Designed for Darkness: The Unique Physiology and Anatomy of Owls

Abstract

Owls are the only truly nocturnal avian raptors and have evolved several unique adaptations to perfectly fill this role. For example, their unique large tubular eyes, packed with light-sensitive cells, enable owls to operate in almost total darkness, while their remarkable auditory system allows them to operate in complete darkness. This unique and complex auditory system is a combination of specialised feathers forming a parabolic facial disc, adjustable operculum, or flaps and, in some species, asymmetrical ear openings. This unique system allows the owl’s brain to construct an auditory map of space when locating its prey. As remarkable as it seems, this is tantamount to owls being able to hear in 3D. While there are minor variations in the individual physiology between certain species due to the type of prey they take and the habitat they operate in, all owls are subject to the same unique adaptations in eyes, hearing, head rotation, feather structure, digestive system, and hind limb musculature. In this study, we examine each individual adaptation that combines to make the owl a superbly designed nocturnal predator and also look at some shared mechanisms and behaviour patterns that are crucial to its survival.

1. Introduction

Owls are one of the most distinctive-looking birds in the world. With their upright stance, large head with forward-facing round eyes, flat facial disc and soft fluffy plumage, they cannot be mistaken for anything else. This distinctive outward appearance is the result of many unique evolutionary adaptations, which have enabled the owl to become a highly efficient crepuscular and nocturnal predator. While they share the night skies with insectivorous Caprimulgiformes, such as Nightjars, Frogmouths, Potoos and Oilbirds, and with Owlet-nightjars of Aegotheliformes, the true nocturnal owls are unlike their diurnal raptor counterparts. Whereas the diurnal raptors, consisting of Eagles, Falcons, Hawks, and Buzzards, have separately evolved in response to a wide range of prey species and habitats, the owl is singularly the only true nocturnal raptor. Species of owls are found on every continent and nearly in every country of the world, except Antarctica and some small isolated islands, and can thrive in habitats as diverse as frozen tundra, equatorial rainforests, temperate northern forests, and even open grasslands and deserts.

Owls belong to the taxonomic order of Strigiformes, which is divided into the two families of Strigidae (Typical Owls) and the much smaller family of Tytonidae (Barn, Bay and Grass Owls). While there are some distinct anatomical differences between the two families, most notably in the structure of the skull (Figure 1), both families share the same adaptations that make them owls. There are approximately 250 known species of owl in the world, ranging in size from the diminutive Elf Owl (Micrathene whitneyi) to the enormous Eurasian Eagle Owl (Bubo bubo). While there are minor variations in the individual physiology between certain species due to the type of prey they take and the habitat they operate in, they are all subject to the same unique adaptations in eyes, hearing, head rotation, feathers structure, digestive system, and hind limb musculature.

Recent research has used a genome-wide scan to uncover the genetic and selective mechanisms that are the basis of the owl’s unique sensory adaptations. As predicted, a primary finding of the study was that genes involved in sensory perception showed a genome-wide signal of positive selection. This category included genes involved in acoustic and light perception, photosensitivity, phototransduction, dim-light vision, and the development of the retina and inner ear. Genes involved in circadian rhythms, which regulate the body’s internal clock, also showed evidence of accelerated evolution, as did some genes related to feather production [1].

Figure 1.

Tytonidae—Strigidae skull comparison. L—Barn owl (Tyto alba). R—Little owl (Athene noctua). Photo: Alan Sieradzki.

2. Eyes

Arguably the most distinctive feature of owls is their large forward-facing eyes. Instead of the usual ‘disc’-shaped eyes normally found in birds, owls have developed large ‘tubular’-shaped eyes (Figure 2) that are held tight within the orbit and protected by the scleral ossicles, or ‘sclerotic ring’, composed of a series of small interlocking bones that form a bony ring within the sclera. These ‘tubular’ eyes are so large that in some small species of owl they can take up to 50% of the skull area. Some eagle species have developed ‘tubular’ eyes, but these are much shorter in length than an owl’s, while the majority of diurnal raptors have much smaller ‘globose’ eyes (Figure 3) [2].

Figure 2.

Diagram of an owl’s eye. Image credit: owlpages.com

Figure 3.

Eye orbit comparison nocturnal-diurnal. L—Little owl (Athene noctua). R—Kestrel (Falco tinnuculus). Photo: Alan Sieradzki.

The owl’s large, forward-facing eyes allow for considerable binocular vision, giving an excellent, but a fairly narrow field of view of 110 degrees, with an overlap of approximately 70 degrees (man, by comparison, has a field of view of 180 degrees with an overlap of 140 degrees) [3]. With such a narrow field of view, many species resort to that very distinctive behaviour of owls, head bobbing, to accurately judge distance and position.

