.
  11. Lohmann, Kenneth J, and Catherine M. F Lohmann. “Geomagnetic Navigation and Magnetic Maps in Sea Turtles.” Navigation, vol. 55, no. 2, 2008, pp. 115–125., doi:10.1002/j.2161-4296.2008.tb00422.x.
  12. Madhu K Sridhar, et al. “Effects of Flight Altitude on the Lift Generation of Monarch Butterflies: From Sea Level to Overwintering Mountain.” Vol. 16, no. 3, 2021, doi:10.1088/1748-3190/abe108.
  13. Manning, E. L, et al. “Discrimination of Ocean Wave Features by Hatchling Loggerhead Sea Turtles, Caretta Caretta.” Marine Biology: International Journal on Life in Oceans and Coastal Waters, vol. 127, no. 4, 1997, pp. 539–544., doi:10.1007/s00227005004
  14. , M., Martin Wild, J. et al. Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432, 508–511 (2004). https://doi.org/10.1038/nature03077
  15. Morash, Andrea J, et al. “Genomic and Metabolic Preparation of Muscle in Sockeye Salmon Oncorhynchus Nerka for Spawning Migration.” Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches, vol. 86, no. 6, 2013, pp. 750–760.
  16. National Geographic. Canada Goose. 2021, from https://www.nationalgeographic.com/animals/birds/facts/canada-goose?loggedin=true (accessed 17/10/2021).
  17. Portugal, Steven J., Tatjana Y. Hubel, Johannes Fritz, Stefanie Heese, Daniela Trobe, Bernhard Voelkl, Stephen Hailes, Alan M. Wilson, and James R. Usherwood. “Upwash Exploitation and Downwash Avoidance by Flap Phasing in Ibis Formation Flight.” Nature 505, no. 7483 (January 1, 2014): 399–402. https://doi.org/10.1038/nature12939.
  18. Putman NF, et al. “An Inherited Magnetic Map Guides Ocean Navigation in Juvenile Pacific Salmon.” Current Biology : Cb, vol. 24, no. 4, 2014, pp. 446–50., doi:10.1016/j.cub.2014.01.017.
  19. Reppert SM, et al. “Navigational Mechanisms of Migrating Monarch Butterflies.” Trends in Neurosciences, vol. 33, no. 9, 2010, pp. 399–406., doi:10.1016/j.tins.2010.04.004.
  20. , O.; Cummins, C.; Kroll, E.; Blatt, M.; Zare-Behtash, H.; Busse, A.; Mastropaolo, E.; Viola, I. M.; Nakayama, N. Informed Dispersal of the Dandelion. bioRxiv 2020, 542696. https://doi.org/10.1101/542696.
  21. Wan G, et al. “Cryptochrome 1 Mediates Light-Dependent Inclination Magnetosensing in Monarch Butterflies.” Nature Communications, vol. 12, no. 1, 2021, pp. 771–771., doi:10.1038/s41467-021-21002-z.
  22. Zou, M., L. Xu, J. Zhou, J. Song, S. Liu, and X. Li. “Microstructure and Compression Resistance of Bean Goose (Anser Fabalis) Feather Shaft.” Microscopy Research and Technique 83, no. 2 (2020): 156–64. https://doi.org/10.1002/jemt.23398.