The eyes have extremely large cornea (the transparent outer coating of the eye) and pupil (the opening at the centre of the eye). A larger cornea allows for a larger pupil size, which in turn serves to increase the number of photons that reach the retina (light-sensitive tissue on which the image is formed), thereby improving visual sensitivity [4]. The pupil’s size is controlled by the iris (the coloured membrane suspended between the cornea and lens). When the pupil is larger, more light passes through the lens and onto the large retina. Light sensitive retinal cells act as receptors and form images. These receptors are made up of two types of cells, rods and cones; so named for their shapes. Cones distinguish colours, function in bright light, and are needed for sharp resolution, while rods function in low light or at night and are sensitive to movement. Primarily a nocturnal predator, an owl’s eyes are packed with rods, giving owls excellent nocturnal vision without the need of the tapetum, a reflecting layer at the back of the eye found in most nocturnal animals, including those other nocturnal birds, the Caprimulgiformes. While the ambient light on a cloudy, moonless night rarely drops below an illumination level of 0.004-foot candles, experiments have shown that some species, such as Long-eared Owl (Asio otus), Tawny Owl (Strix aluco), and Barn Owl (Tyto alba), can spot and approach prey from a distance of 6 feet or more under illumination as low as 0.000,00073 foot candles [5]. A recent study’s findings indicate that owls may have independently evolved a DNA packaging mechanism in the retina that enhances light channelling in photoreceptors, a feature that has not been observed in any other bird species to date [1].

But an owl’s eyes also contain enough cones to enable it to see perfectly in daylight; owls are by no means blind in the daylight. In fact, with its wide range of pupil adjustment, an owl’s ability to see sharply is as developed as in any diurnal raptor and has allowed many owl species, such as the Burrowing Owl (Athene cunicularia), the Snowy Owl (Bubo scandiacus) and the Short-eared Owl (Asio flammeus), to become highly successful diurnal hunters. To protect their eyes, owls are equipped with three eyelids. They have a normal upper and lower eyelid, the upper closing when the owl blinks (as in humans—the only bird to do so), and the lower closing up for sleep. The third eyelid is called a nictitating membrane, which is a thin layer of tissue that closes diagonally across the eye, from the inside to the outside and cleans and protects the surface of the eye (Figure 4).

Figure 4.

The nictitating membrane of the Eurasian eagle owl (Bubo bubo). Photo: Bruce Marcot.

3. Head rotation

Because of the large size of the ‘tubular’ eyes and the fact that they are locked into place by a sclerotic ring of bone, ocular mobility in owls is virtually non-existent [6]. To compensate for this lack of eye movement, and a fairly narrow field of view, owls have evolved with the ability to laterally swivel the head smoothly and quickly through 270 degrees and vertically 90 degrees. Owls have 14 cervical vertebrae, but so do many other species of bird. Indeed, 14 is about the average number of cervical vertebrae in birds in general (birds can have between 10 and 26 vertical vertebrae depending on species) [7]. All birds have to have the ability to turn their heads through 180 degrees and more for preening. The secret to the owl’s ability to swivel its head smoothly and quickly through 270 degrees in the manner that it does is down to two areas of adaptation. The first adaptation is to the neck itself. Owls have only one occipital articulation with the cervical vertebrae, while the neck is permanently compressed into a loose ‘S’ shape [8]. As with a spring coil, this gives the neck great flexibility. It has also been discovered that there are varying degrees of axial rotation within the individual intervertebral joints [9] and that the combination of yawing and rolling in sections of the cervical spine maximises head rotation [10]. The second adaptation is in the reinforcement of the walls of the oesophagus, trachea, and arteries to withstand the enormous torque involved as the head is turned through so many degrees. Also, it has recently been discovered that in the owl neck, one of the major arteries feeding the brain passes through bony holes in the vertebrae. These hollow cavities are approximately 10 times larger in diameter than the vertebral artery travelling through it. The extra space in the transverse foramina, as the holes surrounding the vertebral arteries, are known, creates a set of cushioning air pockets that allow the artery to move around when twisted. Twelve of the 14 cervical vertebrae in the owl’s neck were found to have this adaptation. Blood vessels at the base of the head, just under the jaw bone, can also act as contractile blood reservoirs, allowing owls to pool blood to meet the energy needs of their large brains and eyes, while they rotate their heads. The supporting vascular network, with its many interconnections and adaptations, helps to minimise any interruption in blood flow [11].

4. Hearing

Owls have a unique, complex and highly developed, and specialised auditory system designed to aid in the location and capture of prey. Most owls use a combination of their remarkable hearing and eyesight to locate and capture their prey. However, some species, such as the Barn Owl (Tyto alba), the Great Grey Owl (Strix nebulosa), the Long-eared Owl (Asio otus) and the Short-eared Owl, can use their unique auditory powers to locate and seize prey invisible to the eye and hidden in thick vegetation or even under a deep covering of snow [12]. The facial plumage of the owl forms a parabolic dish, or facial disc, edged by a ruff, that focuses and enhances sounds received (Figure 5). The ears are located at the sides of the head, behind the eyes, and are covered by the densely packed auricular feathers of the facial disc and ruff (Figure 6). The size and shape of the ear opening vary from species to species, with some species also having either a pre-aural or postaural operculum or flap (Figure 7).

Figure 5.

Perfect facial disc of the great Grey. Owl (Strix nebulosa). Photo: Tony Hisgett. Source: Wiki commons: https://creativecommons.org/licenses/by/2.0/deed.en

Figure 6.

External ear-opening behind the facial disc of a barn owl (Tyto alba). Photo: Alan Sieradzki.

An owl’s range of audible sounds is not unlike that of humans, but its hearing is exceptionally more acute within certain frequencies; particularly at frequencies of 5 kHz and above [13], maximising hunting accuracy with frequencies between 4 and 8 kHz [14]. Some owl species have asymmetrically set ear openings (i.e. one ear is higher than the other). This asymmetry is found in five phyletic lines, represented in the Genera Tyto, Phodilus, Strix, Rhinoptynx, Asio, Pseudoscops, and Aegolius [15]. Ear asymmetry makes the auditory directional sensitivity pattern for high frequencies different in elevation between the two ears. This allows the owl to localise sound in the vertical plane, by comparing the intensity and spectral composition of sound between the two ears. In simple terms, when a noise is heard, the owl can locate its source because of the minute time difference in which the sound is perceived in the left and right ears. This interaural time difference can be as short as 10 millionths of a second [16]. For example, if the sound was to the left of the owl, the left ear would hear it before the right ear. The owl then turns its head until the sound arrives at both ears simultaneously—the prey, even when not visible due to darkness or cover, is now directly in the owl’s line of sight. Even once the prey has been located and the owl has launched an attack, the owl will continue to make minute adjustments of the moveable ruff and flaps until the moment of strike. To understand how this works, research has turned to the area of neurology.

Recent research has discovered that interaural time differences (ITD) are used to localise sounds in azimuth, whereas interaural level differences (ILD) are used to localise sounds in elevation. These two features are processed independently in two separate neural pathways that converge in the external nucleus of the inferior colliculus to form an auditory map of space [17]. The brain constructs the auditory space map by comparing the responses of neurons in the two ears to a sound that stimulates both. The left-right positioning of the sound source is computed from the different arrival times of the sound at each ear [18]. Owls with symmetrical ears must determine the horizontal and the vertical directions of a sound separately, one after the other, by tilting head movements [14], thus making it that little bit more difficult a process to lock on to moving prey. Once the prey has been located and locked on to and the owl has launched itself into the attack, movements of the facial ruff and flaps continue to make minute adjustments throughout the flight path until the moment of impact.

Figure 7.

Operculum of a long-eared owl (Asio otus). Photo credit: Creative commons’—https://creativecommons.org/licenses/by-sa/2.5/deed.en

5. Feathers

Owl feathers are unique in both structure and use. Owls are more heavily feathered than any other bird, even having feathered eyelids and, in many species, feathered feet and toes. In 2017, David H. Johnson (Executive Director of the Global Owl Project) and a small group of volunteers systematically plucked and counted every single feather from the remains of a recently deceased female Great Horned Owl (Bubo virginianus). This painstaking exercise, taking 46 man-hours of work, resulted in a total count of 12,230 feathers. Full details of this feather count exercise are planned to be published shortly [Johnson, D.H. personal communication].

It is, however, the unique structure and form of the wing feathers, allowing the owl almost silent movement through the air, that are the most remarkable. The owls’ near-silent flight can be attributed to three wing feather adaptations unique to owls—(1) a comb-like leading edge to the primary and secondary flight feathers (fimbriae); (2) a fine, wispy, fringe-like trailing edge to the flight feathers (Figure 8); and (3) a velvety covering on the upper surface of the wing and a shiny, down-covered underside [19, 20]. The large wings of these birds, resulting in low wing loading (calculated by the weight of the bird divided by the surface area of both wings) [21], and a low aspect ratio, contribute to noise reduction by allowing extremely slow and buoyant flight. Also, the owl’s wing feathers can separate from each other in flight, allowing the air to flow over each of the individual flight feathers. With all other birds, air rushes over the surface of the wing creating turbulence which, in turn, produces noise. With an owl’s wing, the comb-like serrations on the feather’s leading-edge break down the air into little groups of micro-turbulences. This effectively muffles the sound of the air rushing over the wing surface, which is further dampened by the velvety coating on the wing’s surface and allows the owl to fly silently [22]. A recent study has shown that there is a direct correlation between the size of the facial disc in relation to the length of the comb-like serrations, suggesting that species that rely more on their auditory system for locating prey also have the more silent flight [23]. This also suggests a dual purpose in the need for silent flight, the need for stealth, allowing the owl to approach prey undetected and the need for self-masking, enabling the owl to locate prey by sound while in flight [23]. Such is the effectiveness of the owl’s unique wing feathers for silent flight, that the international aeronautical industry is now investing heavily in the research and development of wing design based on the owl’s fimbriae towards solving the aerodynamic noise of aircraft [24].

Figure 8.

The primary flight feather of the barn owl (Tyto alba) shows the serrated leading edge (fimbriae) and the wispy trailing edge. Photo: Alan Sieradzki.

Other uniquely structured feathers of the owl are their auricular feathers. In almost all owl species, the facial plumage forms a parabolic dish with a facial ruff. The centre of the ruff is formed by tightly packed feathers, with thick rachis and dense webbing. Such feathers are also found on the pre-aural flaps which cover the ear openings, and in the region of the beak. The facial ruff made up of auricular feathers, collect and amplify sounds, and direct them to the ear openings [25]. Three different types of auricular feathers occur in the facial disc of the Barn Owl. One type covers the reflector feathers of the disc and dominates the general appearance of the facial ruff. A similar smaller type of auricular feather is situated at the pre-aural flaps. The third type of auricular feather (semi-bristle) is found in the region of the beak and functions as a mechanoreceptor [26].

6. Digestive system

Owls have evolved to eat their smaller prey whole and unlike other birds, they do not have a crop (Figure 9). This system reduces the owl’s need to drink water, as much of its liquid intake comes directly from the body fluids of its prey. The whole prey is passed head first straight down the oesophagus and into the proventriculus (glandular stomach).

Figure 9.

Juvenile tawny owl (Strix aluco) swallowing rodent prey. Photo: Alan Sieradzki.

Digestion begins in the proventriculus, which produces digestive enzymes and stomach acid. The food mass, along with the digestive enzymes, then passes into the second part of the stomach, the ventriculous or gizzard (muscular stomach) where the chemical digestion started in the proventriculus continues and manual digestion begins. The gizzard uses strong muscular contractions to aid in digestion. The soft and digestible parts of the food are allowed to continue along with the digestive system into the small intestine [27]. The indigestible parts (fur, feathers, claws, bones etc.) are retained in the gizzard and compacted into an oval-shaped pellet (oval due to the gizzard’s shape). The digestion process up to this point takes several hours (Figure 10). The pellet is then passed back into the proventriculus where it will remain for several hours more before finally being regurgitated. Additional digestive enzymes are likely digesting any remaining digestible material during this time [28]. Because the stored pellet partially blocks the owl’s digestive system, new prey cannot be swallowed until this pellet is ejected.

Figure 10.

The digestive system of an owl. Image: Alan Sieradzki.

Regurgitation often signifies that the owl is ready to eat again. When the owl eats more than one prey item within several hours, the various remains are consolidated into one pellet. When the digestive process is finished, the owl will regurgitate the pellet by the process of reverse peristalsis, where smooth muscular contractions push the pellet up the oesophagus and back into the mouth. This process is different from coughing or retching and can prove to be quite strenuous for the owl, especially with larger pellets—this is why an owl will often take on a pained expression when producing a pellet and the reason why owls cannot produce pellets in flight. At the moment of expulsion, the neck is stretched up and forward, the beak is opened, and the pellet simply drops out (Figure 11).

Figure 11.

Owl pellet species comparison. L-R: Tawny owl (Strix aluco) barn owl (Tyto alba), short-eared owl (Asio flammeus). Photo: Alan Sieradzki.

7. Leg and foot musculature

Owls have developed extremely specialised and powerful musculature in their legs and feet. Contrary to the visual image of an owl at rest, owls have relatively long legs; in some species, they can be as much as half the total body length. In flight, the legs are tucked under the body with the toes closed. Once the prey has been located, however, the owl will swoop down on the prey with its head forward and its feet swinging like a pendulum until the last moment before impact when its head is thrown back and its legs stretched out with its talons open. The eight toes are spread, just before contact, into a symmetrical configuration to cover as large an area as possible [3, 13].

Hind limbs of owls are characterised by the absence of some muscles found in other birds. They lack m. iliofemoralis, m. ambiens, both portions of m. flexor cruris lateralis, m. plantaris, and m. fibularis longus [29]. They also have a relatively short tarsometatarsus and the presence of well-developed sesamoids [30] and a specialised tendon locking mechanism [31]. These anomalies in the morphology of the owl’s hind limb are associated with adaptations to catch, seize, keep, and kill the large prey [32]. As the owl’s normal method of dispatching prey is by impact and constriction (a bite to the neck or skull may also be employed with larger prey), the musculature of the feet and toes are exceptionally powerful. Owls generate more force than Hawks and Falcons when closing their talons, which anatomically translates into stronger digit flexor muscles, more robust bones, and stronger tendons with ossification [28]. Owl’s talons are more uniform in size amongst digits, generally less curved, and relatively larger than in diurnal raptors, which probably serve to maintain the reach of the toe for grasping [29].

Owls’ feet have extremely thick pads with very prominent papillae (Figure 12). Unlike other birds, owls have cone-like papillae, free from one another [33]. The most extreme and specialised papillae are found in the fish-eating owls, where the distance between the papillae is comparatively long and the top sharply pointed [33]. These long-pointed papillae or spicules, help the owl to seize slippery fish and other aquatic prey. The dermal layer in the pad is thick and has a dense structure of collagenous fibres. The dermis functions as a base for the papillae and is the structurally firm part of the skin. The important function of the papillae is to penetrate the roughness of the ground, tree branches, or the fur and skin of prey [34].

Owls are anisodactylous, having three toes projecting forward and one toe projecting backwards. However, owls should perhaps be classed as semi-zygodactylous, as the outer toe is ‘hinged’ and can be moved backwards to give the owl’s feet two toes projecting forward and two toes projecting backward configuration (zygodactylous). This configuration is ideal for perching on branches and seizing prey with cylindrical-shaped bodies (as in rodents) and also allows all four digits to maintain comparable locking power [29]. The anisodactyl configuration allows the owl greater stability on flat surfaces, such as nests, or when subduing larger, struggling prey on the ground. This hinged toe mechanism is not unique to owls as it is shared with the Osprey (Pandion haliaetus). The middle toe of the Tytonidae family of owls (Barn, Bay and Grass Owls) have a pectinate talon; a serrated, comb-like flange, used to groom the delicate facial auricular feathers (Figure 12). This is another feature shared with the Osprey (Pandion haliaetus).

Figure 12.

The foot of a barn owl (Tyto alba) shows pads and pectinate talon. Photo: Alan Sieradzki.

8. Variations on a theme

While all owls share these unique adaptations, the evolutionary process of adaptive radiation has produced several variations within the many species [3]. These variations have been influenced by a combination of habitat, prey selection, and activity rhythm (nocturnal, crepuscular, or diurnal).

While all owls share the same ocular morphology, there is a limited variation in iris colour between the various species; either yellow, orange, or black/brown. A recent study has shown that dark eyes are to be found in 71 species belonging to 14 genera, whereas 135 species belonging to 20 genera were classed to have bright eyes (yellow or orange). Dark irises are more frequent amongst strictly nocturnal owls (41 out of 70 nocturnal species [59%]) than amongst owls that have diurnal or crepuscular activity rhythms (37 out of 131 diurnal or crepuscular species [28%]) [35]. The results of the study provided strong support for the existence of an evolutionary correlation between iris colouration and activity rhythm in owls. Beyond that correlation, the study did not find any clear evidence that dark eyes are more likely to evolve in species presenting strictly nocturnal habits than in diurnal species. However, it did find that the most likely explanation for the found patterns would be that dark eyes might be less conspicuous at night and help the owl in avoiding detection by predators or prey.

One of the most distinctive features of the owl is the facial disc (Figure 5). However, two groups of owls, Fish Owls and Fishing Owls, have evolved less defined facial discs (also completely lacking the facial disc ruff); almost to the point of being non-existent in the Fish Owl species. There are four species of Fish Owls, the huge Blakiston’s Fish Owl (Bubo blakistoni), the Brown Fish Owl (Bubo zeylonensis) (Figure 13), the Tawny Fish Owl (Bubo flavipes), and the Malay Fish Owl (Bubo ketupa) while there are three species of Fishing Owl, Pel’s Fishing Owl (Bubo peli), the Rufous Fishing Owl (Bubo ussheri), and the Vermiculated Fishing Owl (Bubo bouvieri). Fish and Fishing Owls have recently been moved from the Genera Ketupa and Scotopelia respectively to the Genus Bubo in the taxonomic listing because of their shared skeletal and phylogenetic characteristics with Eagle Owls [36].

Figure 13.

Brown fish owl (Bubo zeylonensis). Photo: Manojiritty. Source: Creative commons: https://creativecommons.org/licenses/by-sa/4.0/deed.en

Fish Owls and Fishing Owls are nocturnal and crepuscular hunters and generally search for their aquatic prey from rocks or low hanging tree branches close to the water’s edge or wade through the shallow water itself [37]. The less defined facial disc and the lack of the disc ruff (to enhance the acoustic locating of prey) suggest that these characteristics, which are common amongst most other owl species, do not increase the efficiency of hunting aquatic prey visually [37]. As well as lacking the distinctive facial disc found in other owl species, the Fish Owls and the Fishing Owls more or less lack another of the owl’s unique adaptations, the comb-like leading edge of the flight feathers (fimbriae) which contributes towards the silent flight in owls [37, 38].

However, it is not just Fish Owls and Fishing Owls that lack the serrations on the leading edge of the flight feathers. A small number of other owl species also lack or have very much less developed fimbriae. These species tend to be primarily diurnal in their activity rhythm [39] and largely insectivorous; species such as the Little Owl (Athene noctua), Burrowing Owl (Athene cunicularia), Elf Owl (Micrathene whitneyi), and Northern Pygmy Owl (Glaucidium californicum). Fish and Fishing Owls have no tactical need for silent flight because sound does not travel well between air and water, while the diurnal species similarly have little need for silent flight as they are visible to prey. This would suggest that the vastly reduced fimbriae in these birds are an evolutionary holdover that lacks current function [23].

Further variations can be found in the hind limbs of owls. The extent of feathering on the legs and feet of owls varies from an almost bare tarsus and entirely bare toes to densely long-feathered tarsus and toes. The extent of this variation between species is dictated by geographic location and habitat [40]. An example of this would be to compare the sparsely feathered legs and feet of the grasslands and desert-dwelling Burrowing Owl (Figure 14) to the densely feathered legs and feet of the Great Grey Owl of the northern taiga/boreal forests (Figure 15).

Figure 14.

Legs and feet of a burrowing owl (Athene cunicularia arubensis). Photo: Global owl project.

Figure 15.

Densely feathered legs and feet of a great Grey owl (Strix nebulosa). Photo: Jari Peltomäki.

In 1936, American ornithologist Leon Kelso identified and categorised five types of leg and foot feathering amongst owls, associating each type to a variety of Climatic zones [40]:

1. Toes and part of tarsus bare. Tarsus is bare of feathers all the way around for part or all of its length. Toes entirely bare of feathers—associated with the humid, warm environment of the Tropical, Subtropical, and Temperate Zones; example of species: Cuban Bare-legged Owl (Gymnoglaux lawrencii).

2. Toes bare. Tarsus fully feathered and at least half of sides and the upper surface of toes bare of feathers—associated with the humid, warm environment of the Tropical, Subtropical, and Temperate Zones; example of species: Tropical Screech-Owl (Megascops choliba) and Northern Barred Owl (Strix varia georgica).

3. Toes sparsely feathered or bristled. Feathers or bristles somewhat thinly distributed over most of upper surface and sides of toes—well represented in all but the colder zones. In the Tropical, Subtropical, and Temperate Zones this type of feathering is more frequently associated with the arid parts of the zones; example of species: Barn Owl and Eastern Screech Owl (Megascops asio).

4. Toes densely short-feathered. The density of feathering is much greater than in the preceding type, sufficient to hide most of the upper surface of toes from view. Feathers short in comparison to the size of the bird, not tending to conceal part of claws—represented in all the life zones but includes a slightly higher percentage of the owl order in those zones which present a cooler environment, while in zones of greater heat and humidity it constitutes low percentages, example of species: Great Horned Owl (Megascops asio) and Short-eared Owl (Asio flammeus).

5. Toes densely long-feathered. Feathers long in comparison with the size of the bird, tending to conceal part of claws—associated with the colder and less humid environment of the Arctic, Hudsonian, Canadian, and Transition Zones; Example species: Great Grey Owl (Strix nebulosa) and Snowy Owl (Bubo scandiacus) [39].

Extremes in foot feathering in owls seem to be associated with zones that have extremes of climate and humidity. A perfect example of this is the extremely long and dense feathering of the feet of the Snowy Owl, which gives this ground-nesting owl perfect insulation against the cold Arctic climate and the frozen tundra (Figure 16).

Figure 16.

The underside of the densely feathered foot of a snowy owl (Bubo scandiacus). Photo: Roar Solheim.

The long-legged Burrowing Owl, which lives in an arid climate, has extremely sparse feather covering on its legs and feet, with the density of this covering varying between the subspecies. Generally, however, the female usually has a slightly heavier covering of plumaceous feathers on their upper leg than the male; the reason for this possibility is that the female spends more time than the male in the much cooler environment of the burrow chamber during the nesting season. The Burrowing Owl also has an extra adaptation to its hind limbs, giving it a longer step length and potentially faster limb movements for terrestrial locomotion and possibly for digging [41].

9. Shared survival mechanisms and behaviour

While these six unique adaptations combine to make the owl the highly efficient nocturnal predator that it is, the owl also shares several other adaptations and habits which contribute to its survival. Owls have cryptic coloured plumage made up of a mixture of soft browns, greys, black, and white and arranged in subtle markings of streaks and spots which serve to break up the bird’s outline, rendering it almost invisible against its background [42]. Some species, such as the Eagle, Owl, and the Long-eared Owl, also have feathered head adornments (ear, tufts, or horns), which help to break up the distinctive round shape of the owl’s head [43], while some Glaucidium species have developed false eye markings, or an occipital face on the nape of their necks, made visible by the fluffing of the head feathers and tilting the head forward [44] (Figure 17). Studies have shown that these false eye markings are an effective countermeasure against daytime avian mobbing [45]. Overall, the camouflage of owls is incredibly effective against predators, against being mobbed by other birds during the day, and against being spotted by potential prey at night.

Figure 17.

The occipital face of Ridgway’s pygmy owl (Glaucidium ridgwayi). Photo: Bruce Marcot.

Roughly one third of all owl species are subject to colour polymorphism (colour morph), existing in genera, such as Strix, Tyto, Megascops, Otus, Psiloscops, Lophostrix, Glaucidium, and Bubo. The pigment melanin is responsible for many observed cases of colour morph, in which there is a great deal of variation within owls and while there are a number of hypotheses surrounding colour morph, the exact mechanisms which drive these variations remain unresolved [46]. One hypothesis, that apostatic selection drives colour morph in owls, where intraspecific colour variation should be promoted in predators by prey forming an avoidance image for the more common colour morph has been proven highly unlikely [47]. A more likely explanation is the niche variation hypothesis, where the species with broader ecological niches should be more variable compared with those with narrow niches because of the action of disruptive selection [48] and that it is an adaptive character likely maintained by the selective advantage of morphs under different environmental conditions via disruptive selection mechanisms [46].

Climate-related colour morph can be seen in the Eastern Screech Owl where individuals exhibit rufous, intermediate, or grey colouration that is likely caused by relative amounts or concentration of black or rufous melanin subtype (eumelanin and pheomelanin, respectively). This species exhibits clinal variation in morph prevalence; the rufous morph predominates in warm climates while the grey morph dominates in a less humid and colder environment (Figure 18).

Figure 18.

Two colour morphs of the eastern screech owl. (Megascops asio) L – Rufous and R – Grey. Photo: Dick Daniels (http://carolinabirds.org/) https://creativecommons.org/licenses/by-sa/3.0/legalcode

The rufous morph of the Eastern Screech Owl is rarely seen in the northern areas of its range as the mortality rate is greater than that of the grey morph variant in conditions of extreme cold. It is also noted that females of the rufous phase have a greater survival rate in much lower ambient temperatures than their rufous-coloured male counterparts [12]. This greater survival rate in females is probably due to reverse sexual dimorphism (RSD), where the female owl is larger and has more bulk than the male and can capture larger prey.

It can also be hypothesised that colour polymorphism in owls is an adaptive character likely maintained by the selective advantage of camouflage under different light regimes or in terms of physiological adaptation to environmental conditions via disruptive selection mechanisms. Under this hypothesis, climate change could bring about a dramatic change in the colour polymorphism of some northern species. The Tawny Owl (Strix aluco) is a colour polymorphic species with a grey and brown morph resident in the Western Palearctic. Studies in Finland have shown that in winter, the grey phase helps to avoid avian mobbing and predators more efficiently than the brown morph and therefore has a higher survival rate in snowy environments. However, as winters are getting milder and shorter in this species range due to climate change, the selection periods promoting grey colouration may eventually disappear [49].

Although some species of owls are specialist feeders, such as Fish Owls and Fishing Owls, and some have a definite preference for certain prey, such as the Barn Owl and the Short-eared Owl with voles, most owls are fairly generalist feeders, with prey as varied as rodents, birds, amphibians, insects and other invertebrates and, in a few opportunistic cases, even bats [50]. Not too long ago, because of their acknowledged diet of live prey, consisting of small vertebrates and invertebrates, it was widely accepted that owls did not scavenge, and any reported observation of this uncharacteristic behaviour was taken as an anomaly. However, recent studies have shown that carrion feeding by owls may be far more prevalent than once thought. In the past, because of their mostly nocturnal activity, dietary information had come mainly from pellet analysis while any observations of scavenging behaviour in owls have been rare and poorly documented. Today, however, with the increasing use of passive infrared wildlife camera traps, baited with a variety of carcasses, including roadkill, a surprising number of owl species have been recorded engaging in this behaviour in Europe, North America, South America, Asia, and Australia (but none, to date, in Africa) [51].

Species recorded scavenging include Barn Owl (Tyto alba), Eurasian Eagle Owl (Bubo bubo), Tawny Owl (Strix aluco), Great Horned Owl (Bubo virginianus), Snowy Owl Owl (Bubo scandiacus), Ural Owl (Strix uralensis), Powerful Owl (Ninox strenua), Western Screech Owl (Megascops kennicotii), Northern Hawk Owl (Surnia ulula), Long-eared Owl (Asio otus), Little Owl (Athene noctua), and Barred Owl (Strix varia). The recorded carrion ranged from feral pigeon to sheep and deer, and there is even a recorded case of a Brown Fish Owl scavenging on the carcass of a crocodile [52, 53, 54].

Owls hatch their eggs asynchronously as a survival mechanism against prey shortage. Incubation starts with the laying of the first egg, unlike many other birds that begin incubation with the laying of the last egg of the clutch. With asynchronous hatchings separated by anywhere from a few hours to several days, this gives the older nestlings a distinct advantage in begging for food. British ornithologist David Lack identified asynchronous hatching as an evolutionary adaptation to unpredictable changes in the food supply; if food declines abruptly during the nestling period, the youngest nestlings would die first without endangering the survival of the whole brood [55].

A small number of species, such as the Burrowing Owl, Short-eared Owl, Long-eared Owl and the Eurasian Scops Owl have become seasonally migratory [56]. In North America, Northern Burrowing Owls enter primarily in the southern United States from California to western Louisiana, much of Mexico, and scattered sites southward into Central America [57]. While the soft, lightly oiled feathers of owls are not equipped for long flights over large bodies of water, in Europe, the Eurasian Scops Owl crosses the Mediterranean Sea on its long migration south of the Sahara Desert in Africa, while the Long-eared Owl and the Short-eared Owl regularly fly across the North Sea from Northern Europe and Scandinavia to winter in the British Isles where they swell the numbers of resident birds [58].

Snowy Owls make nomadic winter movements and are also subject to irruptions; cyclic events triggered by fluctuations in rodent prey population levels [12]. These irruptions can be on such a large scale after a successful breeding season that huge numbers of young owls spread out from the Arctic Circle into southern Canada, Northeast America, and beyond. Although strong fliers, it seems that Snowy Owls are not averse to seeking any advantage in their dispersal. In October 2001, as many as 60 Snowy Owls boarded a ship near Deception Bay, North Quebec, during a severe gale, while a further three landed on another ship east of Newfoundland. Both vessels were heading for the port of Westerscheldt, on the Belgium/Netherlands border. A number of these owls remained on board for the trans-Atlantic crossing, with one individual eventually making it to Felixstowe in England [59].

Owls hitching a ride on ships is nothing new. In 1903, H.W. Henshaw sighted a Short-eared Owl landing on a ship 500 miles (800 km) northwest of the Hawaiian Islands, while in 1901, W.A. Bryan reported a short-eared owl boarding a steamer which plied between Honolulu and Puget Sound, while it was ‘680 miles off the mainland’ [60]. The British Royal Navy has its own bird watching society, the Royal Navy Bird Watching Society (RNBWS), and since its formation in 1946, the RNBWS has been compiling a database of all birds recorded on British Navy vessels around the world. This database includes the names of the vessels and the geographical positions (longitude & latitude). In 2007, Lt. Cdr. Stan Howe, R.N. very kindly extracted a list of all the owls recorded by the RNBWS around the world from its database for me. There were 242 individual sightings listed, which included species, such as Barn Owl (T. alba), Eurasian Scops Owl (Otus scops), Striated Scops Owl (Otus brucei), Collared Scops Owl (Otus bakkamoena), Great Horned Owl (B. virginianus), Eurasian Eagle Owl (B. bubo), Spotted Eagle Owl (Bubo africanus), Snowy Owl (B. scandiacus), Tawny Owl (S. aluco), Barred Owl (S. varia), African Wood Owl (Strix woodfordii), Northern Hawk Owl (S. ulula), Little Owl (A. noctua), Spotted Owlet (Athene brama), Burrowing Owl (Athene cunicularia), Tenmalm’s/Boreal Owl (Aegoleus funereus), Brown Hawk-owl (Ninox scutulata), Moluccan Hawk-owl (Ninox squamipila), Jungle Hawk-owl (Ninox theomacha), Long-eared Owl (A. otus), Short-eared Owl (Asio flammeus), and Marsh Owl (Asio capensis). The Long-eared Owl (A. otus) and Short-eared Owl (A. flammeus) are the most recorded species and there are a number of unidentified species listed only as ‘Strigidae’. Anyone wishing to access the RNBWS database should visit the RNBWS website: https://www.rnbws.org.uk/science.

With a combination of its six unique adaptations and all these shared survival mechanisms, the owl is indeed one of nature’s cleverest survivors.

Acknowledgements and photo credits

I would like to thank David H. Johnson for allowing me to include the total feather count he and a small group of volunteers painstakingly removed from the remains of a Great Horned Owl (B. virginianus) in 2017 before his own publication on the subject and thank Bruce Marcot and Heimo Mikkola for their helpful editorial comments and valuable input. I would also like to thank the following individuals for their kind permission for the use of their photos and images: Deane Lewis (Figure 2), Bruce Marcot (Figure 4), Jari Peltomäki (Figure 15) and Roar Solheim (Figure 16